Abstract
Although rivers are known to promote diversification and shape phylogeographic patterns, they can also be permeable and facilitate the dispersal of species. Using multiple molecular methodological approaches, we conducted a phylogeographic investigation of two semiaquatic snake species with continental distributions across South America, testing how environmental and historical factors (e.g., potential allopatric divergence across rivers) have affected their evolutionary history. Our results show that Hydrodynastes gigas and H. bicinctus have a recent divergence time (~1.5 mya) and that both species have low genetic diversity with no geographic structure. Population genetic divergence in H. gigas is explained by geographic distance (isolation-by-distance), climate (isolation-by-environment), and hydrographic basin. Paleo-niche models suggest that historically stable regions of habitat suitability for both taxa are largely restricted to the La Plata basin. We suggest that life history traits of these species, for example high dispersal capabilities and generalist ecologies, have allowed for their extensive geographic distributions and population connectivity resulting in no geographic structure and low genetic variation.
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Data availability
The datasets analysed during the current study are referenced in the text and publicly available.
References
Aiello-Lammens, M. E., Boria, R. A., Radosavljevic, A., Vilela, B., & Anderson, R. P. (2015). spThin: An R package for spatial thinning of species occurrence records for use in ecological niche models. Ecography, 38(5), 541–545. https://doi.org/10.1111/ecog.01132
Aleixo, A. (2004). Historical diversification of a terra-firme forest bird superspecies: A phylogeographic perspective on the role of different hypotheses of Amazonian diversification. Evolution, 58(6), 1303–1317. https://doi.org/10.1111/j.0014-3820.2004.tb01709.x
Anderson, C. D., Epperson, B. K., Fortin, M. J., Holderegger, R., James, P. M., Rosenberg, M. S., Scribner, K. T., & Spear, S. (2010). Considering spatial and temporal scale in landscape-genetic studies of gene flow. Molecular Ecology, 19(17), 3565–3575. https://doi.org/10.1111/j.1365-294X.2010.04757.x
Arzamendia, V., & Giraudo, A. (2009). Influence of great South American rivers of the Plata basin on distributional patterns of tropical snakes: A panbiogeographic analysis. Journal of Biogeography, 36(9), 1739–1749. https://doi.org/10.1111/j.1365-2699.2009.02116.x
Beheregaray, L. B. (2008). Twenty years of phylogeography: the state of the field and the challenges for the Southern Hemisphere. Molecular Ecology, 17(17), 3754–3774. https://doi.org/10.1111/j.1365-294X.2008.03857.x
Bell, R. C., Parra, J. L., Badjedjea, G., Barej, M. F., Blackburn, D. C., Burger, M., Channing, A., Dehling, J. M., Greenbaum, E., Gvoždík, V., Kielgast, J., Kusamba, C., Lötters, S., McLaughlin, P. J., Nagy, Z. T., Rödel, M. O., Portik, D. M., Stuart, B. L., VanDerWal, J., … Zamudio, K. R. (2017). Idiosyncratic responses to climate-driven forest fragmentation and marine incursions in reed frogs from Central Africa and the Gulf of Guinea Islands. Molecular Ecology, 26(19), 5223–5244. https://doi.org/10.1111/mec.14260
Bielejec, F., Rambaut, A., Suchard, M. A., & Lemey, P. (2011). SPREAD: Spatial phylogenetic reconstruction of evolutionary dynamics. Bioinformatics, 27(20), 2910–2912. https://doi.org/10.1093/bioinformatics/btr481
Bittencourt, P. S., Campos, Z., de Lima Muniz, F., Marioni, B., Souza, B. C., Da Silveira, R., Thoisy, B., Hrbek, T., & Farias, I. P. (2019). Evidence of cryptic lineages within a small South American crocodilian: The Schneider’s dwarf caiman Paleosuchus trigonatus (Alligatoridae: Caimaninae). PeerJ, 7, e6580. https://doi.org/10.7717/peerj.6580
