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The trans-riverine genetic structure of 28 Amazonian frog species is dependent on life history

Published online by Cambridge University Press:  08 June 2015

Antoine Fouquet*
Affiliation:
CNRS Guyane USR3456, Immeuble Le Relais, 2 Avenue Gustave Charlery, 97300, Cayenne, French Guiana
Elodie A. Courtois
Affiliation:
CNRS Guyane USR3456, Immeuble Le Relais, 2 Avenue Gustave Charlery, 97300, Cayenne, French Guiana
Daniel Baudain
Affiliation:
25 lot. Emilio Pascal, 97313, St Georges de l'Oyapock
Jucivaldo Dias Lima
Affiliation:
Centro de Pesquisas Zoobotânicas e Geologicas (CPZG), Divisão de Zoologia, Macapá, AP, Brazil
Sergio Marques Souza
Affiliation:
Universidade de São Paulo, Instituto de Biociências, Departamento de Zoologia, Caixa Postal 11.461, CEP 05508-090, São Paulo, SP, Brazil
Brice P. Noonan
Affiliation:
University of Mississippi, Biology, Box 1848, University, MS 38677, USA
Miguel T. Rodrigues
Affiliation:
Universidade de São Paulo, Instituto de Biociências, Departamento de Zoologia, Caixa Postal 11.461, CEP 05508-090, São Paulo, SP, Brazil
*
1Corresponding author. Email: fouquet.antoine@gmail.com

Abstract:

Among the hypotheses formulated to explain the origin of Amazonian biodiversity, two (the riverine-barrier and the river-refuge hypotheses) focus on the role that rivers play as biotic barriers promoting speciation. However, empirical results have both supported and refuted these hypotheses. This is likely due, at least in part, to river-specific hydrologic characteristics and the biology of the focal species. The rivers of the Guiana Shield represent a model system because they have had more stable courses over time than those of the western Amazon Basin, where most tests of riverine barrier effects have taken place. We tested whether life-history traits (body size, habitat and larval development), expected to be important in determining dispersal ability, of 28 frog species are associated with genetic structure and genetic distances of individuals sampled from both banks of the Oyapock River. Thirteen of these species displayed genetic structure consistent with the river acting as a barrier to dispersal. Surprisingly, body size was not correlated with trans-riverine population structure. However, leaf-litter dwellers and species lacking free-living tadpoles were found to exhibit higher river-associated structure than open habitat/arboreal species and those with exotrophic tadpoles. These results demonstrate that rivers play an important role in structuring the genetic diversity of many frog species though the permeability of such riverine barriers is highly dependent on species-specific traits.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

