ABSTRACT

Amazonia (defined herein as the Amazon basin) is home to the greatest concentration of biodiversity on Earth, providing unique genetic resources and ecological functions that contribute to ecosystem services globally. The lengthy and complex evolutionary history of this region has produced heterogeneous landscapes and riverscapes at multiple scales, altered the geographic and genetic connections among populations, and impacted rates of adaptation, speciation, and extinction. In turn, ecologically diverse Amazonian biotas promoted further diversification, species coexistence, and coevolution, with biodiversity accumulating over tens of millions of years. Important events in Amazonian history included: (i) late Cretaceous and early Paleogene origin of major rainforest plant and animal groups; (ii) Eocene-Oligocene global cooling with rainforests contracting to tropical latitudes separating Atlantic coastal and Amazonian rainforests; (iii) Miocene uplift of central and northern Andes that separated Pacific coastal and Amazonian rainforests, spurred formation of mega-wetlands in the western Amazon, and contributed to the origin of the modern transcontinental Amazon River; (iv) late Neogene formation of the Panamanian Isthmus that facilitated the Great American Biotic Interchange; (v) Pleistocene climate oscillations followed by late Pleistocene-Holocene human colonization and megafaunal extinctions; and (vi) modern era of widespread anthropogenic deforestation, defaunation, and ecological transformations of regional landscapes and global climates. Amazonian conservation requires decade-scale investments into biodiversity documentation and monitoring to leverage existing scientific capacity, and strategic habitat planning to allow continuity of evolutionary and ecological processes now and into the future.

KEYWORDS:
biogeography; conservation; extinction; Neotropics; speciation

RESUMEN

La Amazonía (definida como la cuenca amazónica) concentra la mayor biodiversidad de la Tierra, proporcionando recursos genéticos y funciones ecológicas únicas que contribuyen a los servicios ecosistémicos a nivel mundial. La compleja historia evolutiva de esta región produjo paisajes heterogéneos a múltiples escalas geográficas, alteró las conexiones geográficas y genéticas entre las poblaciones e influyó en las tasas de adaptación, especiación y extinción. Las biotas amazónicas, ecológicamente diversas, promovieron una mayor diversificación, coexistencia de especies y coevolución, acumulando biodiversidad a lo largo de decenas de millones de años. Acontecimientos importantes en la historia de la Amazonía incluyeron: (i) orígenes durante el Cretácico tardío y el Paleógeno temprano de los principales grupos de plantas y animales; (ii) enfriamiento global del Eoceno-Oligoceno, contrayendo los bosques a latitudes tropicales y separando los de la costa Atlántica de los amazónicos; (iii) levantamiento de los Andes centrales y del norte en el Mioceno, separando las selvas tropicales de la costa del Pacífico y de la Amazonía, estimulando la formación de megahumedales en la Amazonía occidental y contribuyendo al origen del moderno Río Amazonas transcontinental; (iv) formación del istmo de Panamá durante el Neógeno tardío, facilitando el Gran Intercambio Biótico Americano; (v) oscilaciones climáticas del Pleistoceno seguidas por la colonización humana y las extinciones de megafauna; (vi) era moderna de deforestación antropogénica generalizada, defaunación y transformaciones ecológicas de paisajes regionales y climas globales. La conservación de la Amazonía requiere inversiones por décadas en la documentación y el seguimiento de la biodiversidad para impulsar la capacidad científica existente, así como la planificación estratégica del hábitat para permitir la continuidad de los actuales y futuros procesos evolutivos y ecológicos.

PALABRAS CLAVE:
biogeografía; conservación; extinción; Neotrópico; especiación

INTRODUCTION

This review was originally developed as Chapter 2 of the Science Panel for the Amazon Assessment Report (https://www.theamazonwewant.org/) (Guayasamin et al. 2021Guayasamin, J.M.; Ribas, C.C.; Carnaval, A.C.; Carrillo, J.D.; Hoorn, C.; Lohmann, L.G.; et al. 2021. Chapter 2: Evolution of Amazonian Biodiversity. In: Nobre, C.; Encalada, A.; Anderson, E.; Roca Alcazar, F.H.; Bustamante, M.; Mena, C.; et al. (Ed.). Amazon Assessment Report 2021. United Nations Sustainable Development Solutions Network, New York, USA. (https://www.theamazonwewant.org/spa-reports/). doi: 10.55161/CZWN4679
https://www.theamazonwewant.org/spa-repo... ). The report aimed to scientifically assess the current state of the Amazon, and to identify and explore opportunities for relevant policy actions. We focused our review on the following main themes: (i) Amazonian biodiversity, (ii) evolution of Amazonian forests, (iii) assembling of Amazonian biota, (iv) species loss and turnover, and (v) conservation of ecological and evolutionary processes. Broad accessibility to this information is at the core of disseminating the knowledge and understanding the complexity of the Amazon basin and the urgency for conservation actions.

AMAZONIAN BIODIVERSITY IS IMMENSE AND VASTLY UNDERESTIMATED

The Amazon basin (Figure 1) houses one of the highest organismal and ecosystemic diversity on Earth (Bass et al. 2010Bass, M.S.; Finer, M.; Jenkins, C.N.; Kreft, H.; Cisneros-Heredia, D.F.; McCracken, S.F.; et al. 2010. Global conservation significance of Ecuador’s Yasuní National Park. PLoS One 5: e8767.; Levêque et al. 2007Levêque, C.; Oberdorff, T.; Paugy, D.; Stiassny, M.L.J.; Tedesco, P.A. 2007. Global diversity of fish (Pisces) in freshwater. Freshwater Animal Diversity Assessment 595:545-567). Approximately 10% of the world’s vertebrate and plant species are contained in an area that corresponds to approximately 0.5% of the Earth’s total surface (Jetz et al. 2012Jetz, W.; Thomas, G.H.; Joy, J.B.; Hartmann, K.; Mooers, A.O.2012. The global diversity of birds in space and time. Nature 491: 444-448.; Tedesco et al. 2017Tedesco, P.A.; Beauchard, O.; Bigorne, R.; Blanchet, S.; Buisson, L.; Conti, L.; et al. 2017. A global database on freshwater fish species occurrence in drainage basins. Scientific Data 4: 170141.; ter Steege et al. 2020ter-Steege, H.; Prado, P.I.; Lima, R.A.F. de; Pos, E.; de Souza, L.; Lima, D.A.; et al. 2020. Biased-corrected richness estimates for the Amazonian tree flora. Scientific Reports 10: 10130.; Figure 2). Amazonian diversity also represents a bewildering range of life forms, ecological functions, chemical compounds, and genetic resources (Darst et al. 2006Darst, C.R.; Cummings, M.E.; Cannatella, D.C. 2006. A mechanism for diversity in warning signals: Conspicuousness versus toxicity in poison frogs. Proceedings of the Natural Academy of Sciences 103: 5852-5827.; Asner et al. 2014Asner, G.P.; Martin, R.E.; Tupayachi, R.; Anderson, C.B.; Sinca, F.; Carranza-Jiménez, L.; Martinez, P. 2014. Amazonian functional diversity from forest canopy chemical assembly. Proceedings of the Natural Academy of Sciences 111: 5604-5609.; Albert et al. 2020Albert, J.S.; Tagliacollo, V.A.; Dagosta, F. 2020a. Diversification of Neotropical freshwater fishes. Annual Review of Ecology Evolution and Systematics 51: 27-53.a; Figure 3). The highly diverse Amazonian ecosystems constitute the core of the Neotropical realm, which harbors about 30% of all species of vascular plants (Raven et al. 2020Raven, P.H.; Gereau, R.E.; Phillipson, P.B.; Chatelain, C.; Jenkins, C.N.; Ulloa, C.U.2020. The distribution of biodiversity richness in the tropics. Science Advances 6: eabc6228.), vertebrates (Jenkins et al. 2013Jenkins, C.N.; Pimm, S.L.; Joppa, L.N. 2013. Global patterns of terrestrial vertebrate diversity and conservation. Proceedings of the Natural Academy of Sciences 110: E2602--E2610.; Reis et al. 2016Reis, R.E.; Albert, J.S.; Dario, F. Di; Mincarone, M.M.; Petry, P.; Rocha, L.A.2016. Fish biodiversity and conservation in South America. Journal of Fish Biology 89: 12-47.), and arthropods (Stork 2018Stork, N.E. 2018. How many species of insects and other terrestrial arthropods are there on Earth? Annual Review of Entomology 63: 31-45.) on Earth.

Despite decades of intensive study, the full dimensions of Amazonian diversity still remain vastly underestimated (da Silva et al. 2005Silva, J.M.C. Da.; Rylands, A.B.; Fonseca, G.A.B. Da. 2005. The fate of the Amazonian Areas of Endemism. Conservation Biology 19: 689-694.; Barrowclough et al. 2016Barrowclough, G.F.; Cracraft, J.; Klicka, J.; Zink, R.M. 2016. How many kinds of birds are there and why does it matter? PLoS One 11: e0166307.; García-Robledo et al. 2020García‐Robledo, C.; Kuprewicz, E.K.; Baer, C.S.; Clifton, E.; Hérnandez, G.G.; Wagner, D.L. 2020. The Erwin equation of biodiversity: From little steps to quantum leaps in the discovery of tropical insect diversity. Biotropica 52: 590-597.). Critical information is lacking in all main biodiversity levels (see Hortal et al. 2015): taxonomic diversity (Linnaean shortfall), biogeographic distributions (Wallacean shortfall), species abundances (Prestonian shortfall), phylogenetic diversity (Darwinian shortfall), species traits (Raunkiæran shortfall), and species interactions (Eltonian shortfall). This knowledge shortfall arises from the extremely high number of species found in the region (Magurran and McGill 2011Magurran, A.E.; McGill, B.J. 2011. Biological Diversity: Frontiers in Measurement and Assessment. Oxford University Press, Oxford, 345p.; Raven et al. 2020Raven, P.H.; Gereau, R.E.; Phillipson, P.B.; Chatelain, C.; Jenkins, C.N.; Ulloa, C.U.2020. The distribution of biodiversity richness in the tropics. Science Advances 6: eabc6228.), the numerous species yet unrecognized due to the so called cryptic biodiversity (i.e., several species undescribed because they share a similar morphology) (Angulo and Icochea 2010Angulo, A.; Icochea, J. 2010. Cryptic species complexes, widespread species and conservation: lessons from Amazonian frogs of the Leptodactylus marmoratus group (Anura: Leptodactylidae). Systematics and Biodiversity 8: 357-370.; Benzaquem et al. 2015Benzaquem, D.C.; Oliveira, C.; Silva Batista, J. da; Zuanon, J.; Rebelo Porto, J.I. 2015. DNA barcoding in pencilfishes (Lebiasinidae: Nannostomus) reveals cryptic diversity across the Brazilian Amazon. PLoS One 10: e0112217.; Draper et al. 2020Draper, F.C.; Baker, T.R.; Baraloto, C.; Chave, J.; Costa, F.; Martin, R.E.; Pennington, T.R.; Vicentini, A.; Asner, G.P. 2020. Quantifying tropical plant diversity requires an integrated technological approach. Trends in Ecology & Evolution 35: 1100-1109.; Jaramillo et al. 2020Jaramillo, A.F.; La Riva, I. De; Guayasamin, J.M.; Chaparro, J.C.; Gagliardi-Urrutia, G.; Gutiérrez, R.C.; Brcko, I.; Vilá, C.; Castroviejo-Fisher, S. 2020. Vastly underestimated species richness of Amazonian salamanders (Plethodontidae: Bolitoglossa) and implications about plethodontid diversification. Molecular Phylogenetics and Evolution 149: 106841.), the logistical difficulties with sampling in remote and inaccessible regions (Cardoso et al. 2017Cardoso, D.; Särkinen, T.; Alexander, S.; Amorim, A.M.; Bittrich, V.; Celis, M.; et al. 2017. Amazon plant diversity revealed by a taxonomically verified species list. Proceedings of the Natural Academy of Sciences 114: 10695-10700.; ter Steege et al. 2020ter-Steege, H.; Prado, P.I.; Lima, R.A.F. de; Pos, E.; de Souza, L.; Lima, D.A.; et al. 2020. Biased-corrected richness estimates for the Amazonian tree flora. Scientific Reports 10: 10130.), collection efforts that are biased towards accessible localities (Nelson et al. 1990Nelson, B.W.; Ferreira, C.A.C.; Silva, M.F. da; Kawasaki, M.L. 1990. Endemism centres, refugia and botanical collection density in Brazilian Amazonia. Nature 345: 714-716.; Hopkins 2007Hopkins, M.J.G. 2007. Modelling the known and unknown plant biodiversity of the Amazon Basin. Journal of Biogeography34: 1400-1411.; Loiselle et al. 2008Loiselle, B.A.; Jørgensen, P.M.; Consiglio, T.; Jiménez, I.; Blake, J.G.; Lohmann, L.G.; Montiel, O.M. 2008. Predicting species distributions from herbarium collections: does climate bias in collection sampling influence model outcomes? Journal of Biogeography 35: 105-116.), and a disproportionate number of studies applied to conspicuous organisms (Ritter et al. 2020Ritter, C.D.; Dunthorn, M.; Anslan, S.; de Lima, V.X.; Tedersoo, L.; Nilsson, R.H.; Antonelli, A.2020. Advancing biodiversity assessments with environmental DNA: Long-read technologies help reveal the drivers of Amazonian fungal diversity. Ecology and Evolution 10: 7509-7524.) and broadly distributed species (Ruokolainen et al. 2002Ruokolainen, K.; Tuomisto, H.; Vormisto, J.; Pitman, N. 2002. Two biases in estimating range Sizes of Amazonian plant species. Journal of Tropical Ecology 18: 935-942.). As a result, many Amazonian species have never been collected, named, or studied; and often an entire group of closely related species (i.e., clade) is mistakenly treated as a single species (Albert et al. 2020Albert, J.S.; Destouni, G.; Duke-Sylvester, S.M.; Magurran, A.E.; Oberdorff, T.; Reis, R.E.; Winemiller, K.O.; Ripple, W.J. 2020b. Scientists’ warning to humanity on the freshwater biodiversity crisis. Ambio 50: 85-94.b).

To fill this gap, integrated studies of Amazonian taxa conducted over the past two decades have employed a combination of molecular and morphological tools that allow scientists to recognize cryptic species of plants (Damasco et al. 2019Damasco, G.; Daly, D.C.; Vicentini, A.; Fine, P.V.A. 2019. Reestablishment of Protium cordatum (Burseraceae) based on integrative taxonomy. Taxon 68: 34-46.; Francisco and Lohmann 2020Francisco, J.N.; Lohmann, L.G. 2020. Phylogeny and Biogeography of the Amazonian Pachyptera (Bignonieae, Bignoniaceae). Systematic Botany 45: 361-374.), birds (Ribas et al. 2012Ribas, C.C.; Aleixo, A.; Nogueira, A.C.R.; Miyaki, C.Y.; Cracraft, J.2012. A palaeobiogeographic model for biotic diversification within Amazonia over the past three million years. Proceedings of the Royal Society Series B Biological Sciences 279: 681-689.; Whitney and Cohn-Haft 2013Whitney, B.M.; Cohn-Haft, M. 2013. Fifteen new species of Amazonian birds. In: Del Hoyo, J.; Elliot, A.; Sargatal, J.; Christie, D.A. (Ed.). Handbook of the Birds of the World. Special volume: New Species and Global Index, Lynx Ediciones, Barcelona, p.225-239.; Thom and Aleixo 2015Thom, G.; Aleixo, A. 2015. Cryptic speciation in the white-shouldered antshrike (Thamnophilus aethiops, Aves--Thamnophilidae): The tale of a transcontinental radiation across rivers in lowland Amazonia and the northeastern Atlantic Forest. Molecular Phylogenetics and Evolution 82: 95-110.; Schultz et al. 2017Schultz, E.D.; Burney, C.W.; Brumfield, R.T.; Polo, E.M.; Cracraft, J.; Ribas, C.C. 2017. Systematics and biogeography of the Automolus infuscatus complex (Aves; Furnariidae): Cryptic diversity reveals western Amazonia as the origin of a transcontinental radiation. Molecular Phylogenetics and Evolution 107: 503-515., 2019Schultz, E.D.; Pérez-Emán, J.; Aleixo, A.; Miyaki, C.Y.; Brumfield, R.T.; Cracraft, J.; Ribas, C.C. 2019. Diversification history in the Dendrocincla fuliginosa complex (Aves: Dendrocolaptidae): insights from broad geographic sampling. Molecular Phylogenetics and Evolution 140: 106581.), amphibians (Gehara et al. 2014Gehara, M.; Crawford, A.J.; Orrico, V.G.D.; Rodríguez, A.; Lötters, S.; Fouquet, A.; et al. 2014. High levels of diversity uncovered in a widespread nominal taxon: continental phylogeography of the Neotropical tree frog Dendropsophus minutus. PLoS One 9: e103958. ; Jaramillo et al. 2020Jaramillo, A.F.; La Riva, I. De; Guayasamin, J.M.; Chaparro, J.C.; Gagliardi-Urrutia, G.; Gutiérrez, R.C.; Brcko, I.; Vilá, C.; Castroviejo-Fisher, S. 2020. Vastly underestimated species richness of Amazonian salamanders (Plethodontidae: Bolitoglossa) and implications about plethodontid diversification. Molecular Phylogenetics and Evolution 149: 106841.; Vacher et al. 2020Vacher, J.; Chave, J.; Ficetola, F.G.; Sommeria-klein, G.; Tao, S.; Thébaud, C.; et al. 2020. Large‐scale DNA‐based survey of frogs in Amazonia suggests a vast underestimation of species richness and endemism. Journal of Biogeography 47: 1781-1791.), fishes (Melo et al. 2016Melo, B.F.; Ochoa, L.E.; Vari, R.P.; Oliveira, C. 2016. Cryptic species in the Neotropical fish genus Curimatopsis (Teleostei, Characiformes). Zoologica Scripta 45: 650-658.; Craig et al. 2017Craig, J.M.; Crampton, W.G.R.; Albert, J.S. 2017. Revision of the polytypic electric fish Gymnotus carapo (Gymnotiformes, Teleostei), with descriptions of seven subspecies. Zootaxa 4318: 401-438.; García-Melo et al. 2019García-Melo, J.E.; Oliveira, C.; Costa Silva, G.J. Da; Ochoa-Orrego, L.E.; Pereira, L.H.G.; Maldonado-Ocampo, J.A. 2019. Species delimitation of neotropical characins (Stevardiinae): Implications for taxonomy of complex groups (Z Peng, Ed). PLoS One 14: e0216786.), and primates (Lynch Alfaro et al. 2015Lynch Alfaro, J.W.; Boubli, J.P.; Paim, F.P.; Ribas, C.C.; da Silva, M.N.F.; Messias, M.R.; et al. 2015. Biogeography of squirrel monkeys (genus Saimiri): South-central Amazon origin and rapid pan-Amazonian diversification of a lowland primate. Molecular Phylogenetics and Evolution 82: 436-454.). Between 1999 and 2015, many new species of plants (1,155 species), fishes (468), amphibians (321), reptiles (112), birds (79), and mammals (65) were described from the Amazon Basin (WWF 2016WWF. 2016. Living planet: Report 2016: Risk and resilience in a new era. World Wildlife Fund, Gland, 74p. (https://c402277.ssl.cf1.rackcdn.com/publications/964/files/original/lpr_living_planet_report_2016.pdf?1477582118&_ga=1.148678772.2122160181.1464121326).
https://c402277.ssl.cf1.rackcdn.com/publ... ).

Spectacular Amazonian species continue to be described. They include, for instance, a new critically endangered titi monkey (Plecturocebus grovesiBoubli et al. 2019Boubli, J.P.; Byrne, H.; da Silva, M.N.F.; Silva-Júnior, J.; Costa Araújo, R.; Bertuol, F.; et al. 2019. On a new species of titi monkey (Primates: Pecturocebus Byrne et al., 2016), from Alta Floresta, southern Amazon, Brazil. Molecular Phylogenetics and Evolution 132: 117-137.; Byrne et al. 2016Byrne, H.; Rylands, A.B.; Carneiro, J.C.; Lynch Alfaram, J.W.; Bertuol, F; da Silva, M.N.F.; et al.2016. Phylogenetic relationships of the New World titi monkeys (Callicebus): First appraisal of taxonomy based on molecular evidence. Frontiers in Zoology 13: 10. doi.org/10.1186/s12983-016-0142-4
https://doi.org/10.1186/s12983-016-0142-... ), 15 new species of Amazonian birds described in a single publication (Whitney and Cohn-Haft 2013Whitney, B.M.; Cohn-Haft, M. 2013. Fifteen new species of Amazonian birds. In: Del Hoyo, J.; Elliot, A.; Sargatal, J.; Christie, D.A. (Ed.). Handbook of the Birds of the World. Special volume: New Species and Global Index, Lynx Ediciones, Barcelona, p.225-239.), 44 new species of lungless Bolitoglossa salamanders that await formal description (Jaramillo et al. 2020Jaramillo, A.F.; La Riva, I. De; Guayasamin, J.M.; Chaparro, J.C.; Gagliardi-Urrutia, G.; Gutiérrez, R.C.; Brcko, I.; Vilá, C.; Castroviejo-Fisher, S. 2020. Vastly underestimated species richness of Amazonian salamanders (Plethodontidae: Bolitoglossa) and implications about plethodontid diversification. Molecular Phylogenetics and Evolution 149: 106841.), a distinctive new and critically endangered vanilla orchid (Vanilla denshikoiraFlanagan and Ospina-Calderón, 2018Flanagan, N.S.; Ospina-Calderón, N.H.; Agapito, L.T.G.; Mendonza, M.; Mateus, H.A. 2018. A new species of Vanilla (Orchidaceae) from the North West Amazon in Colombia. Phytotaxa 364: 250-258.), and a new worm-like fish species (Tarumania walkeraede Pinna et al., 2017de Pinna, M.; Zuanon, J.; Rapp Py-Daniel, L.; Petry, P. 2017. A new family of neotropical freshwater fishes from deep fossorial Amazonian habitat, with a reappraisal of morphological characiform phylogeny (Teleostei: Ostariophysi), Zoological Journal of the Linnean Society 182: 76-106.) that inhabits moist leaf litter deep within the rainforest, and which represents an entirely new family, the Tarumaniidae (de Pinna et al. 2018Pinna, M.; Zuanon, J.; Rapp Py-Daniel, L.; Petry, P. 2018. A new family of neotropical freshwater fishes from deep fossorial Amazonian habitat, with a reappraisal of morphological characiform phylogeny (Teleostei: Ostariophysi). Zoological Journal of the Linnean Society 182: 76-106.).