Bivand, R., Keitt, T., & Rowlingson, B. (2021). rgdal: Bindings for the ‘Geospatial’ data abstraction library. R package version 1.5–23. https://CRAN.R-project.org/package=rgdal
Bouckaert, R., Vaughan, T. G., Barido-Sottani, J., Duchêne, S., Fourment, M., Gavryushkina, A., Heled, J., Jones, G., Kühnert, D., Maio, N., Matschiner, M., Mendes, F. K., Müller, N. F., Ogilvie, H. A., Plessis, L., Popinga, A., Rambaut, A., Rasmussen, D., Siveroni, I., … Drummond, A. J. (2019). BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology, 15(4), e1006650. https://doi.org/10.1371/journal.pcbi.1006650
Brandley, M. C., Guiher, T. J., Pyron, R. A., Winne, C. T., & Burbrink, F. T. (2010). Does dispersal across an aquatic geographic barrier obscure phylogeographic structure in the diamond-backed watersnake (Nerodia rhombifer)? Molecular Phylogenetics and Evolution, 57(2), 552–560. https://doi.org/10.1016/j.ympev.2010.07.015
Brown, J. L., Hill, D. J., Dolan, A. M., Carnaval, A. C., & Haywood, A. M. (2018). PaleoClim, high spatial resolution paleoclimate surfaces for global land areas. Scientific Data, 5(1), 1–9. https://doi.org/10.1038/sdata.2018.254
Brüniche-Olsen, A., Bickham, J. W., Godard-Codding, C. A., Brykov, V. A., Kellner, K. F., Urban, J., & DeWoody, J. A. (2021). Influence of Holocene habitat availability on Pacific gray whale (Eschrichtius robustus) population dynamics as inferred from whole mitochondrial genome sequences and environmental niche modeling. Journal of Mammalogy, 102(4), 986–999. https://doi.org/10.1093/jmammal/gyab032
Burbrink, F. T., Fontanella, F., Pyron, R. A., Guiher, T. J., & Jimenez, C. (2008). Phylogeography across a continent: The evolutionary and demographic history of the North American racer (Serpentes: Colubridae: Coluber constrictor). Molecular Phylogenetics and Evolution, 47(1), 274–288. https://doi.org/10.1016/j.ympev.2007.10.020
Camurugi, F., Gehara, M., Fonseca, E. M., Zamudio, K. R., Haddad, C. F., Colli, G. R., Thomé, M. T. C., Prado, C. P. A., Napoli, M. F., & Garda, A. A. (2021). Isolation by environment and recurrent gene flow shaped the evolutionary history of a continentally distributed Neotropical treefrog. Journal of Biogeography, 48(4), 760–772. https://doi.org/10.1111/jbi.14035
Carvalho, P. S., Zaher, H., da Silva Jr, N. J., & Santana, D. J. (2020). A morphological and molecular study of Hydrodynastes gigas (Serpentes, Dipsadidae), a widespread species from South America. PeerJ, 8, e10073. https://doi.org/10.7717/peerj.10073
Colston, T. J., Grazziotin, F. G., Shepard, D. B., Vitt, L. J., Colli, G. R., Henderson, R. W., Hedges, S. B., Bonatto, S., Zaher, H., Noonan, B. P., & Burbrink, F. T. (2013). Molecular systematics and historical biogeography of tree boas (Corallus spp.). Molecular Phylogenetics and Evolution, 66(3), 953–959. https://doi.org/10.1016/j.ympev.2012.11.027
Cooke, G. M., Landguth, E. L., & Beheregaray, L. B. (2014). Riverscape genetics identifies replicated ecological divergence across an Amazonian ecotone. Evolution, 68(7), 1947–1960. https://doi.org/10.1111/evo.12410
Costa, G. C., Nogueira, C., Machado, R. B., & Colli, G. R. (2010). Sampling bias and the use of ecological niche modeling in conservation planning: A field evaluation in a biodiversity hotspot. Biodiversity and Conservation, 19(3), 883–899. https://doi.org/10.1007/s10531-009-9746-8
Cullingham, C. I., Miller, J. M., Peery, R. M., Dupuis, J. R., Malenfant, R. M., Gorrell, J. C., & Janes, J. K. (2020). Confidently identifying the correct K value using the ΔK method: When does K= 2? Molecular Ecology, 29(5), 862–869. https://doi.org/10.1111/mec.15374
Dal Vechio, F., Prates, I., Grazziotin, F. G., Zaher, H., Graboski, R., & Rodrigues, M. T. (2019). Rain forest shifts through time and riverine barriers shaped the diversification of South American terrestrial pit vipers (Bothrops jararacussu species group). Journal of Biogeography, 47(2), 516–526. https://doi.org/10.1111/jbi.13736
Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: More models, new heuristics and parallel computing. Nature Methods, 9(8), 772–772. https://doi.org/10.1038/nmeth.2109
Daza, J. M., Smith, E. N., Páez, V. P., & Parkinson, C. L. (2009). Complex evolution in the Neotropics: The origin and diversification of the widespread genus Leptodeira (Serpentes: Colubridae). Molecular Phylogenetics and Evolution, 53(3), 653–667. https://doi.org/10.1016/j.ympev.2009.07.022
Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29(8), 1969–1973. https://doi.org/10.1093/molbev/mss075
Earl, D. A., & vonHoldt, B. M. (2012). STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4(2), 359–361. https://doi.org/10.1007/s12686-011-9548-7
Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), 1792–1797. https://doi.org/10.1093/nar/gkh340
Edler, D., Klein, J., Antonelli, A., & Silvestro, D. (2021). raxmlGUI 2.0: A graphical interface and toolkit for phylogenetic analyses using RAxML. Methods in Ecology and Evolution, 12(2), 373–377. https://doi.org/10.1111/2041-210X.13512
Elith, J., Phillips, S. J., Hastie, T., Dudík, M., Chee, Y. E., & Yates, C. J. (2011). A statistical explanation of MaxEnt for ecologists. Diversity and Distributions, 17(1), 43–57. https://doi.org/10.1111/j.1472-4642.2010.00725.x
Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology, 14(8), 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Excoffier, L., & Lischer, H. E. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10(3), 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Fonseca, E. M., Garda, A. A., Oliveira, E. F., Camurugi, F., Magalhães, F. D. M., Lanna, F. M., Zurano, J. P., Marques, R., Vences, M., & Gehara, M. (2021). The riverine thruway hypothesis: Rivers as a key mediator of gene flow for the aquatic paradoxical frog Pseudis tocantins (Anura, Hylidae). Landscape Ecology, 36(10), 3049–3060. https://doi.org/10.1007/s10980-021-01257-z
Fordham, D. A., Saltré, F., Haythorne, S., Wigley, T. M., Otto-Bliesner, B. L., Chan, K. C., & Brook, B. W. (2017). PaleoView: A tool for generating continuous climate projections spanning the last 21 000 years at regional and global scales. Ecography, 40(11), 1348–1358. https://doi.org/10.1111/ecog.03031
Fouquet, A., Courtois, E. A., Baudain, D., Lima, J. D., Souza, S. M., Noonan, B. P., & Rodrigues, M. T. (2015). The trans-riverine genetic structure of 28 Amazonian frog species is dependent on life history. Journal of Tropical Ecology, 31(4), 361–373. https://doi.org/10.1017/S0266467415000206
Garda, A. A., & Cannatella, D. C. (2007). Phylogeny and biogeography of paradoxical frogs (Anura, Hylidae, Pseudae) inferred from 12S and 16S mitochondrial DNA. Molecular Phylogenetics and Evolution, 44(1), 104–114. https://doi.org/10.1016/j.ympev.2006.11.028
Gehara, M., Crawford, A. J., Orrico, V. G. D., Rodríguez, A., Lötters, S., Fouquet, A., Baldo, D., Barrientos, L. S., Brusquetti, F., De La Riva, I., Ernst, R., Faivovich, J., Urrutia, G. G., Glaw, F., Guayasamin, J. M., Hölting, M., Jansen, M., Kok, P. J. R., Kwet, A., … 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(9), e103958. https://doi.org/10.1371/journal.pone.0103958
Gehara, M., Garda, A. A., Werneck, F. P., Oliveira, E. F., da Fonseca, E. M., Camurugi, F., Magalhães, F. M., Lanna, F. M., Sites, J. W., Marques, R., Silveira-Filho, R., São Pedro, V. A., Colli, G. R., Costa, G. C., & Burbrink, F. T. (2017). Estimating synchronous demographic changes across populations using hABC and its application for a herpetological community from northeastern Brazil. Molecular Ecology, 26(18), 4756–4771. https://doi.org/10.1111/mec.14239
