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Amazonia Is the Primary Source of Neotropical Biodiversity Amazonia is the primary source of Neotropical biodiversity The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citation Antonelli, Alexandre, Alexander Zizka, Fernanda Antunes Carvalho, Ruud Scharn, Christine D. Bacon, Daniele Silvestro, and Fabien L. Condamine. 2018. “Amazonia is the primary source of Neotropical biodiversity.” Proceedings of the National Academy of Sciences of the United States of America 115 (23): 6034-6039. doi:10.1073/ pnas.1713819115. http://dx.doi.org/10.1073/pnas.1713819115. Published Version doi:10.1073/pnas.1713819115 Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:37298561 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA Amazonia is the primary source of Neotropical biodiversity Alexandre Antonellia,b,c,d,1,2, Alexander Zizkaa,b,1, Fernanda Antunes Carvalhob,e,1, Ruud Scharna,b,f, Christine D. Bacona,b, Daniele Silvestroa,b,g, and Fabien L. Condamineb,h aGothenburg Global Biodiversity Centre, SE-405 30 Gothenburg, Sweden; bDepartment of Biological and Environmental Sciences, University of Gothenburg, SE-405 30 Gothenburg, Sweden; cGothenburg Botanical Garden, SE-41319 Gothenburg, Sweden; dDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138; eDepartment of Botany and Zoology, Federal University of Rio Grande do Norte, Natal, RN 59078-970, Brazil; fDepartment of Earth Sciences, University of Gothenburg, SE-405 30 Gothenburg, Sweden; gDepartment of Computational Biology, University of Lausanne, 1015 Lausanne, Switzerland; and hCNRS, ISEM, University of Montpellier, 34095 Montpellier, France Edited by Scott V. Edwards, Harvard University, Cambridge, MA, and approved April 13, 2018 (received for review August 4, 2017) The American tropics (the Neotropics) are the most species-rich realm but still remarkable, diversification history in the last few million on Earth, and for centuries, scientists have attempted to understand years (14, 15). the origins and evolution of their biodiversity. It is now clear that What remains less clear, however, is the role of biotic inter- different regions and taxonomic groups have responded differently change in the standing diversity of Neotropical regions. In addition to geological and climatic changes. However, we still lack a basic to differences in speciation and extinction rates, regional diversity understanding of how Neotropical biodiversity was assembled over is determined by the immigration of species from other regions evolutionary timescales. Here we infer the timing and origin of the over time. In some cases, immigrant lineages may constitute a living biota in all major Neotropical regions by performing a cross- substantial proportion of the local diversity, such as in Ecuadorian taxonomic biogeographic analysis based on 4,450 species from six Amazonia, where ca. 20% of all tree species arrived by dispersal major clades across the tree of life (angiosperms, birds, ferns, frogs, from other regions (16). Within the limits of a single region, dis- mammals, and squamates), and integrate >1.3 million species occur- persal events have been high in several plant genera (17, 18). In rences with large-scale phylogenies. We report an unprecedented contrast, dispersal events (including successful establishment) level of biotic interchange among all Neotropical regions, totaling across environmentally disparate regions are considered rare on a global scale (19). 4,525 dispersal events. About half of these events involved transi- Current evidence from the analysis of dated molecular phy- tions between major environmental types, with a predominant di- logenies has shown that some Neotropical regions might be more rectionality from forested to open biomes. For all taxonomic groups permeable than others. South American savannas, for instance, surveyed here, Amazonia is the primary source of Neotropical diver- have been colonized multiple times independently by ancestors sity, providing >2,800 lineages to other regions. Most of these dis- ∼ from other regions (20, 21). Alternatively, intrinsic differences persal events were to Mesoamerica ( 1,500 lineages), followed by among taxonomic groups (such as dispersal ability) may allow dispersals into open regions of northern South America and the some lineages, but not others, to colonize new regions. Although Cerrado and Chaco biomes. Biotic interchange has taken place some taxa tend to maintain their ecological requirements over for >60 million years and generally increased toward the present. time, staying in their region of origin or dispersing to distant regions The total amount of time