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      Biological evidence supports an early and complex emergence of the Isthmus of Panama

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          Significance

          The formation of the Isthmus of Panama, which linked North and South America, is key to understanding the biodiversity, oceanography, atmosphere, and climate in the region. Despite its importance across multiple disciplines, the timing of formation and emergence of the Isthmus and the biological patterns it created have been controversial. Here, we analyze molecular and fossil data, including terrestrial and marine organisms, to show that biotic migrations across the Isthmus of Panama began several million years earlier than commonly assumed. An earlier evolution of the Isthmus has broad implications for the mechanisms driving global climate (e.g., Pleistocene glaciations, thermohaline circulation) as well as the rich biodiversity of the Americas.

          Abstract

          The linking of North and South America by the Isthmus of Panama had major impacts on global climate, oceanic and atmospheric currents, and biodiversity, yet the timing of this critical event remains contentious. The Isthmus is traditionally understood to have fully closed by ca. 3.5 million years ago (Ma), and this date has been used as a benchmark for oceanographic, climatic, and evolutionary research, but recent evidence suggests a more complex geological formation. Here, we analyze both molecular and fossil data to evaluate the tempo of biotic exchange across the Americas in light of geological evidence. We demonstrate significant waves of dispersal of terrestrial organisms at approximately ca. 20 and 6 Ma and corresponding events separating marine organisms in the Atlantic and Pacific oceans at ca. 23 and 7 Ma. The direction of dispersal and their rates were symmetrical until the last ca. 6 Ma, when northern migration of South American lineages increased significantly. Variability among taxa in their timing of dispersal or vicariance across the Isthmus is not explained by the ecological factors tested in these analyses, including biome type, dispersal ability, and elevation preference. Migration was therefore not generally regulated by intrinsic traits but more likely reflects the presence of emergent terrain several millions of years earlier than commonly assumed. These results indicate that the dramatic biotic turnover associated with the Great American Biotic Interchange was a long and complex process that began as early as the Oligocene–Miocene transition.

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          Most cited references37

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          The Phanerozoic record of global sea-level change.

          K. Miller (2005)
          We review Phanerozoic sea-level changes [543 million years ago (Ma) to the present] on various time scales and present a new sea-level record for the past 100 million years (My). Long-term sea level peaked at 100 +/- 50 meters during the Cretaceous, implying that ocean-crust production rates were much lower than previously inferred. Sea level mirrors oxygen isotope variations, reflecting ice-volume change on the 10(4)- to 10(6)-year scale, but a link between oxygen isotope and sea level on the 10(7)-year scale must be due to temperature changes that we attribute to tectonically controlled carbon dioxide variations. Sea-level change has influenced phytoplankton evolution, ocean chemistry, and the loci of carbonate, organic carbon, and siliciclastic sediment burial. Over the past 100 My, sea-level changes reflect global climate evolution from a time of ephemeral Antarctic ice sheets (100 to 33 Ma), through a time of large ice sheets primarily in Antarctica (33 to 2.5 Ma), to a world with large Antarctic and large, variable Northern Hemisphere ice sheets (2.5 Ma to the present).
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            A New Look at the Statistical Model Identification

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              Southern hemisphere biogeography inferred by event-based models: plant versus animal patterns.

              The Southern Hemisphere has traditionally been considered as having a fundamentally vicariant history. The common trans-Pacific disjunctions are usually explained by the sequential breakup of the supercontinent Gondwana during the last 165 million years, causing successive division of an ancestral biota. However, recent biogeographic studies, based on molecular estimates and more accurate paleogeographic reconstructions, indicate that dispersal may have been more important than traditionally assumed. We examined the relative roles played by vicariance and dispersal in shaping Southern Hemisphere biotas by analyzing a large data set of 54 animal and 19 plant phylogenies, including marsupials, ratites, and southern beeches (1,393 terminals). Parsimony-based tree fitting in conjunction with permutation tests was used to examine to what extent Southern Hemisphere biogeographic patterns fit the breakup sequence of Gondwana and to identify concordant dispersal patterns. Consistent with other studies, the animal data are congruent with the geological sequence of Gondwana breakup: (Africa(New Zealand(southern South America, Australia))). Trans-Antarctic dispersal (Australia southern South America) is also significantly more frequent than any other dispersal event in animals, which may be explained by the long period of geological contact between Australia and South America via Antarctica. In contrast, the dominant pattern in plants, (southern South America(Australia, New Zealand)), is better explained by dispersal, particularly the prevalence of trans-Tasman dispersal between New Zealand and Australia. Our results also confirm the hybrid origin of the South American biota: there has been surprisingly little biotic exchange between the northern tropical and the southern temperate regions of South America, especially for animals.
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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
                12 May 2015
                27 April 2015
                27 April 2015
                : 112
                : 19
                : 6110-6115
                Affiliations
                [1] aSmithsonian Tropical Research Institute , 0843-03092 Balboa, Panamá;
                [2] bDepartment of Biological and Environmental Sciences, University of Gothenburg , SE-413 19 Gothenburg, Sweden;
                [3] cDepartment of Ecology and Evolution, University of Lausanne and Swiss Institute of Bioinformatics , CH-1015 Lausanne, Switzerland;
                [4] dDepartment of Ornithology, American Museum of Natural History , New York, NY 10024;
                [5] eDepartment of Biological Sciences, Louisiana State University , Baton Rouge, LA 70803; and
                [6] fGothenburg Botanical Garden , SE-413 19 Gothenburg, Sweden
                Author notes
                1To whom correspondence should be addressed. Email: christinedbacon@ 123456gmail.com .

                Edited by Richard H. Ree, Field Museum of Natural History, Chicago, IL, and accepted by the Editorial Board April 2, 2015 (received for review December 19, 2014)

                Author contributions: C.D.B., C.J., and A.A. designed research; C.D.B., D.S., B.T.S., and P.C. analyzed data; and C.D.B. and A.A. wrote the paper.

                Author information
                http://orcid.org/0000-0003-0100-0961
                Article
                201423853
                10.1073/pnas.1423853112
                4434730
                25918375
                e908d0a7-face-41ea-b3ee-f0d1934208cc

                Freely available online through the PNAS open access option.

                History
                Page count
                Pages: 6
                Funding
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: EAR 0824299; OISE/EAR/DRL 0966884
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: DEB 0916695
                Funded by: Swedish Research Council Formas (Svenska Forskningsrådet Formas) 501100001862
                Award ID: B0569601
                Funded by: EC | European Research Council (ERC) 501100000781
                Award ID: 331024
                Categories
                Biological Sciences
                Evolution

                biogeography,evolution,neotropics,fossil,migration
                biogeography, evolution, neotropics, fossil, migration

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