Diversification of Rhacophorid Frogs Provides Evidence for Accelerated

Diversification of Rhacophorid Frogs Provides Evidence for Accelerated

Corrections APPLIED BIOLOGICAL SCIENCES IMMUNOLOGY Correction for “An algorithm-based topographical biomaterials Correction for “Alternative end-joining catalyzes robust IgH library to instruct cell fate,” by Hemant V. Unadkat, Marc locus deletions and translocations in the combined absence of Hulsman, Kamiel Cornelissen, Bernke J. Papenburg, Roman K. ligase 4 and Ku70,” by Cristian Boboila, Mila Jankovic, Catherine Truckenmüller, Anne E. Carpenter, Matthias Wessling, Gerhard T. Yan, Jing H. Wang, Duane R. Wesemann, Tingting Zhang, Alex F. Post, Marc Uetz, Marcel J. T. Reinders, Dimitrios Stamatialis, Fazeli, Lauren Feldman, Andre Nussenzweig, Michel Nussenzweig, Clemens A. van Blitterswijk, and Jan de Boer, which appeared and Frederick W. Alt, which appeared in issue 7, February 16, 2010, in issue 40, October 4, 2011, of Proc Natl Acad Sci USA (108: of Proc Natl Acad Sci USA (107:3034–3039; first published January 16565–16570; first published September 26, 2011; 10.1073/pnas. 25, 2010; 10.1073/pnas.0915067107). 1109861108). The authors note that the National Institutes of Health Grant The authors note that the following statement should be added AI031541 should instead appear as AI077595. to the Acknowledgments: “This work was supported in part by NIH Grant R01 GM089652 (A.E.C.).” www.pnas.org/cgi/doi/10.1073/pnas.1303073110 www.pnas.org/cgi/doi/10.1073/pnas.1302919110 IMMUNOLOGY Correction for “Downstream class switching leads to IgE anti- EVOLUTION body production by B lymphocytes lacking IgM switch regions,” Correction for “Diversification of rhacophorid frogs provides by Tingting Zhang, Andrew Franklin, Cristian Boboila, Amy evidence for accelerated faunal exchange between India McQuay, Michael P. Gallagher, John P. Manis, Ahmed Amine and Eurasia during the Oligocene,” by Jia-Tang Li, Yang Li, Khamlichi, and Frederick W. Alt, which appeared in issue 7, Sebastian Klaus, Ding-Qi Rao, David M. Hillis, and Ya-Ping February 16, 2010, of Proc Natl Acad Sci USA (107:3040–3045; Zhang, which appeared in issue 9, February 26, 2013, of Proc first published February 1, 2010; 10.1073/pnas.0915072107). Natl Acad Sci USA (110:3441–3446; first published February The authors note that the National Institutes of Health Grant 11, 2013; 10.1073/pnas.1300881110). AI031541 should instead appear as AI077595. The authors note that, within the author line, “Yang Lia,c” should instead appear as “Yang Lib,c”. The corrected author line www.pnas.org/cgi/doi/10.1073/pnas.1303075110 appears below. The online version has been corrected. Jia-Tang Lia,b, Yang Lib,c, Sebastian Klausd, Ding-Qi Raoa, David M. Hillise, and Ya-Ping Zhanga,f IMMUNOLOGY www.pnas.org/cgi/doi/10.1073/pnas.1304031110 Correction for “Robust chromosomal DNA repair via alternative end-joining in the absence of X-ray repair cross-complementing protein 1 (XRCC1),” by Cristian Boboila, Valentyn Oksenych, Monica Gostissa, Jing H. Wang, Shan Zha, Yu Zhang, Hua Chai, Cheng-Sheng Lee, Mila Jankovic, Liz-Marie Albertorio Saez, IMMUNOLOGY Michel C. Nussenzweig, Peter J. McKinnon, Frederick W. Alt, and Correction for “Integrity of the AID serine-38 phosphorylation Bjoern Schwer, which appeared in issue 7, February 14, 2012, of site is critical for class switch recombination and somatic hy- Proc Natl Acad Sci USA (109:2473–2478; first published January permutation in mice,” by Hwei-Ling Cheng, Bao Q. Vuong, 30, 2012; 10.1073/pnas.1121470109). Uttiya Basu, Andrew Franklin, Bjoern Schwer, Jillian Astarita, The authors note that the National Institutes of Health Grant Ryan T. Phan, Abhishek Datta, John Manis, Frederick W. Alt, AI031541 should instead appear as AI077595. and Jayanta Chaudhuri, which appeared in issue 8, February 24, www.pnas.org/cgi/doi/10.1073/pnas.1303078110 2009, of Proc Natl Acad Sci USA (106:2717–2722; first published February 5, 2009; 10.1073/pnas.0812304106). The authors note that the National Institutes of Health Grant AI31541 should instead appear as AI077595. www.pnas.org/cgi/doi/10.1073/pnas.1303069110 CORRECTIONS www.pnas.org PNAS | April 2, 2013 | vol. 110 | no. 14 | 5731 Downloaded by guest on September 27, 2021 Diversification of rhacophorid frogs provides evidence for accelerated faunal exchange between India and Eurasia during the Oligocene Jia-Tang Lia,b,1, Yang Lib,c, Sebastian Klausd, Ding-Qi Raoa, David M. Hillise,1, and Ya-Ping Zhanga,f,1 aState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China; bChengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China; dDepartment of Ecology and Evolution, Goethe University, 60438 Frankfurt am Main, Germany; eSection of Integrative Biology and Center for Computational Biology and Bioinformatics, University of Texas at