lineages spend in a region appears to be with the same environmental conditions (i.e., niche conservatism, the strongest predictor of migration events. These results demon- strate the complex origin of tropical ecosystems and the key role of Significance biotic interchange for the assembly of regional biotas. Amazonia is not only the world’s most diverse rainforest but is biogeography | biome shift | evolution | Neotropics | phylogenetics also the region in tropical America that has contributed most to its total biodiversity. We show this by estimating and comparing he Neotropical realm, spanning from Mexico to southern the evolutionary history of a large number of animal and plant TSouth America and including the West Indies (1), is one of species. We find that there has been extensive interchange of the most species-rich regions on Earth (2, 3). This vast region evolutionary lineages among different regions and biomes, over comprises many different biomes and habitats such as seasonally thecourseoftensofmillionsofyears.Amazoniastandsoutas dry forests, arid zones, high-elevation grasslands, young and old the primary source of diversity, which can be mainly explained mountain systems, and extensive rainforests, such as the Atlantic by the total amount of time Amazonian lineages have occupied Forests and Amazonia (4). Because each region and biome the region. The exceedingly rich and heterogeneous diversity of possesses its own species diversity and communities, it is crucial theAmericantropicscouldonlybeachievedbyhighratesof to investigate the diversification history and biotic connections of dispersal events across the continent. each constituent region to understand how Neotropical bio- diversity was assembled (5, 6). Author contributions: A.A., A.Z., F.A.C., R.S., C.D.B., D.S., and F.L.C. designed research; Consensus is emerging that Neotropical diversification results A.A., A.Z., F.A.C., R.S., D.S., and F.L.C. performed research; A.Z., R.S., and D.S. contributed from a complex interaction of biotic and abiotic processes (2, 5), new reagents/analytic tools; A.A., A.Z., F.A.C., R.S., D.S., and F.L.C. analyzed data; and A.A., A.Z., and C.D.B. wrote the paper. which are now being teased apart by novel analytical approaches (7). Abiotic events of biological significance include the hydrologic The authors declare no conflict of interest. and topographic changes brought about by mountain uplift (4), This article is a PNAS Direct Submission. but also by several events of global and regional climatic changes This open access article is distributed under Creative Commons Attribution-NonCommercial- (8, 9). Biotic triggers of speciation include species interactions (10, NoDerivatives License 4.0 (CC BY-NC-ND). 11) and soil adaptations (12), as well as the evolution of other See Commentary on page 5829. organism-specific traits. Neotropical diversification has been ex- 1A.A., A.Z., and F.A.C. contributed equally to this work. tensive in some regions, such as Amazonia, where speciation in 2To whom correspondence should be addressed. Email: [email protected]. rainforest environments has taken place since at least the Paleocene This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. (∼58 Mya, Ma; ref. 13). Other environments, such as the high- 1073/pnas.1713819115/-/DCSupplemental. elevation grasslands in the northern Andes, have a more recent, Published online May 14, 2018. 6034–6039 | PNAS | June 5, 2018 | vol. 115 | no. 23 www.pnas.org/cgi/doi/10.1073/pnas.1713819115 refs.19and22),othersshowfrequent regional and ecological shifts (21, 23, 24). For the great majority of Neotropical regions and SEE COMMENTARY taxonomic groups, however, our knowledge of their biotic inter- changes and dispersal histories remains surprisingly poor, with few exceptions (e.g., refs. 25 and 26). In particular, we lack an un- WIN derstanding of which regions served as primary sources and sinks of biodiversity, defined here as providers and receivers of lineages, respectively, rather than implying habitat quality as in population MES biology (27). DNO Understanding the dynamics of biotic interchange is chal- lenging, as several abiotic and biotic factors are likely to be in- volved (28). Based on the Theory of Island Biogeography (29), there should be a positive relationship between the number AMA of dispersal events and the area of a region, and a negative re- DWE CAA lationship with geographic isolation. Similarly, the more shared perimeter (adjacency) two regions have, the more interchange Amazonia CEC should also be expected (28). However, many Neotropical re- Atlantic Forests AGL gions and
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