Comprehensive knowledge of the species that inhabit hyperdiverse Amazonian ecosystems is central to better understanding their ecosystem functions (Malhi et al. 2008Malhi, Y.; Roberts, J.T.; Betts, R.A.; Killeen, T.J.; Li, W.; Nobre, C.A. 2008. Climate change, deforestation, and the fate of the Amazon. Science 319: 169-172.) and the emergent properties that arise from interactions among Amazonian species and their abiotic environments. For example, while it is clear that the Amazonian hydrological cycles depend on forest transpiration, and that they impact climate at a continental scale (Costa et al. 2021Costa, M.H.; Borma, L.S.; Espinoza, J.C.; Macedo, M.; Marengo, J.A.; Marra, D.M.; et al. (Ed.). 2021. Amazon Assessment Report 2021. United Nations Sustainable Development Solutions Network, New York , doi: 10.55161/HTSD9250
https://doi.org/10.55161/HTSD9250... ), the influence of local species and their traits on precipitation patterns and climate remains to be understood (Chambers et al. 2007Chambers, J.Q.; Asner, G.P.; Morton, D.C.; Anderson, L.O.; Saatchi, S.S., Espírito-Santo, F.D.B.; Palace, M.; Souza, C. 2007. Regional ecosystem structure and function: ecological insights from remote sensing of tropical forests. Trends in Ecology & Evolution 22: 414-423.). Large-scale approaches aiming at quantifying unknown biodiversity, such as metagenomics, are also contributing to a deeper understanding of poorly studied life forms (e.g., bacteria, fungi, microorganisms) and ecosystem-level biochemical processes in Amazonian soils (Ritter et al. 2020Ritter, C.D.; Dunthorn, M.; Anslan, S.; de Lima, V.X.; Tedersoo, L.; Nilsson, R.H.; Antonelli, A.2020. Advancing biodiversity assessments with environmental DNA: Long-read technologies help reveal the drivers of Amazonian fungal diversity. Ecology and Evolution 10: 7509-7524.) and rivers (Ghai et al. 2011Ghai, R.; Rodríiguez-Valera, F.; McMahon, K.D.; Toyama, D.; Rinke, R.; de Oliveira, T.C.S.; Garcia, J.W.; de Miranda, F.P.; Henrique-Silva, F. 2011. Metagenomics of the water column in the pristine upper course of the Amazon river. PLoS One 6: e23785.; Santos et al. 2019Santos, C.D.; Sarmento, H.; de Miranda, F.P.;Henrique-Silva, F.; Logares, R.. 2020. Uncovering the genomic potential of the Amazon River microbiome to degrade rainforest organic matter. Microbiome, 8:151. doi.org/10.1186/s40168-020-00930-w
https://doi.org/10.1186/s40168-020-00930... ). While still under-utilized, these approaches are revolutionizing our understanding of Amazonian biodiversity patterns and their inherent processes, guiding conservation prioritization approaches and management plans for the basin.

Understanding the evolutionary history of Amazonian biodiversity is crucial to managing its exceptional biodiversity and ecosystem functions (Rull 2011Rull, V. 2011. Origins of Biodiversity. Science 331: 398-399.; Figure 3). This knowledge, in turn, holds key information for guiding conservation of endemic species and ecosystem services in times of climatic change. Until recently, fragmentary comprehension of Amazonian biodiversity at finer taxonomic levels led scientists to use more inclusive taxonomic categories (e.g., genera, families) in studying diversification patterns in this region (Antonelli et al. 2009Antonelli, A.; Nylander, J.A.A.; Persson, C.; Sanmartín, I. 2009. Tracing the impact of the Andean uplift on Neotropical plant evolution. Proceedings of the Natural Academy of Sciences 106: 9749-9754.). While these higher taxonomic categories have provided important insights into biodiversity patterns (Terborgh and Andresen 1998Terborgh, J.; Andresen, E. 1998. The composition of Amazonian forests: Patterns at local and regional scales. Journal of Tropical Ecology 15 645-664.), they cannot be objectively defined nor compared across taxa, rendering generalizations difficult (Cracraft et al. 2020Cracraft, J.; Ribas, C.C.; d’Horta, F.M.; Bates, J.; Almeida, R.P.; Aleixo, A.; et al. 2020. The origin and evolution of Amazonian species diversity. In: Rull, V.; Carnaval, A.C. (Ed.). Neotropical Diversification: Patterns and Processes, Fascinating Life Sciences, Springer Nature Switzerland AG, p.225-244. ). Integrative approaches that combine standardized field sampling, DNA barcoding (García-Melo et al. 2019García-Melo, J.E.; Oliveira, C.; Costa Silva, G.J. Da; Ochoa-Orrego, L.E.; Pereira, L.H.G.; Maldonado-Ocampo, J.A. 2019. Species delimitation of neotropical characins (Stevardiinae): Implications for taxonomy of complex groups (Z Peng, Ed). PLoS One 14: e0216786.; Vacher et al. 2020Vacher, J.; Chave, J.; Ficetola, F.G.; Sommeria-klein, G.; Tao, S.; Thébaud, C.; et al. 2020. Large‐scale DNA‐based survey of frogs in Amazonia suggests a vast underestimation of species richness and endemism. Journal of Biogeography 47: 1781-1791.), comparative phylogenomics (Alda et al. 2019Alda, F.; Tagliacollo, V.A.; Bernt, M.J.; Waltz, B.T.; Ludt, W.B.; Faircloth, C.B.; Alfaro, M.E.; Albert, J.S.; Chakrabarty, P. 2019. Resolving deep nodes in an ancient radiation of neotropical fishes in the presence of conflicting signals from incomplete lineage sorting. Systematic Biology 68: 573-593.; Santos et al. 2019Santos, C.D.; Sarmento, H.; de Miranda, F.P.;Henrique-Silva, F.; Logares, R.. 2020. Uncovering the genomic potential of the Amazon River microbiome to degrade rainforest organic matter. Microbiome, 8:151. doi.org/10.1186/s40168-020-00930-w
https://doi.org/10.1186/s40168-020-00930... ), and artificial intelligence (Draper et al. 2020Draper, F.C.; Baker, T.R.; Baraloto, C.; Chave, J.; Costa, F.; Martin, R.E.; Pennington, T.R.; Vicentini, A.; Asner, G.P. 2020. Quantifying tropical plant diversity requires an integrated technological approach. Trends in Ecology & Evolution 35: 1100-1109.) have accelerated the fine-scale documentation of Amazonian biodiversity (Ritter et al. 2020Ritter, C.D.; Dunthorn, M.; Anslan, S.; de Lima, V.X.; Tedersoo, L.; Nilsson, R.H.; Antonelli, A.2020. Advancing biodiversity assessments with environmental DNA: Long-read technologies help reveal the drivers of Amazonian fungal diversity. Ecology and Evolution 10: 7509-7524.; Vacher et al. 2020). These approaches involve new sampling efforts while also relying on museum specimens, which significantly leverage taxonomic work (e.g., Thom et al. 2020Thom, G.; Xue, A.T.; Sawakuchi, A.O.; Ribas, C.C.; Hickerson, M.J.; Aleixo, A.; Miyaki, C. 2020. Quaternary climate changes as speciation drivers in the Amazon floodplains. Science Advances 6: eaax4718.; Vacher et al. 2020). Unfortunately, Amazonian museum collections are still undervalued despite offering a rich source of information (Escobar 2018). Local institutions need support to hire experts in the field, and to maintain and expand their biological collections (Fontaine et al. 2012Fontaine, B.; Achterberg, K. van; Alonso-Zarazaga, M.A.; Araujo, R.; Asche, M.; Aspöck, H.; et al. 2012. New species in the Old World: Europe as a frontier in biodiversity exploration: A test bed for 21st century taxonomy (B Schierwater, Ed). PLoS One 7: e36881. ; Funk 2018Funk, V.A. 2018. Collections-based science in the 21st century. Journal of Systematics and Evolution 56: 175-193.). Human resources and infrastructure support are also crucial for the maintenance of the large databases of Amazonian species compiled to date. While important and useful, they should be constantly vetted and updated to address knowledge gaps and misidentifications.

EVOLUTION OF AMAZONIAN FORESTS

Flowering plants constitute the main physical structure of Amazonian rainforests. They exhibit a wide variety of growth forms, including woody trees, shrubs, and lianas, as well as epiphytes, herbaceous sedges, grasses, and colonial bamboos (Rowe and Speck 2005Rowe, N.; Speck, T. 2005. Plant growth forms: an ecological and evolutionary perspective. New Phytologist 166: 61-72.). DNA studies suggest that flowering plants first diversified in the Early Cretaceous or ca. 145-100 million years ago (Ma) (Magallón et al. 2015Magallón, S.; Gómez-Acevedo, S.; Sánchez-Reyes, L.L.; Hernández-Hernández, T. 2015. A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytologist 207: 437-453.), and fossil data suggest that they did not dominate Neotropical ecosystems until the Late Cretaceous (ca. 100-66 Ma; Burnham & Johnson 2004Burnham, R.J.; Johnson, K.R. 2004. South American palaeobotany and the origins of neotropical rainforests. Philosophical Transactions of the Royal Society London Series B Biological Sciences 359: 1595-1610.; Dino et al. 1999Dino, R.; Pocknall, D.T.; Dettmann, M.E. 1999. Morphology and ultrastructure of elater-bearing pollen from the Albian to Cenomanian of Brazil and Ecuador: Implications for botanical affinity. Review Palaeobotany Palynology 105: 201-235.; Mejia-Velasquez et al. 2012Mejia-Velasquez, P.J.; Dilcher, D.L.; Jaramillo, C.A.; Fortini, L.B.; Manchester, S.R.2012. Palynological composition of a Lower Cretaceous South American tropical sequence: climatic implications and diversity comparisons with other latitudes. American Journal of Botany 99: 1819-1827.; Carvalho et al. 2021Carvalho, M.R.; Jaramillo, C.; de la Parra, F.; Caballero-Rodríguez, D.; Herrera, F.; Wing, S.; et al. 2021. Extinction at the end-Cretaceous and the origin of modern Neotropical rainforests. Science 372: 63-68.).

While some Amazonian lineages have ancient origins dating back to the Early Cenozoic or Cretaceous (Cracraft et al. 2020Cracraft, J.; Ribas, C.C.; d’Horta, F.M.; Bates, J.; Almeida, R.P.; Aleixo, A.; et al. 2020. The origin and evolution of Amazonian species diversity. In: Rull, V.; Carnaval, A.C. (Ed.). Neotropical Diversification: Patterns and Processes, Fascinating Life Sciences, Springer Nature Switzerland AG, p.225-244. ), most species that currently inhabit the Amazon originated within the past few million years (Da Silva et al. 2005Silva, J.M.C. Da.; Rylands, A.B.; Fonseca, G.A.B. Da. 2005. The fate of the Amazonian Areas of Endemism. Conservation Biology 19: 689-694.; Rull 2008Rull, V. 2008. Speciation timing and neotropical biodiversity: the Tertiary-Quaternary debate in the light of molecular phylogenetic evidence. Molecular Ecology 17: 2722-2729., 2011, 2020Rull, V. 2020. Neotropical diversification: Historical overview and conceptual insights. In: Rull, V.; Carnaval, A.C. (Ed.). Neotropical Diversification: Patterns and Processes. Springer International Publishing, Cham , 13-49p.; Santos et al. 2019Santos, C.D.; Sarmento, H.; de Miranda, F.P.;Henrique-Silva, F.; Logares, R.. 2020. Uncovering the genomic potential of the Amazon River microbiome to degrade rainforest organic matter. Microbiome, 8:151. doi.org/10.1186/s40168-020-00930-w
https://doi.org/10.1186/s40168-020-00930... ). The wide distribution of evolutionary ages of Amazonian species suggests that the formation of its modern-day biodiversity took place over an immense time span (Cracraft et al. 2020), being influenced by the many changes in the physical landscape during the Cenozoic (Antonelli et al. 2009Antonelli, A.; Nylander, J.A.A.; Persson, C.; Sanmartín, I. 2009. Tracing the impact of the Andean uplift on Neotropical plant evolution. Proceedings of the Natural Academy of Sciences 106: 9749-9754.; Hoorn et al. 2010Hoorn, C.; Wesselingh, F.P.; Steege, H. ter; Bermudez, M.A.; Mora, A.; Sevink, J.; et al. 2010. Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330: 927-931.), producing extinctions and turnovers of several lineages (Jaramillo et al. 2010Jaramillo, C.; Hoorn, C.; Silva, S.A.F.; Leite, F.; Herrera, F.; Quiroz, L.; Dino, R.; Antonioli, L. 2010a. The origin of the modern Amazon rainforest: implications of the palynological and palaeobotanical record. In: Hoorn, C.; Wesselingh, F.P. (Ed.). Amazonia, Landscape and Species Evolution: A Look Into the Past. Blackwell Publishing, New York, p.259-280.a, 2010b).

The Amazon was substantially modified by a sudden mass extinction triggered by the Chicxulub asteroid impact about 66 million years ago at the Cretaceous-Paleogene [K-Pg] boundary (De La Parra et al. 2008Parra, G. De La; Jaramillo, C.; Dilcher, D. 2008. Paleoecological changes of spore producing plants through the Cretaceous-Paleocene boundary in Colombia. In: Vaughn, M.B. (Ed.). Palynology. American Association of Stratigraphic Palynologists Foundation c/o Vaughn m Bryant, Jr, palynology laboratory, Texas, 258-259.; Carvalho et al. 2021Carvalho, M.R.; Jaramillo, C.; de la Parra, F.; Caballero-Rodríguez, D.; Herrera, F.; Wing, S.; et al. 2021. Extinction at the end-Cretaceous and the origin of modern Neotropical rainforests. Science 372: 63-68.; Jacobs and Currano 2021Jacobs, B.F.; Currano, E.D. 2021. The impactful origin of neotropical rainforests. Science 372: 28-29.). Many groups of Neotropical birds (Claramunt and Cracraft 2015Claramunt, S.; Cracraft, J. 2015. A new time tree reveals Earth history’s imprint on the evolution of modern birds. Science Advances 1: e1501005.; Oliveros et al. 2019Oliveros, C.H.; Field, D.J.; Ksepka, D.T.; Barker, F.K.; Aleixo, A.; Andersen, M.J.; et al. 2019. Earth history and the passerine superradiation. Proceedings of the Natural Academy of Sciences 116: 7916-7925.), butterflies (Espeland et al. 2015Espeland, M.; Hall, J.P.W.; DeVries, P.J.; Lees, D.C.; Cornwall, M.; Hsu, Y.; et al. 2015. Ancient Neotropical origin and recent recolonisation: Phylogeny, biogeography and diversification of the Riodinidae (Lepidoptera: Papilionoidea). Molecular Phylogenetics and Evolution 93: 296-306., 2018Espeland, M.; Breinholt, J.; Willmott, K.R.; Warren, A.D.; Vila, R.; Toussaint, E.F.A.; et al. 2018. A comprehensive and dated phylogenomic analysis of butterflies. Current Biology 28: 770-778.; Seraphim et al. 2018Seraphim, N.; Kaminski, L.A.; Devries, P.J.; Penz, C.; Callaghan, C.; Wahlberg, N.; Silva-Brandão, K.L.; Freitas, A.V.L 2018. Molecular phylogeny and higher systematics of the metalmark butterflies (Lepidoptera: Riodinidae). Systematic Entomology 43: 407-425.), and fishes (Friedman 2010Friedman, M. 2010. Explosive morphological diversification of spiny-finned teleost fishes in the aftermath of the end-Cretaceous extinction. Proceedings of the Royal Society Series B Biological Sciences 277: 1675-1683.; Hughes et al. 2018Hughes, L.C.; Ortí, G.; Huang, Y.; Sun, Y.; Baldwin, C.C.; Thompson, A.W.; et al. 2018. Comprehensive phylogeny of ray-finned fishes (Actinopterygii) based on transcriptomic and genomic data. Proceedings of the Natural Academy of Sciences 115: 6249-6254.) diversified rapidly following this event. Plant communities similar to those seen in today’s Neotropical rainforests, although with fewer species, evolved in the Paleocene (ca. 66-56 Ma) (Wing et al. 2009Wing, S.L.; Herrera, F.; Jaramillo, C.A.; Gómez-Navarro, C.; Wilf, P.; Labandeira, C.C. 2009. Late Paleocene fossils from the Cerrejón Formation, Colombia, are the earliest record of Neotropical rainforest. Proceedings of the Natural Academy of Sciences 106: 18627-18632.; Jaramillo et al. 2010Jaramillo, C.; Hoorn, C.; Silva, S.A.F.; Leite, F.; Herrera, F.; Quiroz, L.; Dino, R.; Antonioli, L. 2010a. The origin of the modern Amazon rainforest: implications of the palynological and palaeobotanical record. In: Hoorn, C.; Wesselingh, F.P. (Ed.). Amazonia, Landscape and Species Evolution: A Look Into the Past. Blackwell Publishing, New York, p.259-280.a), with many plant lineages diversifying in the Eocene (ca. 56-34 Ma) (Lohmann et al. 2013Lohmann, L.G.; Bell, C.D.; Calió, M.F.; Winkworth, R.C. 2013. Pattern and timing of biogeographical history in the Neotropical tribe Bignonieae (Bignoniaceae). Botanical Journal of the Linnean Society 171: 154-170.). Indeed, Neotropical rainforest plants seem to have reached a pinnacle of diversity during the Eocene (ca. 56-34 Ma), when warm and moist climates still predominated (Jaramillo et al. 2006Jaramillo, C.; Rueda, M.J.; Mora, G. 2006. Cenozoic plant diversity in the Neotropics. Science 311: 1893-1896.). Eocene forests are thought to have been highly rich in species (Burnham and Graham 1999Burnham, R.J.; Graham, A. 1999. The history of neotropical vegetation: new developments and status. Annals of the Missouri Botanical Garden 86: 546-589.; Jaramillo et al. 2006Jaramillo, C.; Rueda, M.J.; Mora, G. 2006. Cenozoic plant diversity in the Neotropics. Science 311: 1893-1896., 2010aJaramillo, C.; Hoorn, C.; Silva, S.A.F.; Leite, F.; Herrera, F.; Quiroz, L.; Dino, R.; Antonioli, L. 2010a. The origin of the modern Amazon rainforest: implications of the palynological and palaeobotanical record. In: Hoorn, C.; Wesselingh, F.P. (Ed.). Amazonia, Landscape and Species Evolution: A Look Into the Past. Blackwell Publishing, New York, p.259-280., 2010bJaramillo, C.; Ochoa, D.; Contreras, L.; Pagani, M.; Carvajal-Ortiz, H.; Pratt, L.M.; et al. 2010b. Effects of rapid global warming at the Paleocene-Eocene boundary on neotropical vegetation. Science 330: 957-961.). Conspicuous elements of Paleocene Neotropical rainforests include members of key plant groups such as palms and herbs (e.g., families Araceae and Zingiberaceae), shrubs (e.g., Malvaceae), lianas (e.g., Menispermaceae), and trees (e.g., Lauraceae) (Burnham and Johnson 2004; Wing et al. 2009; Carvalho et al. 2011Carvalho, M.R.; Herrera, F.A.; Jaramillo, C.A.; Wing, S.L.; Callejas, R. 2011. Paleocene Malvaceae from northern South America and their biogeographical implications. American Journal of Botany 98: 1337-1355.).

The drier seasons and cooler climates of the Early Oligocene (ca. 30 Ma) contributed to extensive vegetational changes throughout South America. Namely, the once continuous and broadly distributed wet South American rainforests were divided in two, the Amazon and Atlantic rainforests, due to expansion of open subtropical woodland forests in central South America and the establishment of the Seasonally Dry Diagonal (Bigarella 1975Bigarella, J.J. 1975. Considerações a respeito das mudanças paleoambientais na distribuição de algumas espécies vegetais e animais no Brasil. Anais da Academia Brasileira de Ciencias 47: 411-464.; Costa 2003Costa, L.P. 2003. The historical bridge between the Amazon and the Atlantic Forest of Brazil: A study of molecular phylogeography with small mammals. Journal of Biogeography 30: 71-86.; Orme 2007Orme, A.R. 2007. Tectonism, climate, and landscape change, pp: 23-44. In: Veblen, T.T.; Young, K.R.; Orme, A.R. (Ed.), The Physical Geography of South America. New York and Oxford, 368p.; Fouquet et al. 2012Fouquet, A.; Recoder, R.; Teixeira Jr, M.; Cassimiro, J.; Amaro, R.C.; Camacho, A.; et al. 2012. Molecular phylogeny and morphometric analyses reveal deep divergence between Amazonia and Atlantic Forest species of Dendrophryniscus. Molecular Phylogenetics and Evolution 62: 826-838.; Sobral-Souza et al. 2015Sobral-Souza, T.; Lima-Ribeiro, M.S.; Solferini, V.N. 2015. Biogeography of Neotropical rainforests: Past connections between Amazon and Atlantic Forest detected by ecological niche modeling. Evolutionary Ecology 29: 643-655.; Thode et al. 2019Thode, V.A.; Sanmartín, I.; Lohmann, L.G. 2019. Contrasting patterns of diversification between Amazonian and Atlantic forest clades of Neotropical lianas (Amphilophium, Bignonieae) inferred from plastid genomic data. Molecular Phylogenetics and Evolution 133: 92-106.). These vegetational changes coincided with the beginning of the uplift of the Mantiqueira Mountains of eastern Brazil, and of the northern Andes in Colombia, causing substantial changes in South American air currents. Increasingly drier climates and the expansion of open savannah vegetation types were accompanied by substantial changes in species composition (e.g., more palms), the origin of C4 grasses (Vicentini et al. 2008Vicentini, A.; Barber, J.C.; Aliscioni, S.S.; Giussani, L.M.; Kellogg, E.A. 2008. The age of the grasses and clusters of origins of C4 photosynthesis. Global Change Biology 14: 2963-2977.; Urban et al. 2010Urban, M.A.; Nelson, D.M.; Jiménez-Moreno, G.; Châteauneuf, J.J.; Pearson, A.; Hu, F.S. 2010. Isotopic evidence of C4 grasses in southwestern Europe during the Early Oligocene--Middle Miocene. Geology 38: 1091-1094.; Bouchenak-Khelladi et al. 2014Bouchenak-Khelladi, Y.; Slingsby, J.A.; Verboom, G.A.; Bond, W.J. 2014. Diversification of C4 grasses (Poaceae) does not coincide with their ecological dominance. American Journal of Botany 101: 300-307.), and the expansion of grasslands and open woodlands at the expense of closed-canopy forested habitats (Edwards and Smith 2010Edwards, E.J.; Smith, S.A. 2010. Phylogenetic analyses reveal the shady history of C4 grasses. Proceedings of the Natural Academy of Sciences 107: 2532-2537.; Edwards et al. 2010Edwards, E.J.; Osborne, C.P.; Strömberg, C.A.E.; Smith, S.A.; Consortium, G.; Bond, W.J.; et al. 2010. The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328: 587-591.; Kirschner and Hoorn 2020Kirschner, J.A.; Hoorn, C. 2020. The onset of grasses in the Amazon drainage basin, evidence from the fossil record. Frontiers of Biogeography 12(2): e44827. ).