Giraudo, A. R., Arzamendia, V., Bellini, G. P., Bessa, C. A., & Costanzo, M. B. (2014). Ecología de una gran serpiente sudamericana, Hydrodynastes gigas (Serpentes: Dipsadidae). Revista Mexicana De Biodiversidad, 85(4), 1206–1216. https://doi.org/10.7550/rmb.43765
Gottscho, A. D., Marks, S. B., & Jennings, W. B. (2014). Speciation, population structure, and demographic history of the Mojave Fringe-toed Lizard (Uma scoparia), a species of conservation concern. Ecology and Evolution, 4(12), 2546–2562. https://doi.org/10.1002/ece3.1111
Grazziotin, F. G., Monzel, M., Echeverrigaray, S., & Bonatto, S. L. (2006). Phylogeography of the Bothrops jararaca complex (Serpentes: Viperidae): Past fragmentation and island colonization in the Brazilian Atlantic Forest. Molecular Ecology, 15(13), 3969–3982. https://doi.org/10.1111/j.1365-294X.2006.03057.x
Guiher, T. J., & Burbrink, F. T. (2008). Demographic and phylogeographic histories of two venomous North American snakes of the genus Agkistrodon. Molecular Phylogenetics and Evolution, 48(2), 543–553. https://doi.org/10.1016/j.ympev.2008.04.008
Henderson, R. W., Pauers, M. J., & Colston, T. J. (2013). On the congruence of morphology, trophic ecology, and phylogeny in Neotropical treeboas (Squamata: Boidae: Corallus). Biological Journal of the Linnean Society, 109(2), 466–475. https://doi.org/10.1111/bij.12052
Hewitt, G. M. (2004). Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 359(1442), 183–195. https://doi.org/10.1098/rstb.2003.1388
Hijmans, R. J. (2020). raster: Geographic data analysis and modeling. R package version 3.4-5. https://CRAN.R-project.org/package=raster.
Hoorn, C., Boschman, L. M., Kukla, T., Sciumbata, M., & Val, P. (2022). The Miocene wetland of western Amazonia and its role in Neotropical biogeography. Botanical Journal of the Linnean Society, 199(1), 25–35. https://doi.org/10.1093/botlinnean/boab098
Hoorn, C., Wesselingh, F. P., ter Steege, H., Bermudez, M. A., Mora, A., Sevink, J., Sanmartín, I., Sanchez-Meseguer, A., Anderson, C. L., Figueiredo, J. P., Jaramillo, C., Riff, D., Negri, F. R., Hooghiemstra, H., Lundberg, J., Stadler, T., Särkinen, T., & Antonelli, A. (2010). Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science, 330(6006), 927–931.
Jaynes, K. E., Myers, E. A., Gvoždík, V., Blackburn, D. C., Portik, D. M., Greenbaum, E., Jongsma, G. F., Rödel, M. O., Badjedjea, G., Bamba-Kaya, A., & Baptista, N. L. (2021). Giant Tree Frog diversification in West and Central Africa: Isolation by physical barriers, climate, and reproductive traits. Molecular Ecology. https://doi.org/10.1111/mec.16169
Kapli, P., Lutteropp, S., Zhang, J., Kobert, K., Pavlidis, P., Stamatakis, A., & Flouri, T. (2017). Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics, 33(11), 1630–1638. https://doi.org/10.1093/bioinformatics/btx025
Karger, D. N., Conrad, O., Böhner, J., Kawohl, T., Kreft, H., Soria-Auza, R. W., Zimmermann, K. N., Linder, H. P., & Kessler, M. (2017). Climatologies at high resolution for the earth’s land surface areas. Scientific Data, 4(1), 1–20. https://doi.org/10.1038/sdata.2017.122
Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T., & Calcott, B. (2017). PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34(3), 772–773. https://doi.org/10.1093/molbev/msw260
Lawson, R., Slowinski, J. B., Crother, B. I., & Burbrink, F. T. (2005). Phylogeny of the Colubroidea (Serpentes): New evidence from mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution, 37(2), 581–601. https://doi.org/10.1016/j.ympev.2005.07.016
Leigh, J. W., & Bryant, D. (2015). POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6(9), 1110–1116. https://doi.org/10.1111/2041-210X.12410