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References

LITERATURE CITED

AVILA-PIRES, T. C. 1995. Lizards of Brazilian Amazonia (Reptilia: Squamata). Zoologische Verhandelingen 299:1706.Google Scholar
AYRES, J. & CLUTTON-BROCK, T. 1992. River boundaries and species range size in Amazonian primates. American Naturalist 140:531537.CrossRefGoogle ScholarPubMed
BATES, H. 1874. The naturalist on the River Amazon. John Murray, London. 506 pp.Google Scholar
BATES, J. M., HAFFER, J. & GRISMER, E. 2004. Avian mitochondrial DNA sequence divergence across a headwater stream of the Rio Tapajós, a major Amazonian river. Journal of Ornithology 145:199205.CrossRefGoogle Scholar
BLOMBERG, S. P., GARLAND, T. & IVES, A. R. 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717745.Google ScholarPubMed
BURNEY, C. W. & BRUMFIELD, R. T. 2009. Ecology predicts levels of genetic differentiation in Neotropical birds. American Naturalist 174:358368.CrossRefGoogle ScholarPubMed
CAPPARELLA, A. 1988. Genetic variation in Neotropical birds: implications for the speciation process. Acta Congressus Internationalis Ornithologici 19:16581673.Google Scholar
DARRIBA, D., TABOADA, G. L., DOALLO, R. & POSADA, D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9:772.CrossRefGoogle ScholarPubMed
DE CASTELNAU, F. 1851. Expédition dans les parties centrales de l'Amérique du sud, de Rio de Janeiro à Lima, et de Lima au Para, 1843-47, exécutée par ordre du gouvernement français pendant les années 1843 à 1847. P. Bertrand, Paris. 480 pp.CrossRefGoogle Scholar
FOUQUET, A. 2008. Diversity and phylogeography of Eastern Guiana shield frogs. PhD Dissertation, University of Canterbury, New Zealand.Google Scholar
FOUQUET, A., GILLES, A., VENCES, M., MARTY, C., BLANC, M. & GEMMELL, N. J. 2007. Underestimation of species richness in Neotropical frogs revealed by mtDNA analyses. PLoS ONE 2:e1109.CrossRefGoogle ScholarPubMed
FOUQUET, A., NOONAN, B., BLANC, M. & ORRICO, V. G. D. 2011. Phylogenetic position of Dendropsophus gaucheri (Lescure and Marty 2000) highlights the need for an in-depth investigation of the phylogenetic relationships of Dendropsophus (Anura: Hylidae). Zootaxa 3035:5967.CrossRefGoogle Scholar
FOUQUET, A., LEDOUX, J., DUBUT, V., NOONAN, B. P. & SCOTTI, I. 2012a. The interplay of dispersal limitation, rivers, and historical events shapes the genetic structure of an Amazonian frog. Biological Journal of the Linnean Society 106:356373.CrossRefGoogle Scholar
FOUQUET, A., NOONAN, B. P., RODRIGUES, M. T., PECH, N., GILLES, A. & GEMMELL, N. J. 2012b. Multiple quaternary refugia in the Eastern Guiana Shield revealed by comparative phylogeography of 12 frog species. Systematic Biology 61:461489.CrossRefGoogle ScholarPubMed
FOUQUET, A., BLOTTO, B. L., MARONNA, M. M., VERDADE, V. K., JUNCA, F. A., DE SA, R. & RODRIGUES, M. T. 2013. Unexpected phylogenetic positions of the genera Rupirana and Crossodactylodes reveal insights into the biogeography and reproductive evolution of leptodactylid frogs. Molecular Phylogenetics and Evolution 67:445457.CrossRefGoogle ScholarPubMed
FUNK, W. C., CALDWELL, J. P., PEDEN, C. E., PADIAL, J. M., DE LA RIVA, I. & CANNATELLA, D. C. 2007. Tests of biogeographic hypotheses for diversification in the Amazonian forest frog, Physalaemus petersi. Molecular Phylogenetics and Evolution 44:825837.CrossRefGoogle ScholarPubMed
FUNK, W. C., CAMINER, M. & RON, S. R. 2012. High levels of cryptic species diversity uncovered in Amazonian frogs. Proceedings of the Royal Society B: Biological Sciences 279:18061814.CrossRefGoogle ScholarPubMed
GASCON, C., LOUGHEED, S. C. & BOGART, J. P. 1998. Patterns of genetic population differentiation in four species of Amazonian frogs: a test of the Riverine Barrier Hypothesis. Biotropica 30:104119.CrossRefGoogle Scholar