In the Miocene, uplift of the northern and central Andes led to a profound reorganization of the river network of the whole of northern South America, including the formation of the Pebas mega-wetland (Hoorn et al. 1995, 2010, 2017; Albert et al. 2018Albert, J.S.; Val, P.; Hoorn, C. 2018. The changing course of the Amazon River in the Neogene: Center stage for Neotropical diversification. Neotropical Ichthyology 16(3): e180033.), a vast region (ca. 1 million km²) of lacustrine and swampy environments located in the area of the modern western Amazon (Hoorn 1993Hoorn, C. 1993. Marine incursions and the influence of Andean tectonics on the Miocene depositional history of northwestern Amazonia: results of a palynostratigraphic study. Palaeogeography Palaeoclimatology Palaeoecology 105: 267-309.; Wesselingh and Salo 2006Wesselingh, F.P.; Salo, JA. 2006. A Miocene perspective on the evolution of the Amazonian biota. Scripta Geologica 133: 439-458.; Bicudo et al. 2019Bicudo, T.C.; Sacek, V.; Almeida, R.P. de; Bates, J.M.; Ribas, C.C. 2019. Andean tectonics and mantle dynamics as a pervasive influence on Amazonian ecosystem. Scientific Reports 9: 1-11.). Progressive uplift of the northern Andes also affected the regional climate, leading to increased precipitation due to the orography (Poulsen et al. 2010Poulsen, C.J.; Ehlers, T.A.; Insel, N. 2010. Onset of convective rainfall during gradual Late Miocene rise of the central Andes. Science 328: 490-493.). Vast areas of flooded forests were then established, composed of palms (i.e., Grimsdalea), ferns, and grasses (Poaceae), among others (Hoorn 1994Hoorn, C. 1994. An environmental reconstruction of the palaeo-Amazon river system (Middle-Late Miocene, NW Amazonia). Palaeogeography Palaeoclimatology Palaeoecology 112: 187-238.; Jaramillo et al. 2017Jaramillo, C.; Romero, I.; D’Apolito, C.; Bayona, G.; Duarte, E.; Louwye, E.; et al. 2017. Miocene flooding events of western Amazonia. Science Advances 3: e1601693.; Hoorn et al. 2017; Kirschner and Hoorn 2020Kirschner, J.A.; Hoorn, C. 2020. The onset of grasses in the Amazon drainage basin, evidence from the fossil record. Frontiers of Biogeography 12(2): e44827. ; Hoorn et al. 2023Hoorn, C.; Lohmann, L.G.; Boschman, L.M.; Condamine, F.L. 2023. Neogene history of the Amazonian flora: A perspective based on geological, palynological, and molecular phylogenetic data. Annual Review of Earth and Planetary Sciences 51: 419-446.). In addition, marine incursions into the western Amazon from the Caribbean Sea allowed estuarine taxa to colonize the northern Pebas shorelines (Hoorn 1993Hoorn, C. 1993. Marine incursions and the influence of Andean tectonics on the Miocene depositional history of northwestern Amazonia: results of a palynostratigraphic study. Palaeogeography Palaeoclimatology Palaeoecology 105: 267-309.; Boonstra et al. 2015Boonstra, M.; Ramos, M.I.F.; Lammertsma, E.I.; Antoine, P.O.; Hoorn, C. 2015. Marine connections of Amazonia: Evidence from foraminifera and dinoflagellate cysts (early to middle Miocene, Colombia/Peru). Palaeogeography Palaeoclimatology Palaeoecology 417: 176-194.; Jaramillo et al. 2017; Hoorn et al. 2023).

In the Late Miocene and Pliocene, a major landscape reshaping took place, caused in part by overfilling of sedimentary basins in the western Amazon with Andean-derived sediments; this led to a renewed drainage reorganization and the onset of the modern transcontinental Amazon River (Hoorn et al. 2010Hoorn, C.; Wesselingh, F.P.; Steege, H. ter; Bermudez, M.A.; Mora, A.; Sevink, J.; et al. 2010. Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330: 927-931., 2017, 2023). The former Pebas wetland surfaces were colonized by many different lineages (Antonelli et al. 2009Antonelli, A.; Nylander, J.A.A.; Persson, C.; Sanmartín, I. 2009. Tracing the impact of the Andean uplift on Neotropical plant evolution. Proceedings of the Natural Academy of Sciences 106: 9749-9754.; Roncal et al. 2013Roncal, J.; Kahn, F.; Millan, B.; Couvreur, T.L.P.; Pintaud, J.C. 2013. Cenozoic colonization and diversification patterns of tropical American palms: evidence from Astrocaryum (Arecaceae). Botanical Journal of the Linnean Society 171: 120-139.), in a process of upland forest expansion that is suggested to have continued until the Late Pleistocene (Pupim et al. 2019Pupim, F.N.; Sawakuchi, A.O.; Almeida, R.P. de; Ribas, C.C.; Kern, A.K.; Hartmann, G.A.; et al. 2019. Chronology of Terra Firme formation in Amazonian lowlands reveals a dynamic Quaternary landscape. Quaternary Science Reviews 210: 154-163.). Landscape changes also led to increased diversification of numerous plant lineages, such as the flowering plant genera Inga (Legumes; Richardson et al. 2001Richardson, J.E.; Pennington, R.T.; Pennington, T.D.; Hollingsworth, P.M. 2001. Rapid diversification of a species-rich genus of neotropical rain forest trees. Science 293: 2242-2245.) and Guatteria (Annonaceae; Erkens et al. 2007Erkens, R.H.J.; Chatrou, L.W.; Maas, J.W.; van der Niet, T.; Savolainen, V. 2007. A rapid diversification of rainforest trees (Guatteria; Annonaceae) following dispersal from Central into South America. Molecular Phylogenetics and Evolution 44: 399-411.). At around the same time, the Andean slopes were colonized by many plant lineages, including species of the Malvaceae (Hoorn et al. 2019), Arecaceae (i.e., palms; Bacon et al. 2018Bacon, C.D.; Velásquez-Puentes, F.J.; Hoorn, C.; Antonelli, A. 2018. Iriarteeae palms tracked the uplift of Andean Cordilleras. Journal of Biogeography 45: 1653-1663.), and Chloranthaceae families (i.e., Hedyosmum; Martínez et al. 2013Martínez, C.; Madriñán, S.; Zavada, M.; Alberto Jaramillo, C. 2013. Tracing the fossil pollen record of Hedyosmum (Chloranthaceae), an old lineage with recent Neotropical diversification. Grana 52: 161-180.). From the Late Miocene to the Pliocene (ca. 11-4 Ma), the rise of the Eastern Cordillera of the Colombian Andes completed the isolation of the cis-Andean (Orinoco-Amazon) from the trans-Andean (Pacific slope, Magdalena, and Maracaibo) basins, resulting in the isolation of their resident aquatic biotas (Albert et al. 2006Albert, J.S.; Lovejoy, N.R.; Crampton, W.G.R. 2006. Miocene tectonism and the separation of cis-and trans-Andean river basins: Evidence from Neotropical fishes. Journal of South America Earth Science 21: 14-27.). Evidence suggests that high levels of plant species diversity existed in Amazonia during the Miocene thanks to a combination of low seasonality, high precipitation, and edaphic heterogeneous substrate (Jaramillo et al. 2010Jaramillo, C.; Ochoa, D.; Contreras, L.; Pagani, M.; Carvajal-Ortiz, H.; Pratt, L.M.; et al. 2010b. Effects of rapid global warming at the Paleocene-Eocene boundary on neotropical vegetation. Science 330: 957-961.a).

The Neogene uplift of the Northern Andes (ca. 23-2.6 Ma) had profound effects on Amazonian landscapes, impacting the diversification of both lowland and highland lineages (Hoorn et al. 2010Hoorn, C.; Wesselingh, F.P.; Steege, H. ter; Bermudez, M.A.; Mora, A.; Sevink, J.; et al. 2010. Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330: 927-931.; Albert et al. 2011Albert, J.S.; Petry, P.; Reis, R.E. 2011a. Major biogeographic and phylogenetic patterns. In: Historical Biogeography of Neotropical Freshwater Fishes, (Ed. Albert, J.S.; Reis, R.E.). University of California Press, 1: 21-57.b; Givnish et al. 2016Givnish, T.J.; Spalink, D.; Ames, M.; Lyon, S.P.; Zuluaga, A.; Doucette, A.; et al. 2016. Orchid historical biogeography, diversification, Antarctica and the paradox of orchid dispersal. Journal of Biogeography 43: 1905-1916.; Rahbek et al. 2019Rahbek, C.; Borregaard, M.K.; Antonelli, A.; Colwell, R.K.; Holt, B.G.; Nogues-Bravo N.; Rasmussen, C.M.O.; Richardson, K.; Rosing, M.T.; Whittaker, R.J.; Fjeldså, J.2019. Building mountain biodiversity: Geological and evolutionary processes. Science 365: 1114-1119.; Montes et al. 2021Montes, C.; Silva, C.A.; Bayona, G.A.; Villamil, R.; Stiles, E.; Rodriguez-Corcho, A.F.;et al. 2021. A Middle to Late Miocene Trans-Andean Portal: Geologic Record in the Tatacoa Desert. Frontiers Earth Science 8: 587022.). Yet, despite its importance for biogeography, the specific role of mountain ranges as a dispersal barrier between South and Central American lowland plant lineages is still poorly understood (Pérez-Escobar et al. 2017Pérez-Escobar, O.A.; Gottschling, M.; Chomicki, G.; Condamine, F.L.; Klitgård, B.B.; Pansarin, E.; Gerlach, G. 2017. Andean mountain building did not preclude dispersal of lowland epiphytic orchids in the Neotropics. Scientific Reports 7: 4919. doi.org/10.1038/s41598-017-04261-z
https://doi.org/10.1038/s41598-017-04261... ). Different diversification patterns have been detected within and between upland and lowland groups, with higher species richness in lowlands and higher species endemism in uplands. The uplift of the northern Andes and its associated dynamic climate history were key drivers of the rapid radiation of Andean-centered plants (Gentry 1982Gentry, A.H. 1982. Neotropical floristic diversity: phytogeographical connections between Central and South America, Pleistocene climatic fluctuations, or an accident of the Andean orogeny? Annals of the Missouri Botanical Garden 69: 557-593.; Jost 2004Jost, L. 2004. Explosive local radiation of the genus Teagueia (Orchidaceae) in the Upper Pastaza watershed of Ecuador. Lyonia 7: 41-47.; Madriñán et al. 2013Madriñán, S.; Cortés, A.J.; Richardson, J.E. 2013. Páramo is the world’s fastest evolving and coolest biodiversity hotspot. Frontiers in Genetics 4: 192. doi: 10.3389/fgene.2013.00192
https://doi.org/10.3389/fgene.2013.00192... ; Luebert and Weigend 2014Luebert, F.; Weigend, M. 2014. Phylogenetic insights into Andean plant diversification. Frontiers in Ecology and Evolution 2: 27. doi: 10.3389/fevo.2014.00027
https://doi.org/10.3389/fevo.2014.00027... ; Lagomarsino et al. 2016Lagomarsino, L.P.; Condamine, F.L.; Antonelli, A.; Mulch, A.; Davis, C.C. 2016. The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae). New Phytologist 210: 1430-1442.; Vargas et al. 2017Vargas, O.M.; Ortiz, E.M.; Simpson, B.B. 2017. Conflicting phylogenomic signals reveal a pattern of reticulate evolution in a recent high-Andean diversification (Asteraceae: Astereae: Diplostephium). New Phytologist 214: 1736-1750.) and animals (Albert et al. 2018; Rahbek et al. 2019; Perrigo et al. 2020Perrigo, A.; Hoorn, C.; Antonelli, A. 2020. Why mountains matter for biodiversity. Journal of Biogeography 47: 315-25.). Near mountain tops, plants of the páramo ecosystem underwent one of the highest speciation rates ever recorded (Madriñán et al. 2013; Padilla-González et al. 2017Padilla-González, G.F.; Diazgranados, M.; Costa, F.B. Da. 2017. Biogeography shaped the metabolome of the genus Espeletia: A phytochemical perspective on an Andean adaptive radiation. Scientific Reports 7: 8835. doi.org/10.1038/s41598-017-09431-7
https://doi.org/10.1038/s41598-017-09431... ; Pouchon et al. 2018Pouchon, C.; Fernández, A.; Nassar, J.M.; Boyer, F.; Aubert, S.; Lavergne, S.; Mavárez, J. 2018. Phylogenomic analysis of the explosive adaptive radiation of the Espeletia complex (Asteraceae) in the tropical Andes. Systematic Biology 67: 1041-1060.).

During the Quaternary (last ca. 2.6 Ma), global climate cooling in combination with geomorphological processes strongly altered the western Amazonian landscape. Alluvial megafans (large sediment aprons >10,000 km²) extended from the Andes into the Amazon (e.g., Räsänen et al. 1990Räsänen, M.E.; Salo, J.S.; Jungnert, H.; Pittman, L.R. 1990. Evolution of the western Amazon lowland relief: impact of Andean foreland dynamics. Terra Nova 2: 320-332., 1992Räsänen, M.; Neller, R.; Salo, J.; Jungner, H. 1992. Recent and ancient fluvial deposition systems in the Amazonian foreland basin, Peru. Geological Magazine 129: 293-306.; Wilkinson et al. 2010Wilkinson, M.J.; Marshall, L.G.; Lundberg, J.G.; Kreslavsky, M.H. 2010. Megafan environments in northern South America and their impact on Amazon Neogene aquatic ecosystems. In: Wiley-Blackwell, N. (Ed.). Amazonia, Landscape and species Evolution a look into past, Oxford Wiley-Blackwell, p.162-184.), and floodplains varied in size according to changes in precipitation patterns (Pupim et al. 2019Pupim, F.N.; Sawakuchi, A.O.; Almeida, R.P. de; Ribas, C.C.; Kern, A.K.; Hartmann, G.A.; et al. 2019. Chronology of Terra Firme formation in Amazonian lowlands reveals a dynamic Quaternary landscape. Quaternary Science Reviews 210: 154-163.). The effect of these cyclic climatic changes on landscape and vegetation composition is yet to be fully understood. Direct studies of the sedimentary and fossil records (Jaramillo et al. 2017Jaramillo, C.; Romero, I.; D’Apolito, C.; Bayona, G.; Duarte, E.; Louwye, E.; et al. 2017. Miocene flooding events of western Amazonia. Science Advances 3: e1601693.; Hoorn et al. 2017Hoorn, C.; Bogotá-A, G.R.; Romero-Baez, M.; Lammertsma, E.I.; Flantua, S.G.A.; Dantas, E.L.; Dino, R.; do Carmo, D.A.; Chemale Jr, F. 2017. The Amazon at sea: Onset and stages of the Amazon River from a marine record, with special reference to Neogene plant turnover in the drainage basin. Global and Planetary Change 153: 51-65.; Mason et al. 2019Mason, C.C.; Romans, B.W.; Stockli, D.F.; Mapes, R.W.; Fildani, A. 2019. Detrital zircons reveal sea-level and hydroclimate controls on Amazon River to deep-sea fan sediment transfer. Geology 47: 563-567.), as well as climatic models (Arruda et al. 2017Arruda, D.M.; Schaefer, C.E.G.R.; Fonseca, R.S.; Solar, R.R.C.; Fernandes-Filho, E.I. 2017. Vegetation cover of Brazil in the last 21 ka: new insights into the Amazonian refugia and Pleistocenic arc hypotheses. Global Ecology and Biogeography 27: 47-56.; Costa et al. 2017Costa, G.C.; Hampe, A.; Ledru, M-P.; Martinez, P.A.; Mazzochini, G.G.; Shepard, D.B.; Werneck, F.P.; Moritz, C.; Carnaval, A.C. 2017. Biome stability in South America over the last 30 kyr: Inferences from long‐term vegetation dynamics and habitat modelling. Global Ecology and Biogeography 27: 285-297.; Häggi et al. 2017Häggi, C.; Chiessi, C.M.; Merkel, U.; Mulitza, S.; Prange, M.; Schulz, M.; Schefuß, E. 2017. Response of the Amazon rainforest to Late Pleistocene climate variability. Earth and Planetary Science Letters 479: 50-59.), suggest that general patterns of regional vegetation cover (i.e. forest, savannah) did not change drastically in tropical South America in comparison with other regions of the world over the past 100,000 years, but did vary spatially and over time under the influence of both geological and climatic changes (Hoorn et al. 2010; Antoine et al. 2016Antoine, P.-O.; Abello, M.A.; Adnet, S.; Altamirano Sierra, A.J.; Baby, P.; Billet, G.; et al. 2016. A 60-million-year Cenozoic history of western Amazonian ecosystems in Contamana, eastern Peru. Gondwana Research 31: 30-59.; Wang et al. 2017Wang, X.; Edwards, R.L.; Auler, A.S.; Cheng, H.; Kong, X.; Wang, Y.; Cruz, F.W.; Dorale, J.A.; Chiang, H.W. 2017. Hydroclimate changes across the Amazon lowlands over the past 45,000 years. Nature 541: 204-207.). The dynamic nature of Amazonian vegetation cover during the Quaternary may not have been extremely drastic (e.g., rapidly replacing closed canopy forest by savanna), but sufficient to change the forest cover and to affect the distribution of specialized species (Arruda et al. 2017; Wang et al. 2017; Silva et al. 2019Silva, S.M.; Peterson, A.T.; Carneiro, L.; et al. 2019. A dynamic continental moisture gradient drove Amazonian bird diversification. Science Advances 5: eaat5752.; but see Sato et al. 2021Sato, H.; Kelley, D.I.; Mayor, S.J.; Calvo, M.M.; Cowling, S.A.; Prentice, I.C. 2021. Dry corridors opened by fire and low CO2 in Amazonian rainforest during the Last Glacial Maximum. Nature Geoscience 14: 578-585.). Current evidence fails to support one of the better-known hypotheses for Amazonian diversification, the Pleistocene Refugia hypothesis as originally proposed by Haffer (1969Haffer, J. 1969. Speciation in Amazonian forest birds. Science 165: 131-137.). The Refugia hypothesis proposed that Pleistocene climatic oscillations led to the cyclic replacement of forest- and savanna-covered landscapes, resulting in recurrent isolation and merging of populations, and leading to an increased rate of formation of new species. Although available data from multiple sources now indicate that savannah and open grassland ecosystems have never been widespread in the Amazon (Liu and Colinvaux 1985Liu, K.; Colinvaux, P.A. 1985. Forest changes in the Amazon Basin during the last glacial maximum. Nature 318: 556-557.; Colinvaux et al. 2000Colinvaux, P.A.; Oliveira, P.E. de; Bush, M.B. 2000. Amazonian and neotropical plant communities on glacial time-scales: The failure of the aridity and refuge hypotheses. Quaternary Science Reviews 19: 141-169.; Bush and Oliveira 2006Bush, M.B.; Oliveira, P.E. de. 2006. The rise and fall of the Refugial Hypothesis of Amazonian speciation: a paleoecological perspective. Biota Neotropica 6(1): bn00106012006. ), the eastern Amazon probably experienced substantial changes in vegetation structure, with possible episodes of open vegetation expansion (Cowling et al. 2001Cowling, S.A.; Maslin, M.A.; Sykes, M.T. 2001. Paleovegetation simulations of lowland Amazonia and implications for neotropical allopatry and speciation. Quaternary Research 55: 140-149.; Arruda et al. 2017, Sato et al. 2021) that may have affected species distributions and diversification. Nevertheless, it is important to stress that the effects of Pleistocene climate oscillations on the diversification of Amazonian biotas are incomplete and generalizations should be taken cautiously.

