Pleistocene Climatic Changes Drove Genetic Variation in Southern Atlantic Forest Treefrogs Boana polytaenia (Anura, Hylidae)

Ibrahim Kamel Rodrigues Nehemy; Felipe Camurugi; Diego José Santana

doi:10.1007/s11692-025-09653-y

journal article Open Access Aug 07, 2025

Pleistocene Climatic Changes Drove Genetic Variation in Southern Atlantic Forest Treefrogs Boana polytaenia (Anura, Hylidae)

Ibrahim Kamel Rodrigues Nehemy

Felipe Camurugi

Diego José Santana

Evolutionary Biology Vol. 52 No. 3 pp. 161-181 · Springer International Publishing

View at Publisher Save 10.1007/s11692-025-09653-y

Topics

No keywords indexed for this article. Browse by subject →

References

147

[1]

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 10.1111/ecog.01132

[2]

Amaro, R. C., Rodrigues, M. T., Yonenaga-Yassuda, Y., & Carnaval, A. C. (2012). Demographic processes in the montane Atlantic rainforest: Molecular and cytogenetic evidence from the endemic frog Proceratophrys boiei. Molecular Phylogenetics and Evolution, 62(3), 880–888. https://doi.org/10.1016/j.ympev.2011.11.004 10.1016/j.ympev.2011.11.004

[3]

Antonelli, A. (2015). Biodiversity: Multiple origins of mountain life. Nature, 524, 300–301. https://doi.org/10.1038/nature14645 10.1038/nature14645

[4]

Antonelli, A. (2017). Biogeography: Drivers of bioregionalization. Nature Ecology & Evolution, 1(4), 1–2. https://doi.org/10.1038/s41559-017-0114 10.1038/s41559-017-0114

[5]

Antonelli, A., Kissling, W. D., Flantua, S. G. A., Bermúdez, M. A., Mulch, A., Muellner-Riehl, A. N., Kreft, H., Linder, H. P., Badgley, C., Fjeldså, J., Fritz, S. A., Rahbek, C., Herman, F., Hooghiemstra, H., & Hoorn, C. (2018). Geological and Climatic influences on mountain biodiversity. Nature Geoscience, 11, 718–725. https://doi.org/10.1038/s41561-018-0236-z 10.1038/s41561-018-0236-z

[6]

Avise, J. C. (2009). Phylogeography: Retrospect and prospect. Journal of Biogeography, 36, 3–15. 10.1111/j.1365-2699.2008.02032.x

[7]

Badgley, C., Smiley, T. M., Terry, R., Davis, E. B., DeSantis, L. R., Fox, D. L., Hopkins, S. S. B., Jezkova, T., Matocq, M. D., Matzke, N., McGuire, J. L., Mulch, A., Riddle, B. R., Roth, V. L., Samuels, J. X., Strömberg, C. A. E., & Yanites, B. J. (2017). Biodiversity and topographic complexity: Modern and geohistorical perspectives. Trends in Ecology & Evolution, 32(3), 211–226. https://doi.org/10.1016/j.tree.2016.12.010 10.1016/j.tree.2016.12.010

[8]

Batalha-Filho, H., Cabanne, G. S., & Miyaki, C. Y. (2012). Phylogeography of an Atlantic forest passerine reveals demographic stability through the last glacial maximum. Molecular Phylogenetics and Evolution, 65, 892–902. https://doi.org/10.1016/j.ympev.2012.08.010 10.1016/j.ympev.2012.08.010

[9]

Behling, H., & Negrelle, R. R. (2001). Tropical rain forest and climate dynamics of the Atlantic lowland, Southern brazil, during the late quaternary. Quaternary Research, 56(3), 383–389. https://doi.org/10.1006/qres.2001.2264 10.1006/qres.2001.2264

[10]

Berneck, B. V., Haddad, C. F., Lyra, M. L., Cruz, C. A., & Faivovich, J. (2016). The green clade grows: A phylogenetic analysis of Aplastodiscus (Anura; Hylidae). Molecular Phylogenetics and Evolution, 97, 213–223. https://doi.org/10.1016/j.ympev.2015.11.014 10.1016/j.ympev.2015.11.014

[11]

Bertoluci, J., & Rodrigues, M. T. (2002). Seasonal patterns of breeding activity of Atlantic rainforest anurans at boracéia, southeastern Brazil. Amphibia-Reptilia, 23(2), 161–167. 10.1163/156853802760061804

[12]

Bolívar-Leguizamón, S. D., Silveira, L. F., Derryberry, E. P., Brumfield, R. T., & Bravo, G. A. (2020). Phylogeography of the variable antshrike (Thamnophilus caerulescens), a South American passerine distributed along multiple environmental gradients. Molecular Phylogenetics and Evolution, 148, 106810. https://doi.org/10.1016/j.ympev.2020.106810 10.1016/j.ympev.2020.106810

[13]

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., Suchard, M. A., Wu, C. H., Xie, D., Zhang, C., Stadler, T., & 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 10.1371/journal.pcbi.1006650

