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Flight over the Proto-Caribbean seaway: Phylogeny and macroevolution of Neotropical Anaeini leafwing butterflies

Toussaint, Emmanuel F.A., Dias, Fernando M.S., Mielke, Olaf H.H., Casagrande, Mirna M., Sañudo-Restrepo, Claudia P., Lam, Athena, Morinière, Jérôme, Balke, Michael, Vila, Roger
Molecular phylogenetics and evolution 2019 v.137 pp. 86-103
Eocene epoch, Malpighiales, Miocene epoch, Nymphalidae, biodiversity, biotic factors, butterflies, environmental factors, extinction, flight, geographical distribution, glaciation, host plants, lowlands, models, new combination, paraphyly, polyphyly, Amazonia, Andes region, Central America, South America
Our understanding of the origin and evolution of the astonishing Neotropical biodiversity remains somewhat limited. In particular, decoupling the respective impacts of biotic and abiotic factors on the macroevolution of clades is paramount to understand biodiversity assemblage in this region. We present the first comprehensive molecular phylogeny for the Neotropical Anaeini leafwing butterflies (Nymphalidae, Charaxinae) and, applying likelihood-based methods, we test the impact of major abiotic (Andean orogeny, Central American highland orogeny, Proto-Caribbean seaway closure, Quaternary glaciations) and biotic (host plant association) factors on their macroevolution. We infer a robust phylogenetic hypothesis for the tribe despite moderate support in some derived clades. Our phylogenetic inference recovers the genus Polygrapha Staudinger, [1887] as polyphyletic, rendering the genera FountaineaRydon, 1971 and Memphis Hübner, [1819] paraphyletic. Consequently, we transfer Polygrapha tyrianthina (Salvin & Godman, 1868) comb. nov. to Fountainea and Polygrapha xenocrates (Westwood, 1850) comb. nov. to Memphis. We infer an origin of the group in the late Eocene ca. 40 million years ago in Central American lowlands which at the time were separated from South America by the Proto-Caribbean seaway. The biogeographical history of the group is very dynamic, with several oversea colonization events from Central America into the Chocó and Andean regions during intense stages of Andean orogeny. These events coincide with the emergence of an archipelagic setting between Central America and northern South America in the mid-Miocene that likely facilitated dispersal across the now-vanished Proto-Caribbean seaway. The Amazonian region also played a central role in the diversification of the Anaeini, acting both as a museum and a cradle of diversity. We recover a diversification rate shift in the Miocene within the species-rich genus Memphis. State speciation and extinction models recover a significant relationship between this rate shift and host plant association, indicating a positive role on speciation rates of a switch between Malpighiales and new plant orders. We find less support for a role of abiotic factors including the progressive Andean orogeny, Proto-Caribbean seaway closure and Quaternary glaciations. Miocene host plant shifts possibly acted in concert with abiotic and/or biotic factors to shape the diversification of Anaeini butterflies.