ASSEMBLING THE MEGADIVERSE AMAZONIAN BIOTA

Diversification dynamics

Amazonian biodiversity was assembled through a unique and unrepeatable combination of processes that intermingle geological, climatic, and biological factors across broad spatial and temporal scales, involving taxa distributed across the whole of the South American continent and evolving over a period of tens of millions of years. From a macroevolutionary perspective, the number of species in a geographic region may be modeled as a balance between rates of speciation and immigration that increase overall species numbers, and extinction that decreases species richness (Voelker et al. 2013Voelker, G.; Marks, B.D.; Kahindo, C.; A’genonga, U.; Bapeamoni, F.; Duffie, L.E.; Huntley, J.W.; Mulotwa, E.; Rosenbaum, S.A.; Light, J.E. 2013. River barriers and cryptic biodiversity in an evolutionary museum. Ecology and Evolution 3: 536-545.; Castroviejo-Fisher et al. 2014Castroviejo-Fisher, S.; Guayasamin, J.M.; Gonzalez-Voyer, A.; Vilà, C. 2014. Neotropical diversification seen through glassfrogs. Journal of Biogeography 41: 66-80.; Roxo et al. 2014Roxo, F.F.; Albert, J.S.; Silva, G.S.C.; Zawadzki, C.H.; Foresti, F.; Oliveira, C.2014. Molecular phylogeny and biogeographic history of the armored Neotropical catfish subfamilies Hypoptopomatinae, Neoplecostominae and Otothyrinae (Siluriformes: Loricariidae). PLoS One 9: e105564.). A region that accrues high species richness due to elevated speciation rates has been referred to as an “evolutionary cradle” of diversity, i.e., a place of high species origination (Gross 2019Gross, M. 2019. Finding the cradles of evolution. Current Biology 29: R71-73.). By contrast, a region where species tend to accumulate through low rates of extinction may be called an “evolutionary museum” of diversity (Stebbins 1974Stebbins, G.L. 1974. Flowering Plants: Evolution Above the Species Level. Harvard University Press, Cambridge, 417p.; Stenseth 1984Stenseth, N.C. 1984. The tropics: Cradle or museum? Oikos 43: 417-420.). Although a useful heuristic in some contexts, this model is a poor fit to Amazonian biodiversity. Amazonian species and higher taxa exhibit a broad range of evolutionary ages, such that the Amazon serves simultaneously as both an evolutionary cradle and museum. Still, groups with different average phylogenetic ages tend to inhabit different geographic portions of the Amazon basin. Species assemblages in the upland Guianas and Brazilian Shields (>250 - 300 m elevation) often include a mix of both older and younger lineages, while the lowland sedimentary basins often harbor younger lineages. This pattern is observed in many taxonomic groups (e.g., plants, Ulloa Ulloa and Neill 2006Ulloa Ulloa, C.; Neill, D.A. 2006. Phainantha shuariorum (Melastomataceae), una especie nueva de la Cordillera del Cóndor, Ecuador, disyunta de un género guayanés. Novon: A Journal for Botanical Nomenclature 16: 281-285.; Amazonian rocket frogs Allobates, Réjaud et al. 2020Réjaud, A.; Rodrigues, M.T.; Crawford, A.J.; Castroviejo-Fisher, S.; Jaramillo, A.F.; Chaparro, C.J.; et al. 2020. Historical biogeography identifies a possible role of Miocene wetlands in the diversification of the Amazonian rocket frogs (Aromobatidae: Allobates). Journal of Biogeography 47: 2472-2482.; fishes, Albert et al. 2020Albert, J.S.; Tagliacollo, V.A.; Dagosta, F. 2020a. Diversification of Neotropical freshwater fishes. Annual Review of Ecology Evolution and Systematics 51: 27-53.a), although exceptions also exist (Castroviejo-Fisher et al. 2014; Bonaccorso and Guayasamin 2013Bonaccorso, E.; Guayasamin, J.M. 2013. On the origin of Pantepui montane biotas: a perspective based on the phylogeny of Aulacorhynchus toucanets. PLoS One 8: e67321.). Similar contrasting core-periphery patterns are observed in many Neotropical taxa, including birds, mammals, snakes, frogs, and plants (Antonelli et al. 2018Antonelli, A.; Zizka, A.; Carvalho, F.A.; Scharn, R.; Bacon, C.D.; Silvestro, D.; Condamine, F.L. 2018. Amazonia is the primary source of Neotropical biodiversity. Proceedings of the Natural Academy of Sciences 115: 6034-6039.; Azevedo et al. 2020Azevedo, J.A.R.; Guedes, T.B.; Nogueira, C. de C.; Passos, P.; Sawaya, R.J.; Prudente, A.L.C.; et al. 2020. Museums and cradles of diversity are geographically coincident for narrowly distributed Neotropical snakes. Ecography 43: 328-339.; Vasconcelos et al. 2020Vasconcelos, T.N.C.; Alcantara, S.; Andrino, C.O.; Forest, F.; Reginato, M.; Simon, M.F.; Pirani, J.R. 2020. Fast diversification through a mosaic of evolutionary histories characterizes the endemic flora of ancient Neotropical mountains. Proceedings of the Royal Society Series B Biological Sciences 287: 20192933.). Diversification in response to geographic barriers is one of the most widespread processes that facilitates speciation. In the Amazon, this process is thought to have played an important role in the evolution of the local biota (e.g., Crouch et al. 2018Crouch, N.M.; Capurucho, J.M.; Hackett, S.J.; Bates, J.M. 2018. Evaluating the contribution of dispersal to community structure in Neotropical passerine birds. Ecography 42: 390-399.). Geographic barriers can isolate individuals that once belonged to a continuous population of a given species into two (or more) non-overlapping sets of populations (Coyne and Orr 2004Coyne, J.A.; Orr, H.A. 2004. Speciation. Sinauer Associates, Inc., Sunderland, MA Sinauer, 545p.). When this geographic separation is maintained for long periods of time, new species may be formed through a process called allopatric speciation (Figure 4). For instance, the uplift of the Andes separated previously connected lowland taxa, preventing dispersal, and establishing new habitats that have fostered the evolution of novel, independent lineages (Albert et al. 2006; Hutter et al. 2013Hutter, C.R.; Guayasamin, J.M.; Wiens, J.J. 2013. Explaining Andean megadiversity: the evolutionary and ecological causes of glassfrog elevational richness patterns. Ecology Letters 16: 1135-1144.; Canal et al. 2019Canal, D.; Köster, N.; Celis, M.; Croat, T.B.; Borsch, T.; Jones, K.T. 2019. Out of Amazonia and back again: Historical biogeography of the species-rich Neotropical genus Philodendron (Araceae) 1. Annals of the Missouri Botanical Garden 104: 49-68.; Figure 5). This event fragmented the aquatic fauna of northwestern South America, leaving a clear signal on all major taxa (Albert et al. 2006). Among families of freshwater fishes, species diversity is significantly correlated with a minimum number of cis-/trans-Andean clades, which indicates that the relative species diversity and biogeographic distributions of Amazonian fishes were effectively modern by the Late Miocene (Albert et al. 2006).

Changes in river drainage networks have also strongly affected dispersal, gene flow, and biotic diversification within the Amazon. Large lowland Amazonian rivers represent important geographic barriers for groups of primates (e.g., Wallace 1852Wallace, A.R. 1852. On the monkeys of the Amazon. Annals and Magazine of Natural History 14(84): 451-454.; Ayres and Clutton-Brock 1992Ayres, J.M.; Clutton-Brock, T.H. 1992. River boundaries and species range size in Amazonian primates. American Naturalist 140: 531-537.), birds (Ribas et al. 2012Ribas, C.C.; Aleixo, A.; Nogueira, A.C.R.; Miyaki, C.Y.; Cracraft, J.2012. A palaeobiogeographic model for biotic diversification within Amazonia over the past three million years. Proceedings of the Royal Society Series B Biological Sciences 279: 681-689.; Silva et al. 2019Silva, S.M.; Peterson, A.T.; Carneiro, L.; et al. 2019. A dynamic continental moisture gradient drove Amazonian bird diversification. Science Advances 5: eaat5752.), fishes (Albert et al. 2011Albert, J.S.; Petry, P.; Reis, R.E. 2011a. Major biogeographic and phylogenetic patterns. In: Historical Biogeography of Neotropical Freshwater Fishes, (Ed. Albert, J.S.; Reis, R.E.). University of California Press, 1: 21-57.a), butterflies (Brower 1996Brower, A.V.Z. 1996. Parallel race formation and the evolution of mimicry in Heliconius butterflies: a phylogenetic hypothesis from mitochondrial DNA sequences. Evolution 50: 195-221.; Rosser et al. 2021Rosser, N.; Shirai, L.T.; Dasmahapatra, K.K.; Mallet, J.; Freitas, A.V.L. 2021. The Amazon river is a suture zone for a polyphyletic group of co-mimetic heliconiine butterflies. Ecography 44: 177-187.), wasps (Menezes et al. 2020Menezes, R.S.T.; Lloyd, M.W.; Brady, S.G. 2020. Phylogenomics indicates Amazonia as the major source of Neotropical swarm-founding social wasp diversity. Proceedings of the Royal Society Series B 287: 20200480.), and plants (Nazareno et al. 2017Nazareno, A.G.; Dick, C.W.; Lohmann, L.G. 2017. Wide but not impermeable: Testing the riverine barrier hypothesis for an Amazonian plant species. Molecular Ecology 26: 3636-3648., 2019aNazareno, A.G.; Dick, C.W.; Lohmann, L.G. 2019. A biogeographic barrier test reveals a strong genetic structure for a canopy-emergent amazon tree species. Scientific Reports 9: 18602. doi.org/10.1038/s41598-019-55147-1
https://doi.org/10.1038/s41598-019-55147... , bNazareno, A.G.; Dick, C.W.; Lohmann, L.G. 2019. Tangled banks: A landscape genomic evaluation of Wallace’s Riverine barrier hypothesis for three Amazon plant species. Molecular Ecology 28: 980-997., 2021Nazareno, A.G.; Knowles, L.L.; Dick, C.W.; Lohmann, L.G. 2021. By animal, water, or wind: Can dispersal mode predict genetic connectivity in riverine plant species? Frontiers in Plant Science 12: 626405.). Similarly, past climatic change is believed to have cyclically changed the distribution of Amazonian habitats such as closed-canopy forests, open forests, non-forest vegetation, and cold-adapted forests, often causing population fragmentation and speciation (Cheng et al. 2013Cheng, H.; Sinha, A.; Cruz, F.W.; Wang, X.; Edwards, R.L.; d´Horta, F.M.; Ribas, C.C.; Vuille, M.; Stott, L.D.; Auler, A.S. 2013. Climate change patterns in Amazonia and biodiversity. Nature Communications 4: 1411. doi.org/10.1038/ncomms2415
https://doi.org/10.1038/ncomms2415... ; Arruda et al. 2017Arruda, D.M.; Schaefer, C.E.G.R.; Fonseca, R.S.; Solar, R.R.C.; Fernandes-Filho, E.I. 2017. Vegetation cover of Brazil in the last 21 ka: new insights into the Amazonian refugia and Pleistocenic arc hypotheses. Global Ecology and Biogeography 27: 47-56.; Wang et al. 2017Wang, X.; Edwards, R.L.; Auler, A.S.; Cheng, H.; Kong, X.; Wang, Y.; Cruz, F.W.; Dorale, J.A.; Chiang, H.W. 2017. Hydroclimate changes across the Amazon lowlands over the past 45,000 years. Nature 541: 204-207.; Silva et al. 2019).

Apart from the importance of past geographic isolation and speciation due to habitat discontinuity, adaptation to specific habitats has also contributed significantly to species diversification in this region (Figure 5). The large geographical extension of the Amazon, tied to its diverse soil types, provided multiple opportunities for ecological specialization (Fine et al. 2005Fine, P.A.; Daly, D.C.; Cameron, K.M. 2005. The contribution of edaphic heterogeneity to the evolution and diversity of burseracear trees in the western Amazon. Evolution 59: 1464-1478.; Tuomisto et al. 2019Tuomisto, H.; Doninck, J. Van; Ruokolainen, K.; Moulatlet, G.M.; Figueiredo, F.O.G.; Sirén, A.; Cárdenas, G.; Lehtonen, S.; Zuquim, G. 2019. Discovering floristic and geoecological gradients across Amazonia. Journal of Biogeography 46: 1734-1748.). This soil heterogeneity reflects the complex geological history of northern South America.

While the erosion of the Guiana and Brazilian shields produced the soils of the eastern Amazon, younger sediments that are products of Andean orogeny have developed soils in the western Amazon that tend to be more fertile (Tuomisto et al. 2014Tuomisto, H.; Zuquim, G.; Cárdenas, G. 2014. Species richness and diversity along edaphic and climatic gradients in Amazonia. Ecography 37: 1034-1046.). This east-to-west gradient in soil fertility is paralleled by a gradient in species composition, wood density, seed mass, and wood productivity (but not forest biomass, see Ter Steege et al. 2006; Tuomisto et al. 2014). Likewise, different levels of forest inundation during the annual flooding cycle have contributed to the formation of diverse habitat types and specializations in groups of birds and fishes (Albert et al. 2011Albert, J.S.; Petry, P.; Reis, R.E. 2011a. Major biogeographic and phylogenetic patterns. In: Historical Biogeography of Neotropical Freshwater Fishes, (Ed. Albert, J.S.; Reis, R.E.). University of California Press, 1: 21-57.a; Wittmann et al. 2013Wittmann, F.; Householder, E.; Piedade, M.T.F.; de Assis, R.L.; Schöngart, J.; Parolin, P.; Junk, W.J. 2013. Habitat specificity, endemism and the neotropical distribution of Amazonian white-water floodplain trees. Ecography 36: 690-707.; Luize et al. 2018Luize, B.G.; Magalhães, J.L.L.; Queiroz, H.; Lopes, M.A.; Venticinque, E.M.; de Moraes, E.M.N.; Silva, T.S.F. 2018. The tree species pool of Amazonian wetland forests: Which species can assemble in periodically waterlogged habitats? PLoS One 13: e0198130.; Thom et al. 2020Thom, G.; Xue, A.T.; Sawakuchi, A.O.; Ribas, C.C.; Hickerson, M.J.; Aleixo, A.; Miyaki, C. 2020. Quaternary climate changes as speciation drivers in the Amazon floodplains. Science Advances 6: eaax4718.).

Habitat heterogeneity has played an important role in the formation of Amazonian biodiversity, with geological changes also impacting the ecological conditions available to the Amazonian biota. Andean uplift, for instance, has had a major effect on the Neotropical climate, as it created both habitat and climate heterogeneity while leading to the humidification of Amazonian lowlands and the aridification of Patagonia (Blisniuk et al. 2005Blisniuk, P.M.; Stern, L.A.; Chamberlain, C.P.; Idleman, B.; Zeitler, P.K. 2005. Climatic and ecologic changes during Miocene surface uplift in the Southern Patagonian Andes. Earth and Planetary Science Letters 230: 125-142.; Rohrmann et al. 2016). The Andes, with an average elevation of 4,000 m, exhibit an immense gradient of humidity and temperature. This has provided numerous opportunities for colonization, adaptation, and speciation events in lowland species, such as frogs, birds, and plants, at different times (Ribas et al. 2007Ribas, C.C.; Moyle, R.G.; Miyaki, C.Y.; Cracraft, J. 2007. The assembly of montane biotas: linking Andean tectonics and climatic oscillations to independent regimes of diversification in Pionus parrots. Proceedings of the Royal Society Series B Biological Sciences 274: 2399-2408.; Hutter et al. 2013Hutter, C.R.; Guayasamin, J.M.; Wiens, J.J. 2013. Explaining Andean megadiversity: the evolutionary and ecological causes of glassfrog elevational richness patterns. Ecology Letters 16: 1135-1144.; Hoorn et al. 2019Hoorn, C.; Ham, R. van der; la Parra, F. de; Salamanca, S.; Steege, H.T.; Banks, H.; et al. 2019. Going north and south: The biogeographic history of two Malvaceae in the wake of Neogene Andean uplift and connectivity between the Americas. Reviews Palaeobotany Palynology 264: 90-109.; Cadena et al. 2020Cadena, C.D.; Cuervo, A.M.; Céspedes, L.N.; Bravo, G.A.; Krabbe, N.; Schulenberg, T.S.; et al. 2020a. Systematics, biogeography, and diversification of Scytalopus tapaculos (Rhinocryptidae), an enigmatic radiation of Neotropical montane birds. Auk 137: ukz077.a; Réjaud et al. 2020Réjaud, A.; Rodrigues, M.T.; Crawford, A.J.; Castroviejo-Fisher, S.; Jaramillo, A.F.; Chaparro, C.J.; et al. 2020. Historical biogeography identifies a possible role of Miocene wetlands in the diversification of the Amazonian rocket frogs (Aromobatidae: Allobates). Journal of Biogeography 47: 2472-2482.; Figure 6). As a consequence, the Andes are disproportionately more biodiverse relative to their surface area (e.g., Testo et al. 2019Testo, W.L.; Sessa, E.; Barrington, D.S. 2019. The rise of the Andes promoted rapid diversification in Neotropical Phlegmariurus (Lycopodiaceae). New Phytologist 222: 604-613.). This dynamic interaction between lowlands and adjacent mountains are known to generate diversity worldwide (Quintero and Jetz 2018Quintero, I.; Jetz, W. 2018. Global elevational diversity and diversification of birds. Nature 555: 246-250.; Rahbek et al. 2019Rahbek, C.; Borregaard, M.K.; Antonelli, A.; Colwell, R.K.; Holt, B.G.; Nogues-Bravo N.; Rasmussen, C.M.O.; Richardson, K.; Rosing, M.T.; Whittaker, R.J.; Fjeldså, J.2019. Building mountain biodiversity: Geological and evolutionary processes. Science 365: 1114-1119.). Repeated cycles of ecological connectivity and spatial isolation in the high Andes (as observed in today’s páramos) may have acted as a “species pump” and significantly increased speciation rates in high-elevation Andean taxa due to the joint action of allopatry, natural selection, and adaptation (Madriñán et al. 2013Madriñán, S.; Cortés, A.J.; Richardson, J.E. 2013. Páramo is the world’s fastest evolving and coolest biodiversity hotspot. Frontiers in Genetics 4: 192. doi: 10.3389/fgene.2013.00192
https://doi.org/10.3389/fgene.2013.00192... ; Rangel et al. 2018Rangel, T.F.; Edwards, N.R.; Holden, P.B.; Diniz-Filho, J.A.F.; Gosling, W.D.; Coelho, M.T.P.; Cassemiro, F.A.S.; Rahbek, C.; Colwell, R.K. 2018. Modeling the ecology and evolution of biodiversity: Biogeographical cradles, museums, and graves. Science 361: eaar5452. doi.org/10.1126/science.aar5452
https://doi.org/10.1126/science.aar5452... ; Pouchon et al. 2018Pouchon, C.; Fernández, A.; Nassar, J.M.; Boyer, F.; Aubert, S.; Lavergne, S.; Mavárez, J. 2018. Phylogenomic analysis of the explosive adaptive radiation of the Espeletia complex (Asteraceae) in the tropical Andes. Systematic Biology 67: 1041-1060.).

The contributing roles of abiotic and biotic processes in biodiversification have been neatly summarized as the so-called Court Jester and Red Queen perspectives, respectively (Benton 2009Benton, M.J. 2009. The Red Queen and the Court Jester: species diversity and the role of biotic and abiotic factors through time. Science 323: 728-732.). The Court Jester hypothesis emphasizes the role of abiotic physical and chemical factors as major drivers of speciation (emphasizing, for example, the role of adaptation to climate, substrate, or water condition; Barnosky 2001Barnosky, A.D. 2001. Distinguishing the effects of the Red Queen and Court Jester on Miocene mammal evolution in the northern Rocky Mountains. Journal of Vertebrate Paleontology 21: 172-185.). Abiotic factors deriving directly from geographic space, climatic and elevation gradients, topographic relief, hydrology, and sediment and water chemistry all serve to facilitate organismal diversification into major habitat types. Intertwined with these landscape processes are innumerable biotic processes that create new species and prevent extinction (e.g., competition, predation, parasitism, mutualism, and cooperation). These biotic interactions can lead to the co-evolution of new traits, increase the structural heterogeneity and functional dimensions of habitats, and enhance the genetic and phenotypic diversity of Amazonian ecosystems. Together with the evolutionary processes that emerge from them, these biological interactions are emphasized in the Red Queen hypothesis. As we discuss below, the immense biodiversity of the Amazon results from both abiotic (see Geographical connectivity through time) and biotic (see How biodiversity generates and maintains biodiversity) factors.

Geographical connectivity through time

The Amazon basin is a highly heterogeneous set of landscapes and riverscapes that form a mosaic of habitat types, often characterized by distinct floras and faunas (e.g., Duellman 1999Duellman, W.E. 1999. Patterns of Distribution of Amphibians: A Global Perspective. JHU Press, Baltimore and London, 565p.; Cardoso et al. 2017Cardoso, D.; Särkinen, T.; Alexander, S.; Amorim, A.M.; Bittrich, V.; Celis, M.; et al. 2017. Amazon plant diversity revealed by a taxonomically verified species list. Proceedings of the Natural Academy of Sciences 114: 10695-10700.; Tuomisto et al. 2019Tuomisto, H.; Doninck, J. Van; Ruokolainen, K.; Moulatlet, G.M.; Figueiredo, F.O.G.; Sirén, A.; Cárdenas, G.; Lehtonen, S.; Zuquim, G. 2019. Discovering floristic and geoecological gradients across Amazonia. Journal of Biogeography 46: 1734-1748.; Albert et al. 2020Albert, J.S.; Tagliacollo, V.A.; Dagosta, F. 2020a. Diversification of Neotropical freshwater fishes. Annual Review of Ecology Evolution and Systematics 51: 27-53.a; Figure 7). Abiotic changes and shifts in the distribution and connection among these different habitats across space and through time drove the accumulation of the impressive number of Amazonian species (Dambros et al. 2020Dambros, C.; Zuquim, G.; Moulatlet, G.M.; Costa, F.R.C.; Tuomisto, H.; Ribas, C.C. 2020. The role of environmental filtering, geographic distance and dispersal barriers in shaping the turnover of plant and animal species in Amazonia. Biodiversity Conservation 29: 3609-3634.). Because organisms differ so widely in their functional traits (such as their dispersal abilities and physiological tolerances), the same landscape conditions that allow for demographic and genetic connections in some groups can have no effects or even reduce connections in others. For example, while large lowland rivers such as the Amazon and the Negro constitute effective barriers to dispersal in upland species of monkeys and birds (representing boundaries between closely related species of those groups; Cracraft 1985Cracraft, J. 1985. Historical biogeography and patterns of differentiation within the South American avifauna: Areas of endemism. Ornithological Monographs 36: 49-84.), these very same waterways serve as dispersal corridors for riverine and floodplain species of fishes, birds, mammals, and plants with seeds dispersed by fishes or turtles (e.g., Albert et al. 2011bAlbert, J.S.; Carvalho, T.P.; Petry, P.; Holder, M.A.; Maxime, L.E.; Espino, J.; Corahua, I.; Quispe, R.; Rengifo, B.; Ortega, H.; Reis, R. 2011b. Aquatic biodiversity in the Amazon: habitat specialization and geographic isolation promote species richness. Animals 1: 205-241.; Parolin et al. 2013Parolin, P.; Wittmann, F.; Ferreira, L.V.. 2013. Fruit and seed dispersal in Amazonian floodplain trees: a review. Ecotropica 19: 15-32.).

This habitat heterogeneity may be one of the reasons why past landscape changes that promoted the diversification of co-existing lineages in the Amazon resulted in different geographical patterns of species distributions among groups, and different times of speciation (Da Silva et al. 2005Silva, J.M.C. Da.; Rylands, A.B.; Fonseca, G.A.B. Da. 2005. The fate of the Amazonian Areas of Endemism. Conservation Biology 19: 689-694.; Naka and Brumfield 2018Naka, L.N.; Brumfield, R.T. 2018. The dual role of Amazonian rivers in the generation and maintenance of avian diversity. Science Advances 4: eaar8575.; Silva et al. 2019). In this heterogeneous and dynamic landscape, the effectiveness of an isolating barrier depends on the biological characteristics of individual species, such as their habitat affinity, their ability to move through the landscape, their tolerance to temperature and precipitation extremes, their generation time, clutch size, and abundance patterns, among other factors (Paz et al. 2015Paz, A.; Ibáñez, R.; Lips, K.R.; Crawford, A.J. 2015. Testing the role of ecology and life history in structuring genetic variation across a landscape: A trait-based phylogeographic approach. Molecular Ecology 24: 3723-3737.; Papadopoulou and Knowles 2016Papadopoulou, A.; Knowles, L.L. 2016. Toward a paradigm shift in comparative phylogeography driven by trait-based hypotheses. Proceedings of the Natural Academy of Sciences 113: 8018-8024.; Capurucho et al. 2020Capurucho, J.M.G.; Borges, S.H.; Cornelius, C.; Vicentini, A.; Prata, E.M.B.; Costa, F.M.; et al. 2020. Patterns and processes of diversification in Amazonian white sand ecosystems: insights from birds and plants. In: Rull, V.; Carnaval, A. (Eds.). Neotropical Diversification: Patterns and Processes. Springer, Cham, p.245-270.). Low dispersal ability, for example, facilitates geographic isolation and genetic differentiation that tend to increase speciation rates (e.g., tropical insects, Polato et al. 2018Polato, N.R.; Gill, B.A.; Shah, A.A.; Gray, M.M.; Casner, K.L.; Barthelet, A.; et al. 2018. Narrow thermal tolerance and low dispersal drive higher speciation in tropical mountains. Proceedings of the Natural Academy of Sciences 115: 12471-12476.), but also increase the risk of local extinction (Cooper et al. 2008Cooper, N.; Bielby, J.; Thomas, G.H.; Purvis, A. 2008. Macroecology and extinction risk correlates of frogs. Global Ecology and Biogeography 17: 211-221.). Thermal tolerances, on the other hand, mediate the impact of climate on diversity maintenance and speciation rates (Janzen 1967Janzen, D.H. 1967. Why mountain passes are higher in the tropics. American Naturalist 101: 233-249.). Because tropical species experience relatively stable environmental temperatures across their annual cycle, they have evolved more narrow thermal tolerances and reduced dispersal capacities relative to temperate species (Janzen 1967; Shah et al. 2017Shah, A.A.; Gill, B.A.; Encalada, A.C.; Flecker, A.S.; Funk, C.W.; Guayasamin, J.M.; et al. 2017. Climate variability predicts thermal limits of aquatic insects across elevation and latitude. Functional Ecology 31: 2118-2127.), which promotes speciation, especially in mountain gradients (Polato et al. 2018). Lowland tropical species also live under temperature conditions close to their thermal maximum, which places them at risk in the face of increased global warming (Colwell et al. 2008Colwell, R.K.; Brehm, G.; Cardelús, C.L.; Gilman, A.C.; Longino, J.T. 2008. Global warming, elevational range shifts, and lowland biotic attrition in the wet tropics. Science 322: 258-261.; Deutsch et al. 2008Deutsch, C.A.; Tewksbury, J.J.; Huey, R.B.; Sheldon, K.S.; Ghalambor, C.K.; Haak, D.C.; Martin, P.R. 2008. Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences 105: 6668- 6672. ; Campos et al. 2018Campos, D.F.; Val, A.L.; Almeida-Val, V.M.F. 2018. The influence of lifestyle and swimming behavior on metabolic rate and thermal tolerance of twelve Amazon forest stream fish species. Journal of Thermal Biology 72: 148-154.; Diele-Viegas et al. 2018Diele-Viegas, LM.; Vitt, L.J.; Sinervo, B.; Colli, G.R.; Werneck, F.P.; Miles, D.B. 2018. Thermal physiology of Amazonian lizards (Reptilia: Squamata). PLoS One 13: e0192834., 2019Diele-Viegas, L.M.; Werneck, F.P.; Rocha, C.F.D. 2019. Climate change effects on population dynamics of three species of Amazonian lizards. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 236: 110530.). This is especially true for species that inhabit areas that are either distant from mountain ranges or fragmented, impeding migration to higher (and cooler) environments.