[14]

Broennimann, O., Fitzpatrick, M. C., Pearman, P. B., Petitpierre, B., Pellissier, L., Yoccoz, N. G., & Guisan, A. (2012). Measuring ecological niche overlap from occurrence and Spatial environmental data. Global Ecology and Biogeography, 21(4), 481–497. 10.1111/j.1466-8238.2011.00698.x

[15]

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. 10.1038/sdata.2018.254

[16]

Brunes, T. O., Thomé, M. T. C., Alexandrino, J., Haddad, C. F. B., & Sequeira, F. (2015). Ancient divergence and recent population expansion in a leaf frog endemic to the Southern Brazilian Atlantic forest. Organisms Diversity & Evolution, 15(4), 695–710. https://doi.org/10.1007/s13127-015-0228-4 10.1007/s13127-015-0228-4

[17]

Cabanne, G. S., Calderon, L., Arias, N. T., Flores, P., Pessoa, R., D’Horta, F. M., & Miyaki, C. Y. (2016). Effects of pleistocene climate changes on species ranges and evolutionary processes in the Neotropical Atlantic forest. Biological Journal of the Linnean Society, 119, 856–872. https://doi.org/10.1111/bij.12844 10.1111/bij.12844

[18]

Canedo, C., & Haddad, C. F. (2012). Phylogenetic relationships within Anuran clade terrarana, with emphasis on the placement of Brazilian Atlantic rainforest frogs genus Ischnocnema (Anura: Brachycephalidae). Molecular Phylogenetics and Evolution, 65(2), 610–620. https://doi.org/10.1016/j.ympev.2012.07.016 10.1016/j.ympev.2012.07.016

[19]

Caramaschi, U., & Cruz, C. A. G. (2013). A new species of the Hypsiboas polytaenius clade from southeastern Brazil (Anura: Hylidae). South American Journal of Herpetology, 8(2), 121–126. 10.2994/sajh-d-13-00009.1

[20]

Cardoso, D. C., Cristiano, M. P., Tavares, M. G., Schubart, C. D., & Heinze, J. (2015). Phylogeography of the sand Dune ant Mycetophylax simplex along the Brazilian Atlantic forest coast: Remarkably low MtDNA diversity and shallow population structure. BMC Evolutionary Biology, 15(1), 1–13. https://doi.org/10.1186/s12862-015-0383-4 10.1186/s12862-015-0383-4

[21]

Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic forest

Ana Carolina Carnaval, Craig Moritz

Journal of Biogeography 2008 10.1111/j.1365-2699.2007.01870.x

[22]

Carnaval, A. C., Hickerson, M. J., Haddad, C. F. B., Rodrigues, M. T., & Moritz, C. (2009). Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot. Science, 323, 785–789. https://doi.org/10.1126/science.1166955 10.1126/science.1166955

[23]

Carnaval, A. C., Waltari, E., Rodrigues, M. T., Rosauer, D., VanDerWal, J., Damasceno, R., Prates, I., Strangas, M., Spanos, Z., Rivera, D., Pie, M. R., Firkowski, C. R., Bornschein, M. R., Ribeiro, L. F., & Moritz, C. (2014). Prediction of phylogeographic endemism in an environmentally complex biome. Proceedings of the Royal Society B: Biological Sciences, 281(1792), e20141461. https://doi.org/10.1098/rspb.2014.1461 10.1098/rspb.2014.1461

[24]

Cassini, C. S., Cruz, C. A. G., & Caramaschi, U. (2010). Taxonomic review of Physalaemus olfersii (Lichtenstein & martens, 1856) with revalidation of Physalaemus lateristriga (Steindachner, 1864) and description of two new related species (Anura: Leiuperidae). Zootaxa, 2010(2491), 1–33. https://doi.org/10.11646/zootaxa.2491.1.1 10.11646/zootaxa.2491.1.1

[25]

Corander, J., Sirén, J., & Arjas, E. (2008). Bayesian Spatial modeling of genetic population structure. Computational Statistics, 23, 111–129. https://doi.org/10.1007/s00180-007-0072-x 10.1007/s00180-007-0072-x

[26]

Corander, J., Marttinen, P., Sirén, J., & Tang, J. (2013). BAPS: Bayesian analysis of population structure (p. 14). Department of Mathematics ans sctatistics University of Helsinki.

[27]

Costa, L. P., Leite, Y. L., da Fonseca, G. A., & da Fonseca, M. T. (2000). Biogeography of South American forest mammals: Endemism and diversity in the Atlantic forest 1. Biotropica, 32(4b), 872–881. https://doi.org/10.1111/j.1744-7429.2000.tb00625.x 10.1111/j.1744-7429.2000.tb00625.x

[28]

Cruz, C. A. G., & Feio, R. N. (2007). Endemismos Em Anfíbios Em áreas de altitude Na Mata Atlântica no sudeste do Brasil. Herpetologia No