Librado, P., & Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25(11), 1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Lukoschek, V., Osterhage, J. L., Karns, D. R., Murphy, J. C., & Voris, H. K. (2011). Phylogeography of the Mekong mud snake (Enhydris subtaeniata): The biogeographic importance of dynamic river drainages and fluctuating sea levels for semiaquatic taxa in Indochina. Ecology and Evolution, 1(3), 330–342. https://doi.org/10.1002/ece3.29
Maciel, N. M., Collevatti, R. G., Colli, G. R., & Schwartz, E. F. (2010). Late Miocene diversification and phylogenetic relationships of the huge toads in the Rhinella marina (Linnaeus, 1758) species group (Anura: Bufonidae). Molecular Phylogenetics and Evolution, 57(2), 787–797. https://doi.org/10.1016/j.ympev.2010.08.025
Magalhães, F. D. M., Lyra, M. L., De Carvalho, T. R., Baldo, D., Brusquetti, F., Burella, P., Colli, G. R., Gehara, M. C., Giaretta, A. A., Haddad, C. F. B., Langone, J. A., López, J. A., Napoli, M. F., Santana, D. J., Sá, F. O., & Garda, A. A. (2020). Taxonomic review of South American Butter Frogs: Phylogeny, geographic patterns, and species delimitation in the Leptodactylus latrans species group (Anura: Leptodactylidae). Herpetological Monographs, 34(1), 131–177. https://doi.org/10.1655/HERPMONOGRAPHS-D-19-00012
Makowsky, R., Marshall, J. C., Jr., McVay, J., Chippindale, P. T., & Rissler, L. J. (2010). Phylogeographic analysis and environmental niche modeling of the plain-bellied watersnake (Nerodia erythrogaster) reveals low levels of genetic and ecological differentiation. Molecular Phylogenetics and Evolution, 55(3), 985–995. https://doi.org/10.1016/j.ympev.2010.03.012
Mângia, S., Oliveira, E. F., Santana, D. J., Koroiva, R., Paiva, F., & Garda, A. A. (2020). Revising the taxonomy of Proceratophrys Miranda-Ribeiro, 1920 (Anura: Odontophrynidae) from the Brazilian semiarid Caatinga: Morphology, calls and molecules support a single widespread species. Journal of Zoological Systematics and Evolutionary Research, 58(4), 1151–1172. https://doi.org/10.1111/jzs.12365
McCartney-Melstad, E., Waller, T., Micucci, P. A., Barros, M., Draque, J., Amato, G., & Mendez, M. (2012). Population structure and gene flow of the yellow anaconda (Eunectes notaeus) in northern Argentina. PLoS ONE. https://doi.org/10.1371/annotation/06482a0a-b49c-4feb-9aa8-d3c8f72e90fb
Morales, N. S., Fernández, I. C., & Baca-González, V. (2017). MaxEnt’s parameter configuration and small samples: Are we paying attention to recommendations? A Systematic Review. PeerJ, 5, e3093. https://doi.org/10.7717/peerj.3093
Moura, A. E., Janse, C., van Rensburg, M., Pilot, A. T., Best, P. B., Thornton, M., Stephanie Plön, P. J., de Bruyn, N., Worley, K. C., Gibbs, R. A., Dahlheim, M. E., & Hoelzel, A. R. (2014). Killer whale nuclear genome and mtDNA reveal widespread population bottleneck during the last glacial maximum. Molecular Biology and Evolution, 31(5), 1121–1131. https://doi.org/10.1093/molbev/msu058
Murta-Fonseca, R. A., Franco, F. L., & Fernandes, D. S. (2015). Taxonomic status and morphological variation of Hydrodynastes bicinctus (Hermann, 1804) (Serpentes: Dipsadidae). Zootaxa, 4007(1), 63–81. https://doi.org/10.11646/zootaxa.4007.1.4
Muscarella, R., Galante, P. J., Soley-Guardia, M., Boria, R. A., Kass, J. M., Uriarte, M., & Anderson, R. P. (2014). ENM eval: An R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models. Methods in Ecology and Evolution, 5(11), 1198–1205. https://doi.org/10.1111/2041-210X.12261
Myers, E. A., Hickerson, M. J., & Burbrink, F. T. (2017). Asynchronous diversification of snakes in the North American warm deserts. Journal of Biogeography, 44(2), 461–474. https://doi.org/10.1111/jbi.12873
Myers, E. A., Weaver, R. E., & Alamillo, H. (2013). Population stability of the northern desert nightsnake (Hypsiglena chlorophaea deserticola) during the Pleistocene. Journal of Herpetology, 47(3), 432–439. https://doi.org/10.1670/12-104