Because Amazonian species have unique evolutionary trajectories and variable environmental requirements, they have been differentially affected by past geological and climatic events. Patterns of historical connectivity among populations that inhabit upland rainforest habitats have been profoundly influenced by the changing courses of major lowland rivers and their associated floodplains over millions of years, and also by prominent topographic and habitat discontinuities, such as patches of rugged terrain, open savannah vegetation, and sandy soils (Capurucho et al. 2020Capurucho, J.M.G.; Borges, S.H.; Cornelius, C.; Vicentini, A.; Prata, E.M.B.; Costa, F.M.; et al. 2020. Patterns and processes of diversification in Amazonian white sand ecosystems: insights from birds and plants. In: Rull, V.; Carnaval, A. (Eds.). Neotropical Diversification: Patterns and Processes. Springer, Cham, p.245-270.; Cracraft et al. 2020Cracraft, J.; Ribas, C.C.; d’Horta, F.M.; Bates, J.; Almeida, R.P.; Aleixo, A.; et al. 2020. The origin and evolution of Amazonian species diversity. In: Rull, V.; Carnaval, A.C. (Ed.). Neotropical Diversification: Patterns and Processes, Fascinating Life Sciences, Springer Nature Switzerland AG, p.225-244. ). As an example, while the relatively narrow and young Branco River delimits the distribution of some primate species (Boubli et al. 2015Boubli, J.P.; Ribas, C.; Lynch Alfaro, J.W.; Alfaro M.E.; da Silva, M.N.F.; Pinho, G.M.; Farias, I.P. 2015. Spatial and temporal patterns of diversification on the Amazon: A test of the riverine hypothesis for all diurnal primates of Rio Negro and Rio Branco in Brazil. Molecular Phylogenetics and Evolution 82: 400-412.), this river has had a different role in the evolution of some birds (Naka and Brumfield 2018Naka, L.N.; Brumfield, R.T. 2018. The dual role of Amazonian rivers in the generation and maintenance of avian diversity. Science Advances 4: eaar8575.), plants (Nazareno et al. 2019Nazareno, A.G.; Dick, C.W.; Lohmann, L.G. 2019. A biogeographic barrier test reveals a strong genetic structure for a canopy-emergent amazon tree species. Scientific Reports 9: 18602. doi.org/10.1038/s41598-019-55147-1
https://doi.org/10.1038/s41598-019-55147... a, bNazareno, A.G.; Dick, C.W.; Lohmann, L.G. 2019. Tangled banks: A landscape genomic evaluation of Wallace’s Riverine barrier hypothesis for three Amazon plant species. Molecular Ecology 28: 980-997., 2021), and some small-bodied fishes (Dagosta and Pinna 2017Dagosta, F.C.P.; de Pinna, M. 2017. Biogeography of Amazonian fishes: Deconstructing river basins as biogeographic units. Neotropical Ichthyology 15(3): e170034.), serving as an effective barrier for some species but not for others. Traits are hence important not only to define the distribution and degree of connectivity of extant populations, but they have also influenced their evolutionary history over time (see Tamme et al. 2014Tamme, R.; Götzenberger, L.; Zobel, M.; Bullock, J.M.; Hooftman, D.A.P.; Kaasik, A.; Pärtel, M. 2014. Predicting species’ maximum dispersal distances from simple plant traits. Ecology 95: 505-513. ; Weeks et al. 2022Weeks, B.C.; O’Brien, B.K.; Chu, J.J.; Claramunt, S.; Sheard, C.; Tobias, J.A. 2022. Morphological adaptations linked to flight efficiency and aerial lifestyle determine natal dispersal distance in birds. Functional Ecology 36: 1681-1689. ).

Both terrestrial and aquatic Amazonian habitats have been profoundly affected by climate change, especially changing precipitation patterns and sea levels, over millions of years (Vonhof and Kaandorp 2010Vonhof, H.B.; Kaandrop, R.J.G. 2010. Climate variation in Amazonia during the Neogene and the Quaternary. In: Hoorn, C.; Wesselingh, F.P. (Ed.). Amazonia, Landscape and Species Evolution: A Look Into the Past. Wiley-Blackwell, Oxford , p.201-210.). Many studies have discussed the influence of past climates on Amazonian landscapes while focusing on changes of the relative cover of forest and savanna (e.g., Bush and Oliveira 2006Bush, M.B.; Oliveira, P.E. de. 2006. The rise and fall of the Refugial Hypothesis of Amazonian speciation: a paleoecological perspective. Biota Neotropica 6(1): bn00106012006. ). However, more subtle changes in forest structure may also affect species distributions and landscape connectivity (Cowling et al. 2001Cowling, S.A.; Maslin, M.A.; Sykes, M.T. 2001. Paleovegetation simulations of lowland Amazonia and implications for neotropical allopatry and speciation. Quaternary Research 55: 140-149.; Arruda et al. 2017Arruda, D.M.; Schaefer, C.E.G.R.; Fonseca, R.S.; Solar, R.R.C.; Fernandes-Filho, E.I. 2017. Vegetation cover of Brazil in the last 21 ka: new insights into the Amazonian refugia and Pleistocenic arc hypotheses. Global Ecology and Biogeography 27: 47-56.). Understanding how to maintain population connectivity is key to protecting Amazonian biodiversity. For instance, it is believed that the resilience of upland Amazonian forest taxa in face of environmental changes that occurred through time could be explained by the large dimensions of suitable habitat that allowed them to track appropriate climatic conditions, possibly explaining why so many upland forest species exhibit signs of changes in population size during the Pleistocene (Silva et al. 2019Silva, S.M.; Peterson, A.T.; Carneiro, L.; et al. 2019. A dynamic continental moisture gradient drove Amazonian bird diversification. Science Advances 5: eaat5752.). These historical dynamics lay the foundation for predictions of how future climate change will affect patches of humid forests, which are becoming increasingly fragmented due to deforestation and other human land-use activities (Albert et al. 2023Albert, J.S.; Carnaval, A.C.; Flantua, S.G.A.; Lohmann, L.G.; Ribas, C.C.; Riff, D.; et al. 2023 Human impacts outpace natural processes in the Amazon. Science, 379: eabo5003. ).

Trait mediated diversification in a heterogeneous Amazon

Studies that consider the habitat affinities of Amazonian species show that the history of each taxon, and its resilience through time, is deeply linked to the kinds of environments it occupies. This view is transforming the way scientists and the general public view the Amazon. Because the heterogeneity of lowland Amazonian habitats has been underappreciated, and because the region has been (wrongly) perceived as a large and homogeneous ecosystem, many taxa have been mistakenly considered widespread and generalist, and, consequently, resilient to landscape change (Bates and Demos 2001Bates, J.M.; Demos, T.C. 2001. Do we need to devalue Amazonia and other large tropical forests? Diversity and Distributions 7: 249-255.). Among birds, one of the best studied groups in Amazonia, it has been demonstrated that species from upland non-flooded forest have different ecological associations and evolutionary histories relative to the species that inhabit the floodplains and to those in open vegetation areas (Figures 7 - 9). Consequently, the geographical distribution of biological diversity differs among those three groups, and likely also their resilience to future environmental shifts (Capurucho et al. 2020Capurucho, J.M.G.; Borges, S.H.; Cornelius, C.; Vicentini, A.; Prata, E.M.B.; Costa, F.M.; et al. 2020. Patterns and processes of diversification in Amazonian white sand ecosystems: insights from birds and plants. In: Rull, V.; Carnaval, A. (Eds.). Neotropical Diversification: Patterns and Processes. Springer, Cham, p.245-270.; Cracraft et al. 2020Cracraft, J.; Ribas, C.C.; d’Horta, F.M.; Bates, J.; Almeida, R.P.; Aleixo, A.; et al. 2020. The origin and evolution of Amazonian species diversity. In: Rull, V.; Carnaval, A.C. (Ed.). Neotropical Diversification: Patterns and Processes, Fascinating Life Sciences, Springer Nature Switzerland AG, p.225-244. ; Thom et al. 2020Thom, G.; Xue, A.T.; Sawakuchi, A.O.; Ribas, C.C.; Hickerson, M.J.; Aleixo, A.; Miyaki, C. 2020. Quaternary climate changes as speciation drivers in the Amazon floodplains. Science Advances 6: eaax4718.).

Birds associated with upland non-flooded forest are the most diverse (currently comprising about 1,000 species; Billerman et al. 2020Billerman, S.M.; Keeney, B.K.; Rodewald, P.G.; Schulenberg, T.S (Eds.). 2020. Birds of the World. Cornell Laboratory of Ornithology, Ithaca, New York (https://birdsoftheworld.org/bow/home).
https://birdsoftheworld.org/bow/home... ). Within these groups, distinct species, although closely related, are found in each main Amazonian interfluve (Silva et al. 2019Silva, S.M.; Peterson, A.T.; Carneiro, L.; et al. 2019. A dynamic continental moisture gradient drove Amazonian bird diversification. Science Advances 5: eaat5752.). Similar patterns have also been described for other groups of Amazonian lineages, mostly distributed in upland forests (e.g., Craig et al. 2017Craig, J.M.; Crampton, W.G.R.; Albert, J.S. 2017. Revision of the polytypic electric fish Gymnotus carapo (Gymnotiformes, Teleostei), with descriptions of seven subspecies. Zootaxa 4318: 401-438.; Godinho and da Silva 2018Godinho, M.B. de C.; Silva, F.R. da. 2018. The influence of riverine barriers, climate, and topography on the biogeographic regionalization of Amazonian anurans. Scientific Reports 8: 3427. doi.org/10.1038/s41598-018-21879-9
https://doi.org/10.1038/s41598-018-21879... ; Figure 9). In contrast, populations associated with seasonally flooded environments, whose available habitats are currently distributed along the main Amazonian rivers, have been impacted by drastic habitat change due to shifts in the drainage system during the last 5 Ma (Bicudo et al. 2019Bicudo, T.C.; Sacek, V.; Almeida, R.P. de; Bates, J.M.; Ribas, C.C. 2019. Andean tectonics and mantle dynamics as a pervasive influence on Amazonian ecosystem. Scientific Reports 9: 1-11.), including significant changes even within the last 45 thousand years ago (Ka) (Pupim et al. 2019Pupim, F.N.; Sawakuchi, A.O.; Almeida, R.P. de; Ribas, C.C.; Kern, A.K.; Hartmann, G.A.; et al. 2019. Chronology of Terra Firme formation in Amazonian lowlands reveals a dynamic Quaternary landscape. Quaternary Science Reviews 210: 154-163.). While large rivers are barriers for the dispersal of small-bodied understory birds in humid non-flooded forests, the seasonally flooded vegetation that grows along these rivers promotes connections across populations of floodplain-associated species adapted to the annual flooding cycle of river floodplains. Differently from the upland non-flooded forest birds, floodplain species have little intraspecific diversity, but they represent older lineages that originated during the Middle to Late Miocene (5-11 Ma; Thom et al. 2020Thom, G.; Xue, A.T.; Sawakuchi, A.O.; Ribas, C.C.; Hickerson, M.J.; Aleixo, A.; Miyaki, C. 2020. Quaternary climate changes as speciation drivers in the Amazon floodplains. Science Advances 6: eaax4718.). The largest genetic differences within these widespread floodplain species are observed between populations from the western sedimentary basins and populations from the eastern shields (Thom et al. 2018Thom, G.; Amaral, F.R. Do; Hickerson, M.J.; Aleixo, A.; Araujo-Silva, L.E.; Ribas, C.C.; Choueri, E.; Miyaki, C.Y.2018. Phenotypic and genetic structure support gene flow generating gene tree discordances in an Amazonian floodplain endemic species. Systematic Biology 67: 700-718., 2020). These distinct evolutionary trajectories have helped to shape the history of Amazonian floodplains (Bicudo et al. 2019). Data from floodplain-adapted birds and fishes, for instance, indicate historically larger and more connected populations in the western Amazon (Santos et al. 2007Santos, M. da C.F.; Ruffino, M.L.; Farias, I.P. 2007. High levels of genetic variability and panmixia of the Tambaqui Colossoma macropomum (Cuvier, 1816) in the main channel of the Amazon River. Journal of Fish Biology 71: 33-44.; Thom et al. 2020), and cycles of connectivity and isolation between species that occupy seasonally flooded habitats in the eastern vs. western Amazon. Organisms adapted to seasonally flooded landscapes are particularly vulnerable to disruptions of connectivity caused either by historical landscape change or by anthropogenic impacts such as dams and waterways (Latrubesse et al. 2017Latrubesse, E.M.; Arima, E.Y.; Dunne, T.; Park, E.; Baker, V.R.; d’Horta, F.M.; et al. 2017. Damming the rivers of the Amazon basin. Nature 546: 363-369.; Anderson et al. 2018Anderson, E.P.; Jenkins, C.N.; Heilpern, S.; Maldonado-Ocampo, J.A.; Carvajal-Vallejos, F.M.; Encalada, A.C.; et al. 2018. Fragmentation of Andes-to-Amazon connectivity by hydropower dams. Science Advances 4: eaao1642.).

Species associated with open vegetation growing on sandy soils have yet a third pattern of diversity distribution in the Amazon. Among plants and birds, for instance, populations of the same species are distributed in patches of open habitat separated by upland and flooded forests and located thousands of kilometers apart, spanning all the main interfluvia (Capurucho et al. 2020Capurucho, J.M.G.; Borges, S.H.; Cornelius, C.; Vicentini, A.; Prata, E.M.B.; Costa, F.M.; et al. 2020. Patterns and processes of diversification in Amazonian white sand ecosystems: insights from birds and plants. In: Rull, V.; Carnaval, A. (Eds.). Neotropical Diversification: Patterns and Processes. Springer, Cham, p.245-270.). Despite having a naturally fragmented distribution today, these species were less isolated in the past, suggesting that, although present in the Amazon for millions of years, the distribution of open vegetation has varied through time (Adeney et al. 2016Adeney, J.M.; Christensen, N.L.; Vicentini, A.; Cohn-Haft, M. 2016. White-sand Ecosystems in Amazonia. Biotropica 48: 7-23.).

Together, these contrasting patterns indicate that the Amazonian landscape and its different habitats have been spatially dynamic during millions of years, and that the current distribution of habitats and species represents a snapshot in time.

How biodiversity generates and maintains biodiversity

There is little doubt that diverse biotas with many functionally distinct organisms, complex biotic environments, and multiple ecological interactions facilitate species coexistence and elevate regional species richness and density values. In this regard, biological diversity may be understood to be autocatalytic: species richness itself is a key feature in the origin of hyperdiverse Amazonian ecosystems (Sombroek 2000Sombroek, W. 2000. Amazon landforms and soils in relation to biological diversity. Acta Amazonica 30: 81-100.; Albert et al. 2011Albert, J.S.; Petry, P.; Reis, R.E. 2011a. Major biogeographic and phylogenetic patterns. In: Historical Biogeography of Neotropical Freshwater Fishes, (Ed. Albert, J.S.; Reis, R.E.). University of California Press, 1: 21-57.b; Dáttilo and Dyer 2014Dáttilo, W.; Dyer, L. 2014. Canopy Openness Enhances Diversity of Ant-Plant Interactions in the Brazilian Amazon Rain Forest. Biotropica 46: 712-719.).

The notion that biotic interactions help drive organismal diversification is not new. In a famous article, the paleontologist Leigh Van Valen observed that the life span of species as shown by the fossil record was roughly constant (van Valen 1973van Valen, L. 1973. A new evolutionary law. Evolutionary Theory 30: 1-30.). Borrowing from a line in Through the Looking Glass by Lewis Caroll, where the Red Queen tells Alice “It takes all the running you can do, to keep in the same place”, he proposed the Red Queen hypothesis as a metaphor to express the idea that lineages do not increase their ability to survive through geological time (van Valen 1973). In modern evolutionary theory, Red Queen dynamics refers to phenotypic evolution in response to biotic interactions, such as the coevolution of parasites and their hosts, chemically defended prey and their predators, and interactions between pollinators and the plant species they visit. In all these biotic interactions, adaptive changes in one species may be followed by adaptations in another species, spurring an evolutionary arms race that may result in co-evolution or extinction, or both (Strotz et al. 2018Strotz, L.C.; Simões, M.; Girard, M.G.; Breitkreus, L.; Kimmig, J.; Lieberman, B.S. 2018. Getting somewhere with the Red Queen: chasing a biologically modern definition of the hypothesis. Biology Letters, 14: 20170734.).

Other examples of potential Red Queen dynamics include organisms that affect the physical environment experienced by other species, such as plants that constitute structural habitat (e.g., tank bromeliads, which provide breeding habitat for frog species and invertebrates), or organisms that modify the physical and chemical environments utilized by several other taxa (e.g., fungi and earthworms that change soil and water chemistry). Organismal interactions such as those, which benefit at least one member of a local species assemblage, are referred to as biotic facilitation (Zélé et al. 2018Zélé, F.; Magalhães, S.; Kéfi, S.; Duncan, A.B. 2018. Ecology and evolution of facilitation among symbionts. Nature Communications, 9: 4869. doi.org/10.1038/s41467-018-06779-w
https://doi.org/10.1038/s41467-018-06779... ). Below, we provide several examples of how biotic interactions have facilitated the evolution of Amazonian diversity.

Host-parasite interactions: Because the species composition of many parasite groups often tracks that of their hosts, it is possible to estimate a minimum number of parasite species by comparison with the diversity of their host taxa (e.g., McNew et al. 2021McNew, S.M.; Barrow, L.N.; Williamson, J.L.; Galen, S.C.; Skeen, H.R.; DuBay, S.G.; et al. 2021. Contrasting drivers of diversity in host and parasites across the tropical Andes. Proceedings of the Natural Academy of Sciences 118: e2010714118.; but see Weckstein 2004). Given that many fish parasites exhibit strong host-specificity, it is believed that the actual diversity of the parasites could rival the immense diversity of their fish hosts (Salgado-Maldonado et al. 2016Salgado-Maldonado, G.; Novelo-Turcotte, M.T.; Caspeta-Mandujano, J.M.; Vazquez-Hurtado, G.; Quiroz-Martínez, B.; Mercado-Silva, N.; Favila, M.2016. Host specificity and the structure of helminth parasite communities of fishes in a Neotropical river in Mexico. Parasite 23: 61. doi.org/10.1051%2Fparasite%2F2016073
https://doi.org/10.1051%2Fparasite%2F201... ). At present, only about 300 species of Neotropical monogenoid flatworms are described, all ectoparasites of fish gills and the external body surface; however, these numbers are rising rapidly due to ongoing taxonomic research (see Vianna and Boeger 2019Vianna, R.T.; Boeger, W.A. 2019. Neotropical Monogenoidea. 60. Two new species of Gyrodactylus (Monogenoidea: Gyrodactylidae) from the armored-catfish, Pareiorhaphis parmula Pereira (Loricariidae) and from the cascarudo, Callichthys callichthys (Linnaeus) (Callichthyidae) from Brazil. Zootaxa 4551: 87-93.). Moreover, tight associations between helminth (flatworm and roundworm) and haemosporidian (Plasmodium) parasites and host species have been reported in many groups of Amazonian vertebrates, including fishes (Thatcher 2006Thatcher, V.E. 2006. Amazon Fish Parasites. Pensoft Publishers, Sofia-Moscow, 508p.), amphibians and reptiles (McAllister et al. 2010McAllister, C.T.; Bursey, C.R.; Freed, P.S. 2010. Helminth parasites of amphibians and reptiles from the Ucayali region, Peru. Journal of Parasitology 96: 444-447.), and birds (Fecchio et al. 2018Fecchio, A.; Pinheiro, R.; Felix, G.; Faria, I.P.; Pinho, J.B.; Lacorte, G.A.; et al. 2018. Host community similarity and geography shape the diversity and distribution of haemosporidian parasites in Amazonian birds. Ecography 41: 505-515.). The diversity of protozoan parasites of vertebrate hosts in the Amazon is presumably much greater still, based on what is known from better-studied faunas (Dobson et al. 2008Dobson, A.; Lafferty, K.D.; Kuris, A.M.; Hechinger, R.F.; Jetz, W. 2008. Homage to Linnaeus: how many parasites? How many hosts? Proceedings of the Natural Academy of Sciences 105: 11482-11489.). Even less is known about the diversity of Amazonian insect and plant parasites, but glimpses provided by recent studies using environmental genomics indicate the existence of extraordinary genetic and functional diversity of metazoan and protozoan parasites in the Amazon (Mahé et al. 2017Mahé, F.; Vargas, C. de; Bass, D.; Czech, L.; Stamatakis, A.; Lara, E.; et al. 2017. Parasites dominate hyperdiverse soil protist communities in Neotropical rainforests. Nature Ecology and Evolution 1: 0091. doi.org/10.1038/s41559-017-0091
https://doi.org/10.1038/s41559-017-0091... ; Puckett 2018Puckett, D.O. 2018. A survey of ant-associated fungal diversity in canopy bromeliads from the Ecuadorian Amazon. Doctoral thesis. Texas State University, USA, 52p (https://digital.library.txstate.edu/bitstream/handle/10877/7881/PUCKETT-THESIS-2018.pdf?sequence=1).
https://digital.library.txstate.edu/bits... ).