GEHARA, M., CRAWFORD, A. J., ORRICO, V. G. D., RODRIGUEZ, A., LÖTTERS, S., FOUQUET, A., BALDO, D., BARRIENTOS, L. S., BRUSQUETTI, F., CASTROVIEJO-FISHER, S., DE LA RIVA, I., ERNST, R., FAIVOVICH, J., GAGLIARDI URRUTIA, G., GLAW, F., GUAYASAMIN, J., HÖLTING, M., JANSEN, M., KOK, P. J. R., KWET, A., LINGNAU, R., LYRA, M., MORAVEC, J., PADIAL, J. M., POMBAL, J., ROJAS-RUNJAIC, F. J. M., SCHULZE, A., SEÑARIS, J. C., SOLÉ, M., RODRIGUEZ, M. T., TWOMEY, E., HADDAD, C. F. B., VENCES, M. & KÖHLER, J. 2014. High levels of diversity uncovered in a widespread nominal taxon: continental phylogeography of the neotropical tree frog Dendropsophus minutus. PLoS ONE 9:e103958.CrossRefGoogle Scholar
GOND, V., FREYCON, V., MOLINO, J.-F., BRUNAUX, O., INGRASSIA, F., JOUBERT, P., PEKEL, J.-F., PRÉVOST, M.-F., THIERRON, V. & TROMBE, P.-J. 2011. Broad-scale spatial pattern of forest landscape types in the Guiana Shield. International Journal of Applied Earth Observation and Geoinformation 13:357367.CrossRefGoogle Scholar
GUINDON, S. & GASCUEL, O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52:696704.CrossRefGoogle ScholarPubMed
HAFFER, J. 1997. Alternative models of vertebrate speciation in Amazonia: an overview. Biodiversity and Conservation 6:451476.CrossRefGoogle Scholar
HAYES, F. E. & SEWLAL, J. N. 2004. The Amazon River as a dispersal barrier to passerine birds: effects of river width, habitat and taxonomy. Journal of Biogeography 31:18091818.CrossRefGoogle Scholar
HILLIS, D. M., MORITZ, C., MABLE, B. K. & OLMSTEAD, R. G. 1996. Molecular systematics. Sinauer Associates, Sunderland. 655 pp.Google Scholar
HOORN, C., WESSELINGH, F., TER STEEGE, H., BERMUDEZ, M., MORA, A., SEVINK, J., SANMARTÍN, I., SANCHEZ-MESEGUER, A., ANDERSON, C. & FIGUEIREDO, J. 2010. Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330:927931.CrossRefGoogle ScholarPubMed
JACKSON, N. D. & AUSTIN, C. C. 2013. Testing the role of meander cutoff in promoting gene flow across a riverine barrier in ground skinks (Scincella lateralis). PloS ONE 8:e62812.CrossRefGoogle ScholarPubMed
JUNGFER, K.-H., FAIVOVICH, J., PADIAL, J. M., CASTROVIEJO-FISHER, S., LYRA, M. L., BERNECK, B. V. M., IGLESIAS, P. P., KOK, P. J. R., MACCULLOCH, R. D., RODRIGUES, M. T., VERDADE, V. K., TORRES GASTELLO, C. P., CHAPARRO, J. C., VALDUJO, P. H., REICHLE, S., MORAVEC, J., GVOŽDÍK, V., GAGLIARDI-URRUTIA, G., ERNST, R., DE LA RIVA, I., MEANS, D. B., LIMA, A. P., SEÑARIS, J. C., WHEELER, W. C. & HADDAD, C. F. B. 2013. Systematics of spiny-backed treefrogs (Hylidae: Osteocephalus): an Amazonian puzzle. Zoologica Scripta 42:351380.CrossRefGoogle Scholar
KAEFER, I. L., TSUJI-NISHIKIDO, B. M., MOTA, E. P., FARIAS, I. P. & LIMA, A. P. 2013. The early stages of speciation in Amazonian forest frogs: phenotypic conservatism despite strong genetic structure. Evolutionary Biology 40:228245.CrossRefGoogle Scholar
KATOH, K. & STANDLEY, D. M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30:772780.CrossRefGoogle ScholarPubMed
KEMBEL, S. W., COWAN, P. D., HELMUS, M. R., CORNWELL, W. K., MORLON, H., ACKERLY, D. D., BLOMBERG, S. P. & WEBB, C. O. 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:14631464.CrossRefGoogle ScholarPubMed
LAMPERT, K. P., RAND, A. S., MUELLER, U. G. & RYAN, M. J. 2003. Fine-scale genetic pattern and evidence for sex-biased dispersal in the túngara frog, Physalaemus pustulosus. Molecular Ecology 12:33253334.CrossRefGoogle ScholarPubMed
LEITE, R. N. & ROGERS, D. S. 2013. Revisiting Amazonian phylogeography: insights into diversification hypotheses and novel perspectives. Organisms Diversity and Evolution 13:639664.CrossRefGoogle Scholar
LESCURE, J. & MARTY, C. 2001. Atlas des amphibiens de Guyane. Museum d'Histoire Naturelle, Paris. 388 pp.Google Scholar
LOUGHEED, S., GASCON, C., JONES, D., BOGART, J. & BOAG, P. 1999. Ridges and rivers: a test of competing hypotheses of Amazonian diversification using a dart-poison frog (Epipedobates femoralis). Proceedings of the Royal Society of London. Series B: Biological Sciences 266:18291835.CrossRefGoogle Scholar
LUNDBERG, J. G., MARSHALL, L. G., GUERRERO, J., HORTON, B., MALABARBA, M. C. S. L. & WESSELINGH, F. 1998. The stage for Neotropical fish diversification: a history of tropical South American rivers. Pp. 1348 in Malabarba, L. R., Reis, R. E., Vari, R. P., Lucena, L. S. & Lucena, C. A. S. (eds.). Phylogeny and classification of Neotropical fishes. Edipucrs, Porto Alegre.Google Scholar