Naka, L. N., & Brumfield, R. T. (2018). The dual role of Amazonian rivers in the generation and maintenance of avian diversity. Science Advances, 4(8), eaar8575. https://doi.org/10.1126/sciadv.aar8575
Nogueira, C. C., Argôlo, A. J. S., Arzamendia, V., Azevedo, J. A., Barbo, F. E., Bérnils, R. S., Bolochio, B. E., Borges-Martins, M., Brasil-Godinho, M., Braz, H., Buononato, M. A., Cisneros-Heredia, D. F., Colli, G. R., Costa, H. C., Franco, F. L., Giraudo, A., Gonzalez, R. C., Guedes, T., Hoogmoed, M. S., … Martins, M. (2019). Atlas of Brazilian snakes: verified point-locality maps to mitigate the Wallacean shortfall in a megadiverse snake fauna. South American Journal of Herpetology, 14(SI 1), 1–274. https://doi.org/10.2994/SAJH-D-19-00120.1
Noonan, B. P., & Chippindale, P. T. (2006). Dispersal and vicariance: The complex evolutionary history of boid snakes. Molecular Phylogenetics and Evolution, 40(2), 347–358. https://doi.org/10.1016/j.ympev.2006.03.010
O’Connell, K. A., & Smith, E. N. (2018). The effect of missing data on coalescent species delimitation and a taxonomic revision of whipsnakes (Colubridae: Masticophis). Molecular Phylogenetics and Evolution, 127, 356–366. https://doi.org/10.1016/j.ympev.2018.03.018
O’Connell, K. A., Streicher, J. W., Smith, E. N., & Fujita, M. K. (2017). Geographical features are the predominant driver of molecular diversification in widely distributed North American whipsnakes. Molecular Ecology, 26(20), 5729–5751. https://doi.org/10.1111/mec.14295
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R., O'Hara, R. B., Simpson, Gavin L., Solymos, P., Stevens, M. H. H., Szoecs, E., & Wagner, H. (2020). Vegan: Community Ecology Package. R package version 2.5-7. https://CRAN.R-project.org/package=vegan
Oliveira, E. F., Martinez, P. A., São-Pedro, V. A., Gehara, M., Burbrink, F. T., Mesquita, D. O., Garda, A. A., Colli, G. R., & Costa, G. C. (2018). Climatic suitability, isolation by distance and river resistance explain genetic variation in a Brazilian whiptail lizard. Heredity, 120(3), 251–265. https://doi.org/10.1038/s41437-017-0017-2
Ony, M., Klingeman, W. E., Zobel, J., Trigiano, R. N., Ginzel, M., Nowicki, M., Boggess, S. L., Everhart, S., & Hadziabdic, D. (2021). Genetic diversity in North American Cercis Canadensis reveals an ancient population bottleneck that originated after the last glacial maximum. Scientific Reports, 11(1), 1–16. https://doi.org/10.1038/s41598-021-01020-z
Otto-Bliesner, B. L., Marshall, S. J., Overpeck, J. T., Miller, G. H., & Aixue, Hu. (2006). Simulating Arctic climate warmth and icefield retreat in the last interglaciation. Science, 311(5768), 1751–1753. https://doi.org/10.1126/science.1120808
Palumbi, S., Martin, A., Romano, S., McMillan, W.O., Stice, L., & Grabowski, G. (2002). The simple fool’s guide to PCR, version 2.0. Honolulu, EUA
Papadopoulou, A., & Knowles, L. L. (2016). Toward a paradigm shift in comparative phylogeography driven by trait-based hypotheses. Proceedings of the National Academy of Sciences, 113(29), 8018–8024. https://doi.org/10.1073/pnas.1601069113
Paradis, E., & Schliep, K. (2019). ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics, 35(3), 526–528. https://doi.org/10.1093/bioinformatics/bty633
Paz, A., Ibáñez, R., Lips, K. R., & Crawford, A. J. (2015). Testing the role of ecology and life history in structuring genetic variation across a landscape: A trait-based phylogeographic approach. Molecular Ecology, 24(14), 3723–3737. https://doi.org/10.1111/mec.13275
Phillips, S. J., Anderson, R. P., & Schapire, R. E. (2006). Maximum entropy modeling of species geographic distributions. Ecological Modelling, 190(3–4), 231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026
Pinto, B. J., Colli, G. R., Higham, T. E., Russell, A. P., Scantlebury, D. P., Vitt, L. J., & Gamble, T. (2019). Population genetic structure and species delimitation of a widespread, Neotropical dwarf gecko. Molecular Phylogenetics and Evolution, 133, 54–66. https://doi.org/10.1016/j.ympev.2012.11.027