Austin, Austin, TX 78712; fLaboratory for Conservation and Utilization of Bioresources, Yunnan University, Kunming 650091, China; and cCollege of Life Sciences, Sichuan University, Chengdu 610064, China Contributed by David M. Hillis, January 15, 2013 (sent for review November 19, 2012) The accretion of the Indian subcontinent to Eurasia triggered a data for a group of amphibians that occurs throughout this area massive faunal and floral exchange, with Gondwanan taxa entering and is restricted by the marine environment. into Asia and vice versa. The traditional view on the Indian–Asian Tectonic collisions do not necessarily produce terrestrial con- collision assumes contact of the continental plates during the Early nections. Thus, biogeographic research is needed to understand Eocene. Many biogeographic studies rely on this assumption. How- the biological implications of plate movements and collisions (19). ever, the exact mode and timing of this geological event is still un- In the case of northward drifting India, this applies especially for der debate. Here we address, based on an extensive phylogenetic potential connections between India and Southeast Asia, as re- analysis of rhacophorid tree frogs, if there was already a Paleogene cently suggested, based on freshwater crab biogeography (19). biogeographic link between Southeast Asia and India; in which di- Amphibians are ideal organisms to infer geological and environ- rection faunal exchange occurred between India and Eurasia within mental history due to their poor marine dispersal capabilities (3, the Rhacophoridae; and if the timing of the faunal exchange corre- 20–24). Frogs of the family Rhacophoridae (Old World tree frogs lates with one of the recently suggested geological models. Rhaco- or shrub frogs) are a particularly appropriate animal group to test phorid tree frogs showed an early dispersal from India to Asia the timing of the Indian–Asian collision as their range comprises between 46 and 57 Ma, as reconstructed from the fossil record. both India and East/Southeast Asia (21, 25) (Fig. S1 and Table During the Middle Eocene, however, faunal exchange ceased, fol- S1). Previous studies identified the Madagascan Mantellidae as lowed by increase of rhacophorid dispersal events between Asia the sister group of the Rhacophoridae and concluded that the and the Indian subcontinent during the Oligocene that continued latter reached Eurasia via the northward drifting Indian sub- until the Middle Miocene. This corroborates recent geological mod- continent (3, 21, 26, 27), whereas three rhacophorid species that els that argue for a much later final collision between the continen- currently inhabit tropical Africa were shown to be the result of EVOLUTION tal plates. We predict that the Oligocene faunal exchange between more recent dispersal from Asia (28, 29). the Indian subcontinent and Asia, as shown here for rhacophorid Here, we integrate phylogenetic, biogeographic, and molecu- – frogs, also applies for other nonvolant organisms with an Indian lar dating methods to reconstruct the comprehensive molecular Asian distribution, and suggest that previous studies that deal with phylogeny of rhacophorid frogs. In this time-calibrated phylo- this faunal interchange should be carefully reinvestigated. genetic framework, we reconstruct ancestral geographical areas to test (i) if there was already a Paleogene biogeographic link phylogeography | molecular dating | tectonics between Southeast Asia and India; (ii) in which direction faunal exchange occurred between India and Eurasia within the Rha- he tectonic collision between India and Asia induced a major cophoridae; and (iii) if the timing of the faunal exchange cor- Tbiotic exchange from the former Gondwana continent to relates with one of the recently suggested geological hypotheses tropical Asia during the Early Cenozoic (1). Recent molecular (Table 1), thus providing evidence for the paleoposition of the studies have confirmed that Late Cretaceous faunal and floral Indian subcontinent as it moved northward. elements entered Asia from Africa and Madagascar via the Results northward drifting Indian subcontinent (2–8). Thus, this tectonic event can be considered a major driver of biotic diversification, Sequence Characteristics. The aligned mtDNA gene fragments con- comparable to the “Great American Interchange” between North sisted of 2,041 sites (excluding positions of unstable alignment). The mitochondrial data correspond to sites 726–2,666 of the Polypedates and South America after the closure of the Isthmus of Panama megacephalus (9). However, the timing of the Indian–Asian collision and, of mitochondrial genome (AY458598). Transitions and transversions within the five nDNA partitions accumulated in a equal importance,

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