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      Amazonia is the primary source of Neotropical biodiversity

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          Amazonia is not only the world’s most diverse rainforest but is also the region in tropical America that has contributed most to its total biodiversity. We show this by estimating and comparing the evolutionary history of a large number of animal and plant species. We find that there has been extensive interchange of evolutionary lineages among different regions and biomes, over the course of tens of millions of years. Amazonia stands out as the primary source of diversity, which can be mainly explained by the total amount of time Amazonian lineages have occupied the region. The exceedingly rich and heterogeneous diversity of the American tropics could only be achieved by high rates of dispersal events across the continent.

          Abstract

          The American tropics (the Neotropics) are the most species-rich realm on Earth, and for centuries, scientists have attempted to understand the origins and evolution of their biodiversity. It is now clear that different regions and taxonomic groups have responded differently to geological and climatic changes. However, we still lack a basic understanding of how Neotropical biodiversity was assembled over evolutionary timescales. Here we infer the timing and origin of the living biota in all major Neotropical regions by performing a cross-taxonomic biogeographic analysis based on 4,450 species from six major clades across the tree of life (angiosperms, birds, ferns, frogs, mammals, and squamates), and integrate >1.3 million species occurrences with large-scale phylogenies. We report an unprecedented level of biotic interchange among all Neotropical regions, totaling 4,525 dispersal events. About half of these events involved transitions between major environmental types, with a predominant directionality from forested to open biomes. For all taxonomic groups surveyed here, Amazonia is the primary source of Neotropical diversity, providing >2,800 lineages to other regions. Most of these dispersal events were to Mesoamerica (∼1,500 lineages), followed by dispersals into open regions of northern South America and the Cerrado and Chaco biomes. Biotic interchange has taken place for >60 million years and generally increased toward the present. The total amount of time lineages spend in a region appears to be the strongest predictor of migration events. These results demonstrate the complex origin of tropical ecosystems and the key role of biotic interchange for the assembly of regional biotas.

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          Recent assembly of the Cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire.

          The relative importance of local ecological and larger-scale historical processes in causing differences in species richness across the globe remains keenly debated. To gain insight into these questions, we investigated the assembly of plant diversity in the Cerrado in South America, the world's most species-rich tropical savanna. Time-calibrated phylogenies suggest that Cerrado lineages started to diversify less than 10 Mya, with most lineages diversifying at 4 Mya or less, coinciding with the rise to dominance of flammable C4 grasses and expansion of the savanna biome worldwide. These plant phylogenies show that Cerrado lineages are strongly associated with adaptations to fire and have sister groups in largely fire-free nearby wet forest, seasonally dry forest, subtropical grassland, or wetland vegetation. These findings imply that the Cerrado formed in situ via recent and frequent adaptive shifts to resist fire, rather than via dispersal of lineages already adapted to fire. The location of the Cerrado surrounded by a diverse array of species-rich biomes, and the apparently modest adaptive barrier posed by fire, are likely to have contributed to its striking species richness. These findings add to growing evidence that the origins and historical assembly of species-rich biomes have been idiosyncratic, driven in large part by unique features of regional- and continental-scale geohistory and that different historical processes can lead to similar levels of modern species richness.
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            A likelihood framework for inferring the evolution of geographic range on phylogenetic trees.

            At a time when historical biogeography appears to be again expanding its scope after a period of focusing primarily on discerning area relationships using cladograms, new inference methods are needed to bring more kinds of data to bear on questions about the geographic history of lineages. Here we describe a likelihood framework for inferring the evolution of geographic range on phylogenies that models lineage dispersal and local extinction in a set of discrete areas as stochastic events in continuous time. Unlike existing methods for estimating ancestral areas, such as dispersal-vicariance analysis, this approach incorporates information on the timing of both lineage divergences and the availability of connections between areas (dispersal routes). Monte Carlo methods are used to estimate branch-specific transition probabilities for geographic ranges, enabling the likelihood of the data (observed species distributions) to be evaluated for a given phylogeny and parameterized paleogeographic model. We demonstrate how the method can be used to address two biogeographic questions: What were the ancestral geographic ranges on a phylogenetic tree? How were those ancestral ranges affected by speciation and inherited by the daughter lineages at cladogenesis events? For illustration we use hypothetical examples and an analysis of a Northern Hemisphere plant clade (Cercis), comparing and contrasting inferences to those obtained from dispersal-vicariance analysis. Although the particular model we implement is somewhat simplistic, the framework itself is flexible and could readily be modified to incorporate additional sources of information and also be extended to address other aspects of historical biogeography.
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              Tracing the impact of the Andean uplift on Neotropical plant evolution.