Niche construction: Biological diversity also contributes to the evolution of more diversity through the many ways by which organisms modify their external environments. The process by which organismal behaviors alter their local environments is called niche construction, which also affects the ecological conditions for all organisms in a local assemblage (Odling-Smee et al. 2013Odling-Smee, F.J.; Laland, K.N.; Feldman, M.W. 2013. Niche Construction: The Neglected Process in Evolution (MPB-37). Princeton University Press, New Jersey, 488p.). Organismal behaviors strongly affect and even create many important habitats in the Amazon. These activities include nest-burrow construction and fruit-seed-pollen dispersal by animals, the formation of vegetation structure and shade by plants, and the roles of plants, fungi, and soil or water microbes in nutrient and energy cycling, soil and water chemistry, and fire regimes (Mueller et al. 2016Mueller, R.C.; Rodrigues, J.L.M.; Nüsslein, K.; Bohannan, B.J.M. 2016. Land use change in the Amazon rain forest favours generalist fungi. Functional Ecology 30: 1845-1853.; Santos-Júnior et al. 2017Santos-Júnior, C.D.; Kishi, L.T.; Toyama, D.; Soares-Acosta, A.; Souza Oliveira, T.C.; de Mirando, F.P.; Henrique-Silva, F. 2017. Metagenome sequencing of prokaryotic microbiota collected from rivers in the upper Amazon basin. Genome Announc 5: e01450-16. doi.org/10.1128/genomea.01450-16
https://doi.org/10.1128/genomea.01450-16... ). Earthworms (Clitellata, Annelida) represent a classic example of how niche construction elevates habitat heterogeneity and biodiversity in the Amazon. Earthworms are important ecosystem engineers, whose activitiy helps to mineralize soil organic matter, construct and maintain soil structure, stimulate plant growth, and protect plants from pests (Marichal et al. 2017Marichal, R.; Praxedes, C.; Decaëns, T.; Grimaldi, M.; Oszwald, J.; Brown, G.G.; et al. 2017. Earthworm functional traits, landscape degradation and ecosystem services in the Brazilian Amazon deforestation arc. European Journal of Soil Biology 83: 43-51.). Several other Amazonian taxa are also important engineers of terrestrial ecosystems, including fungi (Palin et al. 2011Palin, O.F.; Eggleton, P.; Malhi, Y.; Girardin, C.A.J.; Rozas-Dávila, A.; Parr, C.L.2011. Termite diversity along an Amazon--Andes elevation gradient, Peru. Biotropica 43: 100-107.), termites (Duran-Bautista et al. 2020Duran-Bautista, E.H.; Armbrecht, I.; Acioli, A.N.S.; Suárez, J.C.; Romero, M.; Quintero, M.; Lavelle, P. 2020. Termites as indicators of soil ecosystem services in transformed amazon landscapes. Ecological Indicators 117: 106550. ), and ants (Folgarait 1998Folgarait, P.J. 1998. Ant biodiversity and its relationship to ecosystem functioning: A review. Biodiversity and Conservation 7: 1221-1244.).

Keystone species: The high number of fish species in aquatic Amazonian ecosystems can strongly affect nutrient and energy cycling (Winemiller and Jepsen 1998Winemiller, K.O.; Jepsen, D.B. 1998. Effects of seasonality and fish movement on tropical river food webs. Journal of Fish Biology 53: 267-296.; Arruda et al. 2017Arruda, D.M.; Schaefer, C.E.G.R.; Fonseca, R.S.; Solar, R.R.C.; Fernandes-Filho, E.I. 2017. Vegetation cover of Brazil in the last 21 ka: new insights into the Amazonian refugia and Pleistocenic arc hypotheses. Global Ecology and Biogeography 27: 47-56.). A striking example is the ecological role of the “coporo” or “sábalo” (Prochilodus mariaeEigenmann, 1922Eigenmann, C.H. 1922. The fishes of western South America, Part I. The fresh-water fishes of northwestern South America, including Colombia, Panama, and the Pacific slopes of Ecuador and Peru, together with an appendix upon the fishes of the Rio Meta in Colombia. Memoirs of the Carnegie Museum 9: 1-346.), a detritivorous and migratory characiform fish that is functionally important in Andean foothill streams of the western Amazon and Orinoco basins. Selective exclusion of this single species qualitatively changes the structure of local aquatic communities, as measured by sediment accrual and the composition of algal and invertebrate assemblages (Flecker 1996Flecker, A.S. 1996. Ecosystem engineering by a dominant detritivore in a diverse tropical stream. Ecology 77: 1845-1854.). Another example is provided by planktivorous electric fishes (Gymnotiformes) that constitute the base of aquatic food webs in the Amazon and Orinoco basins (Lundberg et al. 1987Lundberg, J.G.; Lewis, W.M.; Saunders, J.F.; Mago-Leccia, F. 1987. A major food web component in the Orinoco River channel: evidence from planktivorous electric fishes. Science 237: 81-83.; Fernandes et al. 2004Fernandes, C.C.; Podos, J.; Lundberg, J.G. 2004. Amazonian ecology: Tributaries enhance the diversity of electric fishes. Science 305: 1960-1962.). Because these food webs are essential to support the regional fisheries on which millions of Amazonian people depend as a primary source of animal protein (Goulding et al. 2019Goulding, M.; Venticinque, E.; Ribeiro, M.L. de B.; Barthem, R.B.; Leite, R.G.; Forsberg, B.; et al. 2019. Ecosystem-based management of Amazon fisheries and wetlands. Fish and Fisheries 20: 138-158.), planktivorous fishes are keystone species to human-dominated Amazonian landscapes.

Predator-prey interactions and the evolution of chemical diversity (Figure 10): Predator-prey dynamics is one of the most powerful evolutionary forces in nature, resulting in a myriad of strategies and weaponry to prey or avoid predation. Some long-evolved interactions between Amazonian species are responsible for the generation and accumulation of natural products amenable to bioprospection. Amazonian poison frogs (family Dendrobatidae), for instance, are known to sequester chemical defenses from the arthropod prey that they feed upon (Saporito et al. 2011Saporito, R.A.; Donnelly, M.A.; Spande, T.F.; Garraffo, H.M. 2011. A review of chemical ecology in poison frogs. Chemoecology 22: 159-168. and references therein). These alkaloids are used by indigenous people and are explored by the medical community and the pharmaceutical industry (Daly et al. 2000Daly, J.W.; Martin Garraffo, H.; Spande, T.F.; Decker, M.W.; Sullivan, J.P.; Williams, M. 2000. Alkaloids from frog skin: The discovery of epibatidine and the potential for developing novel non-opioid analgesics. Natural Product Reports 17: 131-135.; Cordell et al. 2001Cordell, G.A.; Quinn-Beattie, M.L.; Farnsworth, N.R. 2001. The potential of alkaloids in drug discovery. Phytotherapy Research 15: 183-205.; Philippe and Angenot 2005Philippe, G.; Angenot, L. 2005. Recent developments in the field of arrow and dart poisons. Journal of Ethnopharmacology 100: 85-91.). Mites, ants, beetles, and millipedes have all been flagged as sources of alkaloids for poison frogs worldwide (Saporito et al. 2009Saporito, R.A.; Spande, T.F.; Garraffo, H.M.; Donnelly, M.A. 2009. Arthropod alkaloids in poison frogs: a review of the dietary hypothesis. Heterocycles 79: 277-297.; McGugan et al. 2016McGugan, J.R.; Byrd, G.D.; Roland, A.B.; Caty, S.N.; Kabir, N.; Tapia, E.E.; Trauger, S.A.; Coloma, L.A.; O´Connell, L.A.2016. Ant and mite diversity drives toxin variation in the Little Devil Poison frog. Journal of Chemical Ecology 42: 537-551.), and several species of frogs are able to further modify them chemically, leading to other alkaloids (Daly et al. 2003Daly, J.W.; Garraffo, H.M.; Spande, T.F.; Clark, V.C.; Ma, J.; Ziffer, H.; Cover Jr, J.F. 2003. Evidence for an enantioselective pumiliotoxin 7-hydroxylase in dendrobatid poison frogs of the genus Dendrobates. Proceedings of the Natural Academy of Sciences 100: 11092-11097., 2009Daly, J.W.; Ware, N.; Saporito, R.A.; Spande, T.F.; Garrafo, H.M. 2009. N-methyldecahydroquinolines: an unexpected class of alkaloids from Amazonian poison frogs (Dendrobatidae). Journal of Natural Products 72: 1110-1114.). Moreover, although more research is pending, some poison frog alkaloids appear to be derived from plants. This reflects the complex trophic interactions between plants, the arthropods that feed on them, and the frogs that prey on those arthropods (Tokuyama and Daly 1983Tokuyama, T.; Daly, J.W. 1983. Steroidal alkaloids (batrachotoxins and 4$β$-hydroxybatrachotoxins),“indole alkaloids”(calycanthine and chimonanthine) and a piperidinyldipyridin. Tetrahedron 39: 41-47.).

The potential of plants for the Amazonian bioeconomy is enormous. For instance, Amazonian people have known the effects of plant alkaloids as medicine for centuries. Plant alkaloids evolved as a defense mechanism against herbivory (Gauld et al. 1992Gauld, I.D.; Gaston, K.J.; Janzen, D.H. 1992. Plant allelochemicals, tritrophic interactions and the anomalous diversity of tropical parasitoids: The” nasty” host hypothesis. Oikos 65: 353-357.) and are synthesized in the roots, stems (e.g., banisterine), leaves (e.g., caffeine), flowers, fruits, seeds (e.g., strychnine), and bark (e.g., quinine). Some of the known plant alkaloids include the antimalarial quinine, hunting poisons (barbasco, curare), stimulants (guayusa, nicotine, coca), and ritualistic herbs (ayahuasca, scopolamine) (Heinrich et al. 2021Heinrich, M.; Mah, J.; Amirkia, V. 2021. Alkaloids used as medicines: structural phytochemistry meets biodiversity: an update and forward look. Molecules, 26: 1836. doi:10.3390/molecules26071836
https://doi.org/10.3390/molecules2607183... ; Uzor 2020Uzor, P.F. 2020. Alkaloids from plants with antimalarial activity: a review of recent studies. Evidence-Based Complementary and Alternative Medicine 2020: 8749083. ). Many of these compounds are precursors for modern medicine; however, due to their complex chemical structures, only a fraction go into commercial production (Reis et al. 2019Reis, A.; Magne, K.; Massot, S.; Tallini, L.R.; Scopel, M.; Bastida, J.; Ratet, P.; Zuanazzi, J.A.S. 2019. Amaryllidaceae alkaloids: identification and partial characterization of montanine production in Rhodophiala bifida plant. Scientific Reports 9: 8471. doi.org/10.1038/s41598-019-44746-7
https://doi.org/10.1038/s41598-019-44746... ). Moreover, allochemicals from some Amazonian plants might prove useful as sources of biodegradable pesticides; the “piquiá” (Caryocar), for instance, produces a compound that seems to be toxic to the leaf-cutter ant (Atta), which causes large financial losses to South American agriculture each year (Plotkin 1988Plotkin, M.J. 1988. The Outlook for New Agricultural and Industrial Products from the Tropics. National Academy Press, Washington, DC, 538p.). Today, entire companies are dedicated to screening chemical compounds in plants, insects, and frogs, in search for potential drugs. Natural products and their derivatives have been, and continue to be, a primary source in the drug discovery domain (Lopes et al. 2019Lopes, A.A.; Chioca, B.; Musquiari, B.; Crevelin, E.J.; de C. França, S.; da Silva, M.F.F. 2019. Unnatural spirocyclic oxindole alkaloids biosynthesis in Uncaria guianensis. Scientific Reports 9: 11349. doi: 10.1038/s41598-019-47706-3
https://doi.org/10.1038/s41598-019-47706... ).

SPECIES LOSS AND TURNOVER IN AMAZONIA: LESSONS FROM THE FOSSIL RECORD

Extinction rates vary throughout evolutionary time. It has been estimated that more than 99% of all species that have ever lived on Earth are now extinct (Raup 1986Raup, D.M. 1986. Biological extinction in earth history. Science 231: 1528-1533.). The fossil record offers unique evidence to study extinctions. Paleontologists have identified 18 time intervals with elevated extinction rates over the past 540 million years, five of which are classified as mass extinction events (Bambach 2006Bambach, R.K. 2006. Phanerozoic biodiversity mass extinctions. Annual Review of Earth and Planetary Science 34: 127-155.). Models based on DNA analyses and the fossil record, especially of marine invertebrates and mammals, show that background extinction rates over geological time have ranged from 0.02 to 0.14 extinctions per million species per year. In turn, speciation rates are estimated to be about twice this value, ranging from 0.05 to 0.20 speciation events per million species per year (Jablonski 2005; De Vos et al. 2015). The fossil record also shows changes in biodiversity over geological time with occasional catastrophic mass extinction events, when extinction rates increased by thousands of times, eliminating large clades with distinctive genes and body plans (Bambach 2006; Ceballos et al. 2015Ceballos, G.; Ehrlich, P.R.; Barnosky, A.D.; García, A.; Pringle, M.R.; Palmer, T.M. 2015. Accelerated modern human--induced species losses: Entering the sixth mass extinction. Science Advances 1: e1400253.).

This understanding of the past allows us to put in perspective the wave of extinctions faced by the modern biota, which is estimated to be 1,000 to 10,000 times larger than the background rate, and therefore similar in scope to that of past mass extinction events (Barnosky et al. 2011Barnosky, A.; Matzke, N.; Tomiya, S.; Wogan, G.O.U.; Swartz, B.; Quental, T.B., et al. 2011. Has the Earth’s sixth mass extinction already arrived?. Nature 471: 51-57.; Ceballos et al. 2015Ceballos, G.; Ehrlich, P.R.; Barnosky, A.D.; García, A.; Pringle, M.R.; Palmer, T.M. 2015. Accelerated modern human--induced species losses: Entering the sixth mass extinction. Science Advances 1: e1400253.). While its causes are multiple, the increase in the concentration of carbon dioxide in the atmosphere, and the acidification of the oceans caused by human action, match the great natural environmental changes that triggered mass extinction events in the deep past.

Throughout its lengthy geological history, the Amazonian region has undergone extensive environmental changes, driven primarily by regional tectonic and global climatic forces. It once extended over most of northern South America, with lowlands characterized by alternating fluvial and lacustrine conditions and marginal marine embayments. Modern lineages of Amazonian organisms have survived and adapted to five major rearrangements of landforms and habitats during the Cenozoic (66-0 Ma), as follows (summarized from Val et al. 2021Val, P.; Figueiredo, J.; Melo, G.; Flantua, S.G.A.; Quesada, C.A.; Fan, Y.; et al. 2021. Chapter 1: Geological History and Geodiversity of the Amazon. In: Nobre, C.; Encalada, A.; Anderson, E.; Roca Alcazar, F.H.; Bustamante, M.; Mena, C.; et al. (Ed.). Amazon Assessment Report 2021 . United Nations Sustainable Development Solutions Network, New York, USA (https://www.theamazonwewant.org/spa-reports/).
https://www.theamazonwewant.org/spa-repo... , and references therein):

The Paleogene uplift of the central Andes, caused by plate subduction along the Pacific margin and the breakup of the Pacific plate (ca. 23 Ma), resulted in the establishment of a sub-Andean river basin draining north towards a large embayment of the Caribbean Sea. The basin extended over the area that is now occupied by the Colombian and Venezuelan Llanos.

Mountain building in the central and northern Andes narrowed the Caribbean influence and led to the origin and movement of mega-wetlands in the western Amazon ca. 22-10 Ma. The Pebas mega-wetland system resulted from this expansion, reaching more than 1 million km².

Intense Andean mountain building since the late-middle Miocene (last 10 Ma), which coincided with global fluctuations in sea level, prevented further marine influences in the western Amazon and along the northern Andean foreland basin. This retained much of the drainages that flowed into the Pacific and the Caribbean, and formed the wide floodplain named the Acre System.

From the end of the Miocene (ca. 7 Ma) on, further Andean uplift forced the mega-wetland to be completely drained and the onset of the modern Amazon River system. This led to the development of widespread river terrace systems with expanded terra firme rainforests.

The closure of the Central American Seaway and the emergence of the Panama Isthmus (ca. 13-3.5 Ma) provided opportunities for extensive migrations of North American lineages to both the Amazon and new montane habitats in the Andes.

The biotic responses to these immense environmental changes included dispersal and habitat shifts at the organismal level, adaptation and geographic range shifts at the population level, and speciation and extinction at the species level. While the geological record does not provide evidence of sudden mass extinction events during the Cenozoic in the Amazon, some groups of animals once abundant in both terrestrial and aquatic environments were extirpated by one or more of the aforementioned events, including species expected to provide a variety of ecological functions (Scheyer et al. 2013Scheyer, T.M.; Aguilera, O.A.; Delfino, M.; Fortier, D.C.; Carlini, A.A.; Sánchez, R.; Carrillo-Briceño, J.D.; Quiroz, L.; Sánchez-Villagra, M.R.2013. Crocodylian diversity peak and extinction in the Late Cenozoic of the northern Neotropics. Nature Communications 4: 1907. doi.org/10.1038/ncomms2940
https://doi.org/10.1038/ncomms2940... ).

Extinctions and Amazonian mega-wetlands (Figure 11)

The fossil record evidences pulses of extinctions in Amazonia that occurred in the transition from the lacustrine-fluvial Pebas to the fluvio-lacustrine Acre mega-wetland systems, in association with the origin of the modern transcontinental Amazon River, ca. 9-4.5 Ma (Albert et al. 2018Albert, J.S.; Val, P.; Hoorn, C. 2018. The changing course of the Amazon River in the Neogene: Center stage for Neotropical diversification. Neotropical Ichthyology 16(3): e180033.). The most significant extinctions were those affecting the rich and endemic lacustrine fauna, notably bivalve mollusks (Wesselingh and Ramos 2010Wesselingh, F.P.; Ramos, M-IF. 2010. Amazonian aquatic invertebrate faunas (Mollusca, Ostracoda) and their development over the past 30 million years. In:Hoorn, C.; Wesselingh, F.P. (Ed.). Amazonia: Landscape and Species Evolution. Wiley-Blackwell Publishing Ltd., Oxford, p.323-361.) and crocodilian reptiles (Riff et al. 2010Riff, D.R.; Romano, P.S.; Oliveira, G.R.; Aguilera, O.A. 2010. Neogene crocodile and turtle fauna in northern South America. In: Hoorn, C.; Wesselingh, F.P. (Ed.). Amazonia, Landscape and Species Evolution: A Look Into the Past. Blackwell Publishing, New York , p.259-280. ; Scheyer et al. 2013Scheyer, T.M.; Aguilera, O.A.; Delfino, M.; Fortier, D.C.; Carlini, A.A.; Sánchez, R.; Carrillo-Briceño, J.D.; Quiroz, L.; Sánchez-Villagra, M.R.2013. Crocodylian diversity peak and extinction in the Late Cenozoic of the northern Neotropics. Nature Communications 4: 1907. doi.org/10.1038/ncomms2940
https://doi.org/10.1038/ncomms2940... ; Salas-Gismondi et al. 2015Salas-Gismondi, R.; Flynn, J.J.; Baby, P.; Tejada-Lara, J.V.; Wessenlingh, F.P.; Antoine, P.O. 2015. A Miocene hyperdiverse crocodylian community reveals peculiar trophic dynamics in proto-Amazonian mega-wetlands. Proceedings of the Royal Society Series B Biological Sciences 282: 20142490.).

Mollusks and crocodilians are among the best represented clades in the fossil record of the Amazon; they exemplify the diversification and subsequent extinction of aquatic fauna in association with the evolution of mega-wetlands during the Neogene. About 85 species of mollusks were documented from the last stages of the Pebas System (Middle to Late Miocene). This fauna was dominated by Pachydontinae bivalves, which originated in coastal Pacific and Caribbean marine waters. Marine mollusks colonized the western Amazon during pulses of marine ingressions ca. 23-15 Ma, together with other aquatic animal groups such as freshwater stingrays, anchovies, needlefishes, dolphins, manatees, and various parasitic lineages (Lovejoy et al. 1998Lovejoy, N.R.; Bermingham, E.; Martin, A.P. 1998. Marine incursion into South America. Nature 396: 421-422.). Small, blunt-snouted crocodilians evolved crushing dentitions that allowed them to feed on hard-shelled organisms and prey on the Pebasian malacofauna (Salas-Gismondi et al. 2015Salas-Gismondi, R.; Flynn, J.J.; Baby, P.; Tejada-Lara, J.V.; Wessenlingh, F.P.; Antoine, P.O. 2015. A Miocene hyperdiverse crocodylian community reveals peculiar trophic dynamics in proto-Amazonian mega-wetlands. Proceedings of the Royal Society Series B Biological Sciences 282: 20142490.). The crocodilian fauna of the Pebas system also included species specialized in eating fish (long-snouted gharials), large to giant prey (Purussaurus), “gulp-feeding” of small prey (Mourasuchus), and generalized small prey (Caiman and Paleosuchus). On land, the last representatives of an extinct group of terrestrial crocodyliforms, the Sebecidae, competed with mammals as top-predators. This group included the largest terrestrial predator of the Amazon during the Middle Miocene, Barinasuchus arveloiPaolillo and Linares, 2007Paolillo, A.; Linares, O.J. 2007. Nuevos cocodrilos sebecosuchia del Cenozoico suramericano (Mesosuchia: Crocodylia). Paleobiologia Neotropical 3: 1-25., from the Parangula Formation in Venezuela, which reached up to 6 meters in length (Paolillo and Linares 2007). Because top predators are very susceptible to drastic environmental changes, it is possible that the changes in the mega-wetland impacted the survivorship of these organisms (Salas-Gismondi et.al. 2015).

With the end of the Pebas System, most of the associated molluscan fauna became extinct. Consequently, modern Amazonian mollusk diversity is remarkably poor and dominated by cosmopolitan freshwater groups, such as freshwater mussels, clams, and snails (Wesselingh and Ramos 2010Wesselingh, F.P.; Ramos, M-IF. 2010. Amazonian aquatic invertebrate faunas (Mollusca, Ostracoda) and their development over the past 30 million years. In:Hoorn, C.; Wesselingh, F.P. (Ed.). Amazonia: Landscape and Species Evolution. Wiley-Blackwell Publishing Ltd., Oxford, p.323-361.). The disappearance of the Pebasian endemic mollusks adversely affected crocodilians, who then suffered their first large-scale extinction event (Salas-Gismondi et al. 2015Salas-Gismondi, R.; Flynn, J.J.; Baby, P.; Tejada-Lara, J.V.; Wessenlingh, F.P.; Antoine, P.O. 2015. A Miocene hyperdiverse crocodylian community reveals peculiar trophic dynamics in proto-Amazonian mega-wetlands. Proceedings of the Royal Society Series B Biological Sciences 282: 20142490.; Souza-Filho et al. 2019Souza-Filho, J.P.; Souza, R.G.; Hsiou, A.S.; Riff, D.; Guilherme, E.; Negri, F.R.; Cidade, G.M.2018. A new caimanine (Crocodylia, Alligatoroidea) species from the Solimões Formation of Brazil and the phylogeny of Caimaninae. Journal of Vertebrate Paleontology 38: e1528450.).