MAYR, E. 1942. Systematics and the origin of species, from the viewpoint of a zoologist. Columbia University Press, New York. 334 pp.Google Scholar
NAKA, L. N., BECHTOLDT, C. L., HENRIQUES, L. M. P. & BRUMFIELD, R. T. 2012. The role of physical barriers in the location of avian suture zones in the Guiana Shield, northern Amazonia. American Naturalist 179:E115–E132.CrossRefGoogle ScholarPubMed
NEWMAN, R. A. & SQUIRE, T. 2001. Microsatellite variation and fine-scale population structure in the wood frog (Rana sylvatica). Molecular Ecology 10:10871100.CrossRefGoogle ScholarPubMed
NOONAN, B. P. & WRAY, K. P. 2006. Neotropical diversification: the effects of a complex history on diversity within the poison frog genus Dendrobates. Journal of Biogeography 33:10071020.CrossRefGoogle Scholar
PATTON, J. L., DA SILVA, M. N. F. & MALCOLM, J. R. 1994. Gene genealogy and differentiation among arboreal spiny rats (Rodentia: Echimyidae) of the Amazon Basin: a test of the riverine barrier hypothesis. Evolution 48:13141323.CrossRefGoogle Scholar
PELOSO, P. L. V., STURARO, M. J., FORLANI, M. C., MOTTA, A. P. & WHEELER, W. C. 2014. Phylogeny, taxonomic revision, and character evolution of the genera Chiasmocleis and Syncope (Anura, Microhylidae) in Amazonia, with descriptions of three new species. Bulletin of the American Museum of Natural History 386:1112.CrossRefGoogle Scholar
PERES, C., PATTON, J. & DA SILVA, N. F. 1996. Riverine barriers and gene flow in Amazonian saddle-back tamarins. Folia Primatologica 67:113124.CrossRefGoogle ScholarPubMed
PYRON, A. R. & WIENS, J. J. 2011. A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution 61:543583.CrossRefGoogle Scholar
RIBAS, C. C., ALEIXO, A., NOGUEIRA, A. C. R., MIYAKI, C. Y. & CRACRAFT, J. 2011. A palaeobiogeographic model for biotic diversification within Amazonia over the past three million years. Proceedings of the Royal Society of London. Series B: Biological Sciences 279:681689.Google ScholarPubMed
RICHARDSON, J. L. 2012. Divergent landscape effects on population connectivity in two co-occurring amphibian species. Molecular Ecology 21:44374451.CrossRefGoogle ScholarPubMed
RONQUIST, F. & HUELSENBECK, J. P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:15721574.CrossRefGoogle ScholarPubMed
RULL, V. 2011. Neotropical biodiversity: timing and potential drivers. Trends in Ecology and Evolution 26:508513.CrossRefGoogle ScholarPubMed
SALDUCCI, M.-D., MARTY, C., FOUQUET, A. & GILLES, A. 2005. Phylogenetic relationships and biodiversity in hylids (Anura: Hylidae) from French Guiana. Comptes Rendus Biologies 328:10091024.CrossRefGoogle ScholarPubMed
SLATKIN, M. 1987. Gene flow and the geographic structure of natural populations. Science 236:787792.CrossRefGoogle ScholarPubMed
SOUZA, S. M., RODRIGUES, M. T. & COHN-HAFT, M. 2013. Are Amazonia rivers biogeographic barriers for lizards? A study on the geographic variation of the spectacled lizard Leposoma osvaldoi Avila-Pires (Squamata, Gymnophthalmidae). Journal of Herpetology 47:511519.CrossRefGoogle Scholar
TAMURA, K., PETERSON, D., PETERSON, N., STECHER, G., NEI, M. & KUMAR, S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28:27312739.CrossRefGoogle ScholarPubMed
VAN BOCXLAER, I., LOADER, S. P., ROELANTS, K., BIJU, S., MENEGON, M. & BOSSUYT, F. 2010. Gradual adaptation toward a range-expansion phenotype initiated the global radiation of toads. Science 327:679682.CrossRefGoogle Scholar
WALLACE, A. R. 1854. On the monkeys of the Amazon. Journal of Natural History 14:451454.CrossRefGoogle Scholar
WOLLENBERG, K. C., VIEITES, D. R., GLAW, F. & VENCES, M. 2011. Speciation in little: the role of range and body size in the diversification of Malagasy mantellid frogs. BMC Evolutionary Biology 11:217.CrossRefGoogle ScholarPubMed
ZEISSET, I. & BEEBEE, T. 2008. Amphibian phylogeography: a model for understanding historical aspects of species distributions. Heredity 101:109119.CrossRefGoogle Scholar