              Recent phylogenetic studies have revealed the major role played by the uplift of the Andes in the extraordinary diversification of the Neotropical flora. These studies, however, have typically considered the Andean uplift as a single, time-limited event fostering the evolution of highland elements. This contrasts with geological reconstructions indicating that the uplift occurred in discrete periods from west to east and that it affected different regions at different times. We introduce an approach for integrating Andean tectonics with biogeographic reconstructions of Neotropical plants, using the coffee family (Rubiaceae) as a model group. The distribution of this family spans highland and montane habitats as well as tropical lowlands of Central and South America, thus offering a unique opportunity to study the influence of the Andean uplift on the entire Neotropical flora. Our results suggest that the Rubiaceae originated in the Paleotropics and used the boreotropical connection to reach South America. The biogeographic patterns found corroborate the existence of a long-lasting dispersal barrier between the Northern and Central Andes, the "Western Andean Portal." The uplift of the Eastern Cordillera ended this barrier, allowing dispersal of boreotropical lineages to the South, but gave rise to a huge wetland system ("Lake Pebas") in western Amazonia that prevented in situ speciation and floristic dispersal between the Andes and Amazonia for at least 6 million years. Here, we provide evidence of these events in plants.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                5 June 2018
                14 May 2018
                14 May 2018
                : 115
                : 23
                : 6034-6039
                Affiliations
                [1] aGothenburg Global Biodiversity Centre , SE-405 30 Gothenburg, Sweden;
                [2] bDepartment of Biological and Environmental Sciences, University of Gothenburg , SE-405 30 Gothenburg, Sweden;
                [3] cGothenburg Botanical Garden , SE-41319 Gothenburg, Sweden;
                [4] dDepartment of Organismic and Evolutionary Biology, Harvard University , Cambridge, MA 02138;
                [5] eDepartment of Botany and Zoology, Federal University of Rio Grande do Norte , Natal, RN 59078-970, Brazil;
                [6] fDepartment of Earth Sciences, University of Gothenburg , SE-405 30 Gothenburg, Sweden;
                [7] gDepartment of Computational Biology, University of Lausanne , 1015 Lausanne, Switzerland;
                [8] hCNRS, ISEM, University of Montpellier , 34095 Montpellier, France
                Author notes
                2To whom correspondence should be addressed. Email: alexandre.antonelli@ 123456bioenv.gu.se .

                Edited by Scott V. Edwards, Harvard University, Cambridge, MA, and approved April 13, 2018 (received for review August 4, 2017)

                Author contributions: A.A., A.Z., F.A.C., R.S., C.D.B., D.S., and F.L.C. designed research; 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 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.

                1A.A., A.Z., and F.A.C. contributed equally to this work.

                Author information
                http://orcid.org/0000-0003-1842-9297
                http://orcid.org/0000-0002-1680-9192
                http://orcid.org/0000-0002-3485-0797
                http://orcid.org/0000-0002-9305-2162
                http://orcid.org/0000-0003-2341-2705
                http://orcid.org/0000-0003-0100-0961
                http://orcid.org/0000-0003-1673-9910
                Article
                201713819
                10.1073/pnas.1713819115
                6003360
                29760058
                f4c55602-e656-4994-90a1-5e4c608ce662
                Copyright © 2018 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                Page count
                Pages: 6
                Funding
                Funded by: EC | FP7 | FP7 Ideas: European Research Council (FP7 Ideas) 100011199
                Award ID: 331024
                Categories
                Biological Sciences
                Evolution
                From the Cover

                biogeography,biome shift,evolution,neotropics,phylogenetics
                biogeography, biome shift, evolution, neotropics, phylogenetics

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