Still, most of the crocodilian lineages survived to the formation of the Acre System ca. 10-7 Ma. In the extensive wetlands of the Acre System flourished a notable diversity of around 30 species showing morphological variation greater than any other crocodilian fauna, extant or extinct (Riff et al. 2010Riff, D.R.; Romano, P.S.; Oliveira, G.R.; Aguilera, O.A. 2010. Neogene crocodile and turtle fauna in northern South America. In: Hoorn, C.; Wesselingh, F.P. (Ed.). Amazonia, Landscape and Species Evolution: A Look Into the Past. Blackwell Publishing, New York , p.259-280. ; Cidade et al. 2019Cidade, G.M.; Fortier, D.; Hsiou, A.S. 2019. The crocodylomorph fauna of the Cenozoic of South America and its evolutionary history: A review. Journal of South America Earth Science 90: 392-411.). Similarly, the period witnessed a large diversity of turtles, including one of the largest turtles that ever lived on Earth, more than 2.5 m in length and with an estimated body mass of about 1,000 kg (Cadena et al. 2020Cadena, E.A.; Scheyer, T.M.; Carrillo-Briceño, J.D.; Sánchez, R.; Pardo, A.V.M.; Hansen, D.M.; Sánchez-Viññagra, M.R. 2020b. The anatomy, paleobiology, and evolutionary relationships of the largest extinct side-necked turtle. Science Advances 6: eaay4593.b). Beyond some generalist taxa that have been present in the Amazon since the Middle Miocene through to today (e.g., Caiman, Melanosuchus, and Paleosuchus), the availability of large-bodied prey and competition with other aquatic predators likely triggered the evolution of giant top predators. Examples include Purussaurus brasiliensisBarbosa-Rodrigues, 1892Barbosa-Rodrigues, J. 1892. Les Reptiles fossiles de la vallée de l’Amazone. Vellosia, 2: 41-46., with its 12-meter long body (Aureliano et al. 2015Aureliano, T.; Ghilardi, A.M.; Guilherme, E.; Souza-Filho, J.P.; Cavalcanti, M.; Riff, D. 2015. Morphometry, bite-force, and paleobiology of the Late Miocene Caiman Purussaurus brasiliensis. PLoS One 10: e0117944.), highly specialized forms such as the bizarre species in the genus Mourasuchus, known for their long, wide, dorsoventrally flat skull, and tiny dentition (Cidade et al. 2019), and the long-snouted gharials, some also giant in size (Riff et al. 2010).

The transition from the Acre System to the modern fluvial and terra firme Amazonian environments, starting at around 7 Ma, led to a large extinction event affecting crocodilian fauna. All specialized forms, from small to giant, vanished. The extant South American crocodilians are now a small fraction of their former diversity. Entire body types and ecological roles among aquatic fauna disappeared after the demise of the Amazonian Miocene mega-wetlands.

In stark contrast to the turnover of mollusks and crocodilians, modern Amazonian fish fauna has remained largely unchanged at the genus level and above. Direct evidence from the fossil record indicates that all but one fossil genus known from the Miocene is still living (Lundberg et al. 1998Lundberg, J.G.; Marshall, L.G.; Guerrero, J.; Horton, B.; Malabarba, M.C.S.L.; Wesselingh, F. 1998. The stage for Neotropical fish diversification: a history of tropical South American rivers. In: Malabarba, L.R.; Reis, R.E.; Vari, R.P.; Lucena, Z.M.; Lucena, C.A.S. (Ed.). Phylogeny and Classification of Neotropical Fishes, Part 1: Fossils and Geological Evidence, Edipucrs, Porto Alegre, p.13-48.). Further, molecular phylogenies of most Amazonian fish genera are now available, including more than 1,000 of the 3,000 known species (van der Sleen and Albert 2017Sleen, P. van der; Albert, J.S. 2017. Field Guide to the Fishes of the Amazon, Orinoco, and Guianas. Princeton University Press, New Jersey 115:460p.). In combination, these datasets indicate that most genera that compose today’s rich Amazonian fish fauna were present by the middle Miocene (ca. 15-10 Ma). The evolutionary origins of most Amazonian fish forms and their ecological roles predate the geological assembly of the modern Amazon and Orinoco basins during the Late Miocene and Pliocene (ca. 9-4.5 Ma; Albert et al. 2011bAlbert, J.S.; Carvalho, T.P.; Petry, P.; Holder, M.A.; Maxime, L.E.; Espino, J.; Corahua, I.; Quispe, R.; Rengifo, B.; Ortega, H.; Reis, R. 2011b. Aquatic biodiversity in the Amazon: habitat specialization and geographic isolation promote species richness. Animals 1: 205-241.).

The American Biotic Interchange and the influence of humans on Amazonian biota

The tectonics that elevated the Andes and caused the great environmental changes also elevated the terrestrial route that ended a long-lasting isolation of South America from other continents during most of the Cenozoic (Croft 2016Croft, D.A. 2016. Horned Armadillos and Rafting Monkeys: The Fascinating Fossil Mammals of South America. Indiana University Press, Bloomington, Indiana, USA, 320p.). This isolation, which led South America to harbor a peculiar and endemic mammalian megafauna (Defler 2019Defler, T. 2019. History of Terrestrial Mammals in South America. Springer International Publishing, Cham, 372p.), ceased when the formation of the Isthmus of Panama facilitated the biotic interchange between North and South America, through the event known as the Great American Biotic Interchange (GABI; Stehli and Webb 1985Stehli, F.G.; Webb, S.D. 1985. The Great American biotic Interchange. Springer Science & Business Media, New York, 532p.). This connection had great implications for the historical assembly of the Amazonian fauna and flora. Plants, which have a greater dispersal ability, dispersed before animals did, even before a land bridge was fully established between the continents (ca. 50-20 Ma; Cody et al. 2010Cody, S.; Richardson, J.E.; Rull, V.; Ellis, C.; Pennington, T.2010. The great American biotic interchange revisited. Ecography 33: 326-332.). The fossil record of terrestrial mammals, which is abundant in both continents and therefore illustrates dispersal dynamics, shows that the interchange was initially symmetrical, but followed by an increasing dominance of mammals of North American origin in South America (Marshall et al. 1982Marshall, L.G.; Webb, S.D.; Sepkoski, J.J.; Raup, D.M. 1982. Mammalian evolution and the great American interchange. Science 215: 1351-1357.), caused by a higher extinction of South American mammals (Carrillo et al. 2020Carrillo, J.D.; Faurby, S.; Silvestro, D.; Zizka, A.; Jaramillo, C.; Bacon, C.D.; Antonelli, A. 2020. Disproportionate extinction of South American mammals drove the asymmetry of the Great American Biotic Interchange. Proceedings of the Natural Academy of Sciences 117: 26281-26287. ). Because the fossil record mostly reflects patterns of the temperate regions (Carrillo et al. 2015Carrillo, J.D.; Forasiepi, A.; Jaramillo, C.; Sánchez-Villagra, M.R. 2015. Neotropical mammal diversity and the Great American Biotic Interchange: Spatial and temporal variation in South America’s fossil record. Frontiers in Genetics 5: 451. doi: 10.3389/fgene.2014.00451
https://doi.org/10.3389/fgene.2014.00451... ), molecular phylogenies have also been employed to understand the GABI; they show that dispersal from South to North America occurred most likely between the tropical regions of the two continents (Bacon et al. 2015Bacon, C.D.; Silvestro, D.; Jaramillo, C.; Smith, B.T.; Chakrabarty, P.; Antonelli, A. 2015. Biological evidence supports an early and complex emergence of the Isthmus of Panama. Proceedings of the Natural Academy of Sciences 112: 6110-6115.). Indeed, many groups of mammals that are found today in tropical forests from Central America originated in the Amazon, and many of the Neotropical placental mammals, such as felids, canids, peccaries, deer, otters, tree squirrels, camelids, as well as the extinct proboscideans and horses, are descendants of North American migrants (Webb 1991Webb, S.D. 1991. Ecogeography and the great American interchange. Paleobiology 17: 266-280.; Antonelli et al. 2018Antonelli, A.; Zizka, A.; Carvalho, F.A.; Scharn, R.; Bacon, C.D.; Silvestro, D.; Condamine, F.L. 2018. Amazonia is the primary source of Neotropical biodiversity. Proceedings of the Natural Academy of Sciences 115: 6034-6039.).

Global-scale extinction of megafauna impacted the Amazon at the end of the Pleistocene. It reduced megafauna diversity worldwide by two thirds approximately 50,000-10,000 years ago (Barnosky et al. 2004Barnosky, A.D.; Koch, P.L.; Feranec, R.S.; Wing, S.L.; Shabel, A.B. 2004. Assessing the causes of Late Pleistocene extinctions on the continents. Science 306: 70-75.). Hunting by humans was an important cause of extinctions, in some regions in synergy with climate change (Barnosky et al. 2004; Barnosky and Lindsey, 2010Barnosky, A.D.; Lindsey, E.L. 2010. Timing of Quaternary megafaunal extinction in South America in relation to human arrival and climate change. Quaternary International 217: 10-29.). South America lost about 83% of its megafauna (adult body weight > 44 kg sensu Martin 1973Martin, P.S. 1973. The discovery of America: the first Americans may have swept the Western Hemisphere and decimated its fauna within 1000 years. Science 179: 969-974.) during this extinction event, more than any other continent (Barnosky and Lindsey 2010Barnosky, A.D.; Lindsey, E.L. 2010. Timing of Quaternary megafaunal extinction in South America in relation to human arrival and climate change. Quaternary International 217: 10-29.; Prado et al. 2015Prado, J.L.; Martinez-Maza, C.; Alberdi, M.T. 2015. Megafauna extinction in South America: A new chronology for the Argentine Pampas. Palaeogeography Palaeoclimatology Palaeoecology 425: 41-49.). This loss affected some important ecosystem processes. Because large animals play an important role in the spatial movement of nutrients from areas of high to low nutrient concentration, megafauna extinctions resulted in reduced nutrient flows (Doughty et al. 2016aDoughty, C.E.; Roman, J.; Faurby, S.; Wolf, A.; Haque, A.; Bakker, E.S.; Malhi, Y.; Dunning, J.B.; Svenning, C.J. 2015. Global nutrient transport in a world of giants. Proceedings of the Natural Academy of Sciences 113: 868-873.). Extinctions likely reduced the population size of large-seeded tree species that depended on large herbivores for dispersal. In the Amazon basin, the size range of large seeded trees decreased by about 26-31% (Doughty et al. 2016bDoughty, C.E.; Wolf, A.; Morueta-Holme, N.; Jørgensen, P.M.; Sandel, B.; Violle, C.; et al. 2015. Megafauna extinction, tree species range reduction, and carbon storage in Amazonian forests. Ecography 39: 194-203.). Furthermore, because fruit size correlates with wood density, the reduction of large-seeded trees dispersed by animals is thought to have reduced the carbon content in the Amazon by about 1.5% after megafauna extinction (Doughty et al. 2016bDoughty, C.E.; Wolf, A.; Morueta-Holme, N.; Jørgensen, P.M.; Sandel, B.; Violle, C.; et al. 2015. Megafauna extinction, tree species range reduction, and carbon storage in Amazonian forests. Ecography 39: 194-203.).

The global fossil record shows us that species with specialized diet, larger body size, broader geographic distribution, longer life span, slower reproduction rate, and fewer offspring, are more susceptible to change and in greater risk of extinction (McKinney 1997McKinney, M.L. 1997. Extinction Vulnerability and Selectivity: Combining Ecological and Paleontological Views. Annual Review of Ecology and Systematics 28: 495-516.; Purvis et al. 2000Purvis, A.; Gittleman, J.L.; Cowlishaw, G.; Mace, G.M. 2000. Predicting extinction risk in declining species. Proceedings of the Royal Society London Series B Biological Sciences 267: 1947-1952.). On the other hand, short-lived species with rapid population growth, more generalist diet, and with high phenotypic plasticity are better suited to adapt and cope with environmental change (Chichorro et al. 2019Chichorro, F.; Juslén, A.; Cardoso, P. 2019. A review of the relation between species traits and extinction risk. Biological Conservation 237: 220-229.). The Amazonian fossil record of Cenozoic crocodilians illustrates this pattern, with large and dietarily-specialized forms occupying large areas that were heavily impacted by environmental change (Scheyer et al. 2013Scheyer, T.M.; Aguilera, O.A.; Delfino, M.; Fortier, D.C.; Carlini, A.A.; Sánchez, R.; Carrillo-Briceño, J.D.; Quiroz, L.; Sánchez-Villagra, M.R.2013. Crocodylian diversity peak and extinction in the Late Cenozoic of the northern Neotropics. Nature Communications 4: 1907. doi.org/10.1038/ncomms2940
https://doi.org/10.1038/ncomms2940... ; Cidade et al. 2019Cidade, G.M.; Fortier, D.; Hsiou, A.S. 2019. The crocodylomorph fauna of the Cenozoic of South America and its evolutionary history: A review. Journal of South America Earth Science 90: 392-411.). In the face of environmental pressures currently faced by the Amazon, such as deforestation, fires, hydroelectric dams, and other anthropogenic disturbances (Escobar 2019Escobar, H. 2019. Amazon fires clearly linked to deforestation, scientists say. Science 365: 853. doi:10.1126/science.365.6456.853
https://doi.org/10.1126/science.365.6456... ; Albert et al. 2023), it is possible that species with more specialized diet might face greater extinction risk (Bodmer et al. 1997Bodmer, R.E.; Eisenberg, J.F.; Redford, K.H. 1997. Hunting and the likelihood of extinction of Amazonian mammals: Caza y Probabilidad de Extinción de Mamiferos Amazónicos. Conservation Biology 11: 460-466.; Shahabuddin and Ponte 2005Shahabuddin, G.; Ponte, C.A. 2005. Frugivorous butterfly species in tropical forest fragments: correlates of vulnerability to extinction. Biodiversity and Conservation 14: 1137-1152.; Benchimol and Peres 2015Benchimol, M.; Peres, C.A. 2015. Predicting local extinctions of Amazonian vertebrates in forest islands created by a mega dam. Biological Conservation 187: 61-72.).

Humans may have occupied the Americas much earlier than previously thought, with records dating back to 33,000-31,000 years ago in Mexico (Ardelean et al. 2020Ardelean, C.F.; Becerra-Valdivia, L.; Pedersen, M.W.; Schwenninger, J.L.; Oviatt, C.G.; Marcías-Quintero, J.I.; et al. 2020. Evidence of human occupation in Mexico around the Last Glacial Maximum. Nature 584: 87-92.) and 13,000 years ago in lower latitudes (Roosevelt et al. 2013Roosevelt, A.C. 2013. The Amazon and the Anthropocene: 13,000 years of human influence in a tropical rainforest. Anthropocene 4: 69-87.). As such, human impact on local ecosystems, including the Amazon, has a lengthy history (Levis et al. 2017Levis, C.; Costa, F.R.C.; Bongers, F.; Peña-Claros, M.; Junqueira, A.B.; Neves, E.G.; et al. 2017. Persistent effects of pre-Columbian plant domestication on Amazonian forest composition. Science 355: 925-931.; Watling et al. 2017Watling, J.; Iriarte, J.; Mayle, F.E.; Schaan, D.; Pessenda, L.C.R.; Loader, N.J.; Street-Perrott, F.A.; Dickau, R.E.; Damasceno, A.; Ranzi, A. 2017. Impact of pre-Columbian “geoglyph” builders on Amazonian forests. Proceedings of the Natural Academy of Sciences 114: 1868-1873.). Studies from multiple disciplines suggest that pre-Columbian human settlements in the Amazon basin were complex and culturally diverse, and that they influenced current patterns of Amazonian biodiversity (Heckenberger and Neves 2009Heckenberger, M.; Neves, E.G. 2009. Amazonian archaeology. Annual Review of Anthropology 38: 251-266.; Shepard and Ramirez 2011Shepard, G.H.; Ramirez, H. 2011. “Made in Brazil”: Human dispersal of the Brazil Nut (Bertholletia excelsa, Lecythidaceae) in ancient Amazonia. Economic Botany 65: 44-65.).

Although human influence in the Amazon basin has changed through time, one of the most outstanding legacies of these interactions over many millennia is the abundance and widespread distribution of plant species commonly used by indigenous peoples. These trees, now identified as hyperdominant, include the Brazil nut (Bertholletia excelsaHumboldt and Bonpland, 1807Humboldt, F.H.A. von; Bonplant, A. 1807. Protologue of Bertholletia excels. Plantae Aequinoctiales, 1: 122-127.), several species of palms (e.g., Astrocaryum murumuruMartius, 1824Martius, C.F.P. von. 1824. Historia Naturalis Palmarum, Vol. 2 . T.O. Weigel, Lipsiae, 70p., Oenocarpus bacaba), cacao (Theobroma cacao,Linnaeus, 1753Linnaeus, C. 1753. Species plantarum: exhibentes plantas rite cognitas, ad genera relatas, cum differentiis specificis, nominibus trivialibus, synonymis selectis, locis natalibus, secundum systema sexuale digestas. Tomus I & II. Impensis Laurentii Salvii, Stockholm, 1146p.), and the caimito (Pouteria caimito [Ruiz & Pavón, 1802]) (Shepard and Ramirez 2011Shepard, G.H.; Ramirez, H. 2011. “Made in Brazil”: Human dispersal of the Brazil Nut (Bertholletia excelsa, Lecythidaceae) in ancient Amazonia. Economic Botany 65: 44-65.; Levis et al. 2017Levis, C.; Costa, F.R.C.; Bongers, F.; Peña-Claros, M.; Junqueira, A.B.; Neves, E.G.; et al. 2017. Persistent effects of pre-Columbian plant domestication on Amazonian forest composition. Science 355: 925-931.). These domesticated/managed species have been vital to the livelihood of Amazonian peoples, who have interacted with the forest for many centuries (Levis et al. 2017; Montoya et al. 2020Montoya, E.; Lombardo, U.; Levis, C.; et al. 2020. Human contribution to Amazonian plant diversity: Legacy of pre-Columbian land use in modern plant communities. In: Rull, V.; Carnaval, A. (Ed.). Neotropical Diversification: Patterns and Processes. Springer, Cham , pp 495-520. ).

Accumulating evidence demonstrates that the socially and culturally complex pre-Columbian Amerindians modified the riverine, terra firme, and wetland areas of the Amazon, directly impacting the distribution of local species assemblages (Heckenberger 2005Heckenberger, M. 2005. The Ecology of Power: Culture, Place, and Personhood in the Southern Amazon, AD 1000-2000. Routledge, Oxfordshire, 430p.; Montoya et al. 2020Montoya, E.; Lombardo, U.; Levis, C.; et al. 2020. Human contribution to Amazonian plant diversity: Legacy of pre-Columbian land use in modern plant communities. In: Rull, V.; Carnaval, A. (Ed.). Neotropical Diversification: Patterns and Processes. Springer, Cham , pp 495-520. ). Examples include anthropogenic soils (terra preta) and artificial earthworks such as fish ponds, ring ditches, habitation mounds, and raised fields (Heckenberger and Neves 2009; Prestes-Carneiro et al. 2016Prestes-Carneiro, G.; Béarez, P.; Bailon, S.; Py-Daniel, A.R.; Neves, E.G. 2016. Subsistence fishery at Hatahara (750-1230 CE), a pre-Columbian central Amazonian village. Journal of Archaeological Science Reports 8: 454-462.). The magnitude of these changes varied considerably. In areas such as the Llano de Moxos (Bolivia), natives created a landscape that comprised approximately 4,700 artificial forest islands within a seasonally flooded savannah (Lombardo et al. 2020Lombardo, U.; Iriarte, J.; Hilbert, L.; Ruiz-Pérez, J.; Capriles, J.M.; Veit, H. 2020. Early Holocene crop cultivation and landscape modification in Amazonia. Nature 581: 190-193.). This region has been confirmed as a hotspot for early plant cultivation, including squash (Cucurbita sp.), at about 10,250 calibrated years before present (cal. yr bp), manioc (Manihot sp.) at about 10,350 cal. yr bp, and a secondary improvement center for the partially domesticated maize (Zea maysLinnaeus, 1753Linnaeus, C. 1753. Species plantarum: exhibentes plantas rite cognitas, ad genera relatas, cum differentiis specificis, nominibus trivialibus, synonymis selectis, locis natalibus, secundum systema sexuale digestas. Tomus I & II. Impensis Laurentii Salvii, Stockholm, 1146p.), at about 6,850 cal. yr bp (Kistler et al. 2018Kistler, L.; Yoshi Maezumi, S.; Souza, J.G. De; Przelomska, N.A.S.; Costa, F.M.; Smith, O.; et al. 2018. Multiproxy evidence highlights a complex evolutionary legacy of maize in South America. Science 362: 1309-1313.; Lombardo et al. 2020).

Changes across the Amazon basin accelerated with Portuguese and Spanish colonization in the past 500 years, and accelerated again during with the transition to modern socio-economic activities (reviewed by Albert et al. 2023). The modern Amazon basin is now home to about 35 million people, including about 400 indigenous and traditional communities, but also a large mestizo population concentrated in urban and rural áreas (see Nobre et al. 2021Nobre, C.; Encalada, A.; Anderson, E.; Roca Alcazar, F.H.; Bustamante, M.; Mena, C.; et al. (Ed.). 2021. Amazon Assessment Report 2021. United Nations Sustainable Development Solutions Network, New York . (https://www.theamazonwewant.org/spa_publication/amazon-assessment-report-2021/).
https://www.theamazonwewant.org/spa_publ... ). In the last 40 years, the Amazon has undergone unprecedented demographic and ecological transformations, in which the original indigenous populations suffered population crashes because of new diseases, displacement, and hostility (Walker et al. 2015Walker, R.S.; Sattenspiel, L.; Hill, K.R. 2015. Mortality from contact-related epidemics among indigenous populations in Greater Amazonia. Scientific Reports 5: 14032. doi: 10.1038/srep14032
https://doi.org/10.1038/srep14032... ; Cuvi et al. 2021Cuvi, N.; Guiteras Mombiola, A.; Lehm Ardaya, Z. 2021. Chapter 9: Peoples of the Amazon and European Colonization (16th-18th Centuries). In: Nobre, C.; Encalada, A.; Anderson, E.; Roca Alcazar, F.H.; Bustamante, M.; Mena, C.; et al. (Ed.). Amazon Assessment Report 2021. United Nations Sustainable Development Solutions Network, New York, USA (https://www.theamazonwewant.org/spa-reports/). doi: 10.55161/RPZI4818
https://www.theamazonwewant.org/spa-repo... ), and ecosystems have been degraded by industrial and agricultural activities (Albert et al. 2023). The magnitude of past and current human interlinks and impacts on Amazonian biodiversity was recently reviewed by the Science Panel for the Amazon (Nobre et al. 2021).