Pirani, R. M., Werneck, F. P., Thomaz, A. T., Kenney, M. L., Sturaro, M. J., Ávila-Pires, T. C., Peloso, P. L. V., Rodrigues, M. T., & Knowles, L. L. (2019). Testing main Amazonian rivers as barriers across time and space within widespread taxa. Journal of Biogeography, 46(11), 2444–2456. https://doi.org/10.1111/jbi.13676
Pook, C. E., Wüster, W., & Thorpe, R. S. (2000). Historical biogeography of the western rattlesnake (Serpentes: Viperidae: Crotalus viridis), inferred from mitochondrial DNA sequence information. Molecular Phylogenetics and Evolution, 15(2), 269–282. https://doi.org/10.1006/mpev.1999.0756
Prado, C. P., Haddad, C. F., & Zamudio, K. R. (2012). Cryptic lineages and Pleistocene population expansion in a Brazilian Cerrado frog. Molecular Ecology, 21(4), 921–941. https://doi.org/10.1111/j.1365-294X.2011.05409.x
Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155(2), 945–959. https://doi.org/10.1093/genetics/155.2.945
Puillandre, N., Brouillet, S., & Achaz, G. (2021). ASAP: Assemble species by automatic partitioning. Molecular Ecology Resources, 21(2), 609–620. https://doi.org/10.1111/1755-0998.13281
Rambaut, A., Drummond, A. J., Xie, D., Baele, G., & Suchard, M. A. (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67(5), 901–904. https://doi.org/10.1093/sysbio/syy032
Rato, C., Sillero, N., Ceacero, F., García-Muñoz, E., & Carretero, M. A. (2021). A survival story: Evolutionary history of the Iberian Algyroides (Squamata: Lacertidae), an endemic lizard relict. Biodiversity and Conservation, 30(10), 2707–2729. https://doi.org/10.1007/s10531-021-02217-4
Rivera, D., Prates, I., Rodrigues, M. T., & Carnaval, A. C. (2020). Effects of climate and geography on spatial patterns of genetic structure in tropical skinks. Molecular Phylogenetics and Evolution, 143, 106661. https://doi.org/10.1016/j.ympev.2019.106661
Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19(12), 1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Rull, V. (2008). Speciation timing and neotropical biodiversity: the Tertiary-Quaternary debate in the light of molecular phylogenetic evidence. Molecular Ecology, 17(11), 2722–2729. https://doi.org/10.1111/j.1365-294X.2008.03789.x
Rull, V. (2011). Neotropical biodiversity: Timing and potential drivers. Trends in Ecology & Evolution, 26(10), 508–513. https://doi.org/10.1016/j.tree.2011.05.011
Sambrook, J., Fritsch, E. F., & Maniatis, R. (1989). Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press.
Santos, M. G., Nogueira, C., Giugliano, L. G., & Colli, G. R. (2014). Landscape evolution and phylogeography of Micrablepharus atticolus (Squamata, Gymnophthalmidae), an endemic lizard of the Brazilian Cerrado. Journal of Biogeography, 41(8), 1506–1519. https://doi.org/10.1111/jbi.12291
Silva, R. C. C., Freitas, M. A., Sant'Anna, S. S., & Seibert, C. S. (2019). Serpentes no Tocantins: guia ilustrado. Anolis Books
South, A. (2011). rworldmap: A New R package for Mapping Global Data. The R Journal, 3(1), 35–43.
Stamatakis, A. (2014). RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9), 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Stephens, M., Smith, N. J., & Donnelly, P. (2001). A new statistical method for haplotype reconstruction from population data. The American Journal of Human Genetics, 68(4), 978–989. https://doi.org/10.1086/319501
Strüssmann, C., & Sazima, I. (1990). Esquadrinhar com a cauda: Uma tática de caça da serpente Hydrodynastes gigas no Pantanal, Mato Grosso. Memórias Do Instituto Butantan, 52(2), 57–61.
Strüssmann, C., & Sazima, I. (1993). The snake Assemblage of the Pantanal at Poconé, Western Brazil: Faunal composition and ecological summary. Studies on Neotropical Fauna and Environment, 28(3), 157–168.