CONSERVATION OF ECOLOGICAL AND EVOLUTIONARY PROCESSES

One key goal of conservation biology is to provide effective principles and tools for preserving biodiversity (Soulé 1985Soulé, M.E. 1985. What is conservation biology? Bioscience 35: 727-734.), especially in complex and threatened ecosystems. Critical information for conservation planning in the Amazon is lacking in all major biodiversity dimensions, including taxonomic diversity, geographic distributions, species abundances, phylogenetic relationships, species traits, and species interactions.

The main threats to Amazonian diversity, just like its ecosystems and landscapes, are heterogeneously distributed (RAISG 2020RAISG. 2020. Amazonian Network of Georeferenced Socio-Environmental Information ( Amazonian Network of Georeferenced Socio-Environmental Information (https://www.amazoniasocioambiental.org/en/ ). Accessed on November 2021
https://www.amazoniasocioambiental.org/e... ; Figure 12). As such, a “one-plan-fits-all” strategy will not work in the region. Effective conservation strategies must consider the evolutionary and ecological processes that generate and maintain local species diversity in the many unique biological communities present in this large and ecologically relevant area. However, the legal structure for biodiversity conservation in the Amazon (and globally) is based primarily on individual species. Both governmental initiatives (e.g., US Endangered Species Act: https://www.fws.gov/media/endangered-species-act) and non-governmental initiatives (e.g., IUCN Red List: https://www.iucnredlist.org/) are organized around the ideas and actions of species conservation status and threat categories. In a similar manner, deforestation processes and impacts of infrastructure development, like roads, dams, and waterways, often ignore the compartmentalization of Amazonian diversity, and the unique characteristics of each region and habitat type (Da Silva et al. 2005Silva, J.M.C. Da.; Rylands, A.B.; Fonseca, G.A.B. Da. 2005. The fate of the Amazonian Areas of Endemism. Conservation Biology 19: 689-694.; Latrubesse et al. 2017Latrubesse, E.M.; Arima, E.Y.; Dunne, T.; Park, E.; Baker, V.R.; d’Horta, F.M.; et al. 2017. Damming the rivers of the Amazon basin. Nature 546: 363-369.).

While current initiatives focused on endangered species are crucial, it is important not to lose sight of the processes that keep these species alive and those that generate new diversity. For instance, when conservation priorities are viewed from an evolutionary standpoint, areas that hold the same number of species may not share the same conservation relevance. Instead, the preservation of areas holding distinct, unique, and/or higher amounts of evolutionary lineages should be given higher conservation priority (Forest et al. 2007Forest, F.; Grenyer, R.; Rouget, M.; Davies, T.J.; Cowling, R.M.; Faith, D.P.; et al. 2007. Preserving the evolutionary potential of floras in biodiversity hotspots. Nature 445: 757-760.; Castro et al. 2020Castro, R.B.; Pereira, J.L.G.; Albernaz, A.L.K.M.; Zanin, M. 2020. Connectivity, spatial structure and the identification of priority areas for conservation of Belém area of endemism, Amazon. Anais da Academia Brasileira de Ciencias 92: e20181357.; Jézéquel et al. 2020Jézéquel, C.; Tedesco, P.A.; Darwall, W.; Dias, M.S.; Frederico, R.G.; Hidalgo, M.; et al. 2020. Freshwater fish diversity hotspots for conservation priorities in the Amazon Basin. Conservation Biology 34: 956-965.; Figure 13). By prioritizing connected regions that host widely-divergent lineages, higher levels of phylogenetic uniqueness, and a broader spectrum of the genealogy of life (Meffe and Carroll 1994Meffe, G.K.; Carroll, C.R. 1994. Principles of Conservation Biology. Sinauer Associates, Massachusetts, 779p.), scientists can maximize future options, both for the continuing evolution of life on Earth and for the benefit of society (Forest et al. 2007). Maximum levels of global phylogenetic diversity lead to higher ecosystem services globally and higher plant services in general for humankind (Molina-Venegas et al. 2021Molina-Venegas, R.; Rodríguez, M.Á.; Pardo-de-Santayana, M.; Ronquillo, C.; Mabberley, D.J. 2021. Maximum levels of global phylogenetic diversity efficiently capture plant services for humankind. Nature Ecology and Evolution 5: 583-588.).

Conservation priorities based on a deep understanding of how biodiversity patterns have emerged allow us to preserve a potential for future evolution and adaptation (Erwin 1991Erwin, T.L. 1991. An Evolutionary Basis for Conservation Strategies. Science 253: 750-752.; Brooks et al. 1992Brooks, D.R.; Mayden, R.L.; McLennan, D.A. 1992. Phylogeny and biodiversity: Conserving our evolutionary legacy. Trends in Ecology and Evolution 7: 55-59.). By prioritizing lineages that are rapidly speciating and adapting we might, for instance, be able to preserve higher potential to resist future climatic and ecological change (Gavin et al. 2018). Likewise, by increasing evolutionary diversity, we are likely to increase trait diversity and provide increased resilience for Amazon rainforests (Sakschewski et al. 2016Sakschewski, B.; Bloh, W. Von; Boit, A.; Poorter, L.; Peña-Claros, M.; Heinke, J.; Joshi, J.; Thonicke, K. 2016. Resilience of Amazon forests emerges from plant trait diversity. Nature Climate Change 6: 1032-1036.).

Another way to incorporate evolutionary thinking into conservation is to focus on landscape attributes that generate unique variation or maintain connectivity among populations. Geographic barriers, for instance, restrict species ranges and lead to allopatric diversification (Figure 4). In the Amazon, rivers have imposed limits to the distribution of closely related species (Ribas et al. 2012Ribas, C.C.; Aleixo, A.; Nogueira, A.C.R.; Miyaki, C.Y.; Cracraft, J.2012. A palaeobiogeographic model for biotic diversification within Amazonia over the past three million years. Proceedings of the Royal Society Series B Biological Sciences 279: 681-689.). On the other hand, rivers may also be corridors of connectivity for species associated with floodplain habitats.

Free flowing rivers are hence fundamental not only for the species they support, but also for the evolutionary processes that they drive (Barbarossa et al. 2020Barbarossa, V.; Schmitt, R.J.; Huijbregts, M.A.; Zarfl, C.; King, H.; Schipper, A.M. 2020. Impacts of current and future large dams on the geographic range connectivity of freshwater fish worldwide. Proceedings of the National Academy of Sciences 117: 3648-3655.; Bem et al. 2021Bem, J. D.; Ribolli, J.; Röpke, C.; Winemiller, K. O.; Zaniboni-Filho, E. 2021. A cascade of dams affects fish spatial distributions and functional groups of local assemblages in a subtropical river. Neotropical Ichthyology, 19: e200133.; Vasconcelos et al. 2021Vasconcelos, L.P.; Alves, D.C.; da Câmara, L.F.; Hahn, L. 2021. Dams in the Amazon: The importance of maintaining free‐flowing tributaries for fish reproduction. Aquatic Conservation 31: 1106-1116.). Similarly, the conservation of regions of steep environmental gradients, which are expected to promote ecological speciation (Figure 4), is relevant from an evolutionary standpoint. In the Amazon, for instance, adjacent yet distinct soil types are intimately associated with plant specialization and differentiation (Fine et al. 2005Fine, P.A.; Daly, D.C.; Cameron, K.M. 2005. The contribution of edaphic heterogeneity to the evolution and diversity of burseracear trees in the western Amazon. Evolution 59: 1464-1478.; Tuomisto et al. 2014Tuomisto, H.; Zuquim, G.; Cárdenas, G. 2014. Species richness and diversity along edaphic and climatic gradients in Amazonia. Ecography 37: 1034-1046.). Promoting conservation of these gradients and diverse habitats associated with distinct soil types is therefore important in the short and long term.

The singular diversity of Amazonian organisms was generated over a period of millions of years and represents a large portion of Earth’s known and unknown diversity. Because the Amazon has been functioning as a primary source of biodiversity to all other Neotropical biomes (Antonelli et al. 2018Antonelli, A.; Zizka, A.; Carvalho, F.A.; Scharn, R.; Bacon, C.D.; Silvestro, D.; Condamine, F.L. 2018. Amazonia is the primary source of Neotropical biodiversity. Proceedings of the Natural Academy of Sciences 115: 6034-6039.), forest destruction and species loss in the Amazon (WWF 2016) likely has a direct impact on biodiversity and ecosystem function, threatening evolutionary processes governing the origin and maintenance of species diversity in all other South and Central American regions. A strong regional network of biological collections combined with long term monitoring of Amazonian populations, such as those conducted by the RAINFOR network (https://rainfor.org/en/), ForestGeo (https://forestgeo.si.edu/), LTER (https://lternet.edu/), and PPBio programs (PPBio 2005PPBio. 2005. Programa de Pesquisa em Biodiversidade. ( (https://ppbio.inpa.gov.br/en/home ). Accessed on November 2021.
https://ppbio.inpa.gov.br/en/home... ), are urgently needed to improve our understanding of Amazonian biodiversity, ecology, evolution, biogeography, and demography (Stouffer et al. 2021Stouffer, P.C.; Jirinec, V.; Rutt, C.L.; Bierregaard Jr, R.O.; Hernández-Palma, A.; Johnson, E.I.; Midway, S.R.; Powell, L.L.; Wolfe, J.D.; Lovejoy, T.E. 2021. Long‐term change in the avifauna of undisturbed Amazonian rainforest: ground‐foraging birds disappear and the baseline shifts. Ecology Letters 24: 186-195.).

Conservation efforts in the Amazon must take into account the unique ecological properties and evolutionary processes of its constituent biotas. Organismal habits and behaviors are one important example. The annual migrations of fishes (piracema), birds, and insects, as well as tree fruiting blooms, all constitute important biotic resources for human agroecosystems and other natural Amazonian ecosystems (Goulding et al. 2019Goulding, M.; Venticinque, E.; Ribeiro, M.L. de B.; Barthem, R.B.; Leite, R.G.; Forsberg, B.; et al. 2019. Ecosystem-based management of Amazon fisheries and wetlands. Fish and Fisheries 20: 138-158.). These behaviors are the basis for important ecological phenomena and annual life cycles, including mast flowering, phenological patterns, reproductive booms, and natural flood regimes (Alho 2020Alho, C. J. 2020. Hydropower dams and reservoirs and their impacts on Brazil’s biodiversity and natural habitats: a review. World Journal of Advanced Research and Reviews, 6: 205-215.; Cunha-Machado et al. 2021Cunha-Machado, A.S.; Farias, I.P.; Hrbek, T.; Escobar, M.D.; Alves-Gomes, J.A.; Formiga, K.M.; da Silva Batista, J. 2021. Genetic differentiation and gene flow of the Amazonian catfish Pseudoplatystoma punctifer across the Madeira River rapids prior to the construction of hydroelectric dams. Hydrobiologia, 849: 29-46.). Such phenomena need to be considered in regional planning and during rainforest conservation efforts. The establishment of river impoundments, for instance, interrupt natural flood regimes and disrupt migration corridors that are critical for the survival of Amazonian freshwater organisms (Winemiller et al. 2016Winemiller, K.O.; McIntyre, P.B.; Castello, L.; Fluet-Chouinard, E.; Giarrizzo, T.; Nam, S.; et al. 2016. Balancing hydropower and biodiversity in the Amazon, Congo, and Mekong. Science 351: 128-129.; Latrubesse et al. 2017Latrubesse, E.M.; Arima, E.Y.; Dunne, T.; Park, E.; Baker, V.R.; d’Horta, F.M.; et al. 2017. Damming the rivers of the Amazon basin. Nature 546: 363-369.; Barthem et al. 2017Barthem, R.B.; Goulding, M.; Leite, R.G.; Cañas, C.; Forsberg, B.; Venticinque, E.; et al. 2017. Goliath catfish spawning in the far western Amazon confirmed by the distribution of mature adults, drifting larvae and migrating juveniles. Scientific Reports 7: 1-13.; Albert et al. 2020Albert, J.S.; Destouni, G.; Duke-Sylvester, S.M.; Magurran, A.E.; Oberdorff, T.; Reis, R.E.; Winemiller, K.O.; Ripple, W.J. 2020b. Scientists’ warning to humanity on the freshwater biodiversity crisis. Ambio 50: 85-94.b).

CONCLUSIONS

Amazonian biodiversity is immense and vastly underestimated

Amazonian biodiversity is among the highest on Earth and constitutes the core of the Neotropical realm. The Amazon basin encompasses a vast range of life forms, genetic resources, and ecological functions, including hydrological cycles that impact climate at continental and global scales. This bewildering biodiversity arose from evolutionary diversification over highly heterogeneous landscapes and lengthy time periods in which rates of speciation exceeded those of extinction. A comprehensive understanding of Amazonian biodiversity is fundamental for data-driven conservation and management plans for these crucial ecosystems. Yet Amazonian biodiversity remains poorly known, due to high numbers of cryptic species, logistic difficulties of samplings, and insufficient human and infrastructure resources for assessments. Critical information is lacking in all major biodiversity dimensions: taxonomic diversity (Linnaean shortfall), biogeographic distributions (Wallacean shortfall), species abundances (Prestonian shortfall), phylogenetic diversity (Darwinian shortfall), species traits (Raunkiæran shortfall), and species interactions (Eltonian shortfall). Resolutions to all these information shortfalls will require increased investments in both governmental and non-governmental organizations, in particular in universities, research institutes, and natural history museums, within Amazonia and elsewhere, to leverage existing information and resources to fill existing gaps. Resources must also be invested in large-scale metagenomic screenings to quantify the known and document the as-yet unknown aspects of biodiversity, especially targeting poorly-studied but ecologically important life forms (e.g. bacteria, microorganisms, fungi, meiofauna) that drive ecosystem-level biochemical processes in Amazonian soils and waters.

Macroevolutionary history of Amazonian terrestrial and aquatic ecosystems

Tropical rainforests composed primarily of flowering plants originated on the supercontinent of Western Gondwana during the Early Cretaceous (ca. 145 - 100 Ma), and most modern tropical plant and animal groups diversified in the super-greenhouse world of the Late Cretaceous (ca. 100 - 66) and Early Paleogene (ca. 66 - 30 Ma). Two landmark events during this time were the final separation of South America from Africa (ca. 100 Ma) that isolated the biotas of these continental blocks, and the Chicxulub asteroid impact (ca. 66 Ma) that caused the End-Cretaceous global mass extinction, and which spurred rapid Early Paleogene (ca. 66-55 Ma) diversification of most modern terrestrial and aquatic taxa.

Global cooling starting in the Early Oligocene (ca. 30 Ma) resulted in extensive vegetational changes throughout South America, with tropical rainforests contracting to lower latitudes and grasslands expanding at temperate latitudes. These vegetation changes divided the formerly continuous moist Neotropical rainforest into disjunct Amazon and Atlantic rainforests. Climatic warming and tectonic processes during the Miocene (ca. 23 - 4.5 Ma) resulted in the formation of enormous mega-wetland systems in western Amazonia. Late Miocene (ca. 10 Ma) uplift of the northern Andes reorganized river drainage patterns across northern South America, driving the formation of the modern trans-continental Amazon river, as well as the courses of the modern Orinoco and Magdalena rivers, among many others.

Late Miocene to Pliocene (ca. 12-3.5 Ma) uplift of the Panama Isthmus allowed reciprocal dispersal between the biotas of North and South America, an event known as the Great American Biotic Interchange (GABI). The interchange was approximately symmetrical at first, with about equal numbers of taxa moving north and south, however the subsequent survival was highly asymmetrical, with mammals of North American origin surviving better than those from South America. Global climate oscillations during the Pleistocene (ca. 2.5 - 0.1), combined with human hunting, are associated with the extinctions of megafaunas worldwide. The extinction of large-bodied mammals in South American was more severe than elsewhere, where 83% of the megafauna (adult body weight > 44 kg) genera were lost.

Assembly of the megadiverse Amazonian biota

Amazonia’s outstanding biodiversity was assembled over a period of tens of millions of years, through a unique history of geological, climatic, and biological factors, all operating over partially-overlapping time scales. Geological and climatic factors operating over evolutionary time scales (thousands to millions of years) constrained the landscape and riverscape processes that generated heterogeneous soil and water chemistry profiles and other factors, which in turn affected the geographic, demographic, and genetic connections among populations. Through their controls on organismal dispersal, these abiotic factors strongly affected rates of adaptation, speciation and extinction. Lowland Amazonian landscapes and riverscapes are highly dynamic over time periods ranging from tens to hundreds of thousands of years, under the perennial influence of river capture over the broad low-relief topography, and of climate fluctuations over the course of the Plio-Pleistocene (ca. 5.3-0.01 Ma).

Biodiversity itself also contributes to elevated Amazonian species richness, through autocatalytic feedback mechanisms within hyperdiverse Amazonian ecosystems. Functionally and structurally diverse biotas provide more complex and multifarious environmental substrates that facilitate the evolution of physiological and behavioral specializations that may promote ecological coexistence and, in some cases, genetic isolation and speciation. Abiotic factors deriving directly from geographic space, climatic and elevation gradients, topographic relief, hydrology, and sediment and water chemistry, all serve to facilitate organismal diversification into major habitat types. Intertwined with these landscape processes are biotic processes that allow species to coexist within the same habitats and thereby lower their extinction risks. These ecological interactions include competition, predation, parasitism, mutualism, and cooperation, and the many ways in which organisms modify their environment. Such activities, known as niche construction, include the building of nests and burrows by animals, the formation of vegetation structure and shade by plants, and nutrient and energy cycling in soils and waterways by plants, fungi, and microbes. These biotic interactions lead to the evolution of new traits, increase the structural heterogeneity and functional dimensions of habitats, and enhance the genetic and phenotypic diversity of Amazonian ecosystems.

The human footprint on Amazonia

Human activities have greatly impacted Amazonian biodiversity for at least 20 Ka. The main effects by indigenous peoples were in plant domestication and agricultural practices that altered local vegetation structure and species abundance, and hunting practices that, combined with climatic changes, produced the extinction of pre-Pleistocene megafauna. Changes to the Amazonian ecosystems accelerated with Portuguese and Spanish colonization in the past 500 years, and accelerated again with the transition to modern socio-economic activities during the past 40 years. During this time, the Amazon has undergone profound demographic and ecological transformations, in which the original indigenous tribal populations suffered tremendous population crashes because of new diseases, displacement, and hostility. The modern Amazon basin is now home to about 35 million people, including about 400 indigenous and traditional communities, but also a large mestizo population concentrated in urban and rural areas. Rapid changes in land-use and other human activities (logging, mining, hunting, fishing, dams, roads) are profoundly affecting the species richness and evolutionary processes of the Amazon basin, by altering the distribution, abundance, connectivity, and ecology of species.

Conservation of ecological and evolutionary processes

The exceptional Amazonian biota accumulated over the course of millions of years by the action of numerous ecological and evolutionary processes that promoted ecological coexistence, facilitated both dispersal and genetic isolation, and ultimately resulted in a biota in which rates of speciation exceeded those of extinction. However, population sizes of many Amazonian species have been falling rapidly in recent years, due to human activities, imperilling many species and degrading the forest biome as a whole. The most effective conservation efforts prioritize regions characterized by: (1) high lineage and functional trait diversity (e.g., mature or “old growth” rainforests); (2) a high proportion of geographically restricted species (e.g. tepuí table-top mountains and other uplands areas of the Guiana and Brazilian Shields); (3) environmentally extreme habitats (e.g., white sand forests, acidic blackwater rivers) where species exhibit distinctive and specialized physiological and genetic traits; and (4), ongoing and rapid environmental change and lineage diversification (e.g. cloud forests of the Andean foothills, Páramos at higher elevations).

The most effective conservation strategies are both dynamic and pluralistic, balancing the irreplaceability, representativeness, and vulnerability of species and ecosystems (Jézéquel et al. 2020Jézéquel, C.; Tedesco, P.A.; Darwall, W.; Dias, M.S.; Frederico, R.G.; Hidalgo, M.; et al. 2020. Freshwater fish diversity hotspots for conservation priorities in the Amazon Basin. Conservation Biology 34: 956-965.). These strategies prioritize species with ecological and evolutionary resilience, with the goal to preserve lineages with a greater potential to resist and respond to ongoing and future climatic and ecological changes. Effective conservation planning seeks to maintain population connectivity, dispersal and gene flow, which facilitate ongoing evolutionary and ecological processes. Special attention and resources are required in areas of rapid economic and infrastructure development (e.g. road and dam construction), or where major anthropogenic habitat changes have fragmented natural populations via deforestation and defaunation for agriculture, hunting and mining.

ACKNOWLEDGMENTS

We thank the Science Panel for the Amazon (SPA) Technical Secretariat for envisioning and producing the in-depth scientific assessment of the state of the Amazon basin (www.theamazonwewant.org). We thank Dr. Hanna Tuomisto, Dr. José Maria Cardoso da Silva, and Dr. Orangel A. Aguilera S. for suggestions on an earlier version of this text. We extend our gratitude to Julia Arieira and Isabella Leite for their constant comments, assistance, and hard work during the preparation of the Science Panel for the Amazon report. We also thank comments and suggestions from other SPA members offered during brainstorming cross-fertilization sessions. We are grateful to all researchers who have undertaken extensive fieldwork in Amazonia to collect biotic and abiotic data, and the curators and collections managers at biological collections, who provide unique information that allow comparative studies across this vast region. We also thank MSc. Eduardo de Deus Schultz for assembling the first version of the map in Figure 10, and Dr. Alexandre Réjaud for providing the original files for preparing Figure 6. CCR would like to thank FAPEAM, FAPESP, CNPq, CAPES, NSF, USAID and the Biodiversa consortium for continuous support. JMG thanks COCIBA and USFQ for supporting his research (grants HUBI 17857, 5467, 16871, 17857) and to Daniela Franco-Mena for her help on the literature review. JSA acknowledges William Eschmeyer’s Catalog of Fishes for taxonomic data, and United States National Science Foundation awards 0614334, 0741450, and 1354511. JDC was supported by the Swiss Science Foundation Grants P400PB_186733 and P4P4PB_199187. LGL thanks CNPq for a Pq-1B grant (310871/2017-4), FAPESP for a Thematic Project (2018/23899-2), and a collaborative FAPESP/NSF/NASA grant on the “Assembly and evolution of the Amazionain biota and its environment” (2012/50260-6). CUU thanks the MBG for supporting her research. ACC acknowledges support by the National Science Foundation, FAPESP and NASA through awards DEB 1343578, DEB 1745562, and DBI 1926928.

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