Thuiller, W., Georges, D., Engler, R., & Breiner, F. (2020). biomod2: Ensemble Platform for Species Distribution Modeling. R package version 3.4.6. https://CRAN.R-project.org/package=biomod2
Turchetto-Zolet, A. C., Pinheiro, F., Salgueiro, F., & Palma-Silva, C. (2013). Phylogeographical patterns shed light on evolutionary process in South America. Molecular Ecology, 22(5), 1193–1213. https://doi.org/10.1111/mec.12164
Vargas-Ramírez, M., Caballero, S., Morales-Betancourt, M. A., Lasso, C. A., Amaya, L., Martínez, J. G., Vianag, M. N. S., Vogt, R. C., Farias, I. P., Hrbek, T., Campbell, P. D., & Fritz, U. (2020). Genomic analyses reveal two species of the matamata (Testudines: Chelidae: Chelus spp.) and clarify their phylogeography. Molecular Phylogenetics and Evolution, 148, 106823. https://doi.org/10.1016/j.ympev.2020.106823
Vasconcellos, M. M., Colli, G. R., Weber, J. N., Ortiz, E. M., Rodrigues, M. T., & Cannatella, D. C. (2019). Isolation by instability: Historical climate change shapes population structure and genomic divergence of treefrogs in the Neotropical Cerrado savanna. Molecular Ecology, 28(7), 1748–1764. https://doi.org/10.1111/mec.15045
Warren, D., & Dinnage, R. (2020). ENMTools: Analysis of Niche Evolution using Niche and Distribution Models. R package version 1.0.2. https://CRAN.R-project.org/package=ENMTools
Werneck, F. P., Gamble, T., Colli, G. R., Rodrigues, M. T., & Sites, J. W., Jr. (2012). Deep diversification and long-term persistence in the South American ‘dry diagonal’: Integrating continent-wide phylogeography and distribution modeling of geckos. Evolution: International Journal of Organic Evolution, 66(10), 3014–3034. https://doi.org/10.1111/j.1558-5646.2012.01682.x
Zaher, H., Murphy, R. W., Arredondo, J. C., Graboski, R., Machado-Filho, P. R., Mahlow, K., Montingelli, G. G., Quadros, A. B., Orlov, K. L., Wilkinson, M., Zhang, Y., & Grazziotin, F. G. (2019). Large-scale molecular phylogeny, morphology, divergence-time estimation, and the fossil record of advanced caenophidian snakes (Squamata: Serpentes). PLoS ONE, 14(5), e0216148. https://doi.org/10.1371/journal.pone.0216148
Zamudio, K. R., Bell, R. C., & Mason, N. A. (2016). Phenotypes in phylogeography: Species’ traits, environmental variation, and vertebrate diversification. Proceedings of the National Academy of Sciences, 113(29), 8041–8048. https://doi.org/10.1073/pnas.1602237113
Acknowledgements
We are grateful to Antoine Fouquet, Mael Dewynter, Adrian Garda, Guarino Coli, Miguel Rodrigues, Felipe Curcio, Fernanda Werneck, Camila Ribas, Francisco Franco, Felipe Grazziotin, Rafael Benetti, Matheus Neves, Elvis Almeida and Hugo Cabral for providing tissues samples. We are grateful to Diego Baldo, Carla Bessa and Vanessa Arzamendia for provindig sequences. PSC thanks Jaqueline Battilana, Sarah Mângia and Ricardo Koroiva for their help with the techniques in the molecular laboratory, Sarah Mângia and Eliana Oliveira for their help in editing the sequences.
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PSC, DS, EAM, conceived the ideas, formal analysis; PSC, DS and HZ, data acquisition; PSC, data curation; and PSC led the writing with assistance from EAM, DS and HZ.
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Supplementary file1 (PDF 3409 kb)—Fig. S1 Bayesian gene genealogies Cytb; 16S; Cmos; NT3. Numbers above/below branches are posterior probability (PP) values. Scale bar indicates substitutions per site.
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Carvalho, P.S., Santana, D.J., Zaher, H. et al. Effects of Environmental Variation in Structuring Population Genetic Variation in the False-Water Cobras (Xenodontinae: Hydrodynastes). Evol Biol 50, 224–238 (2023). https://doi.org/10.1007/s11692-023-09601-8
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DOI: https://doi.org/10.1007/s11692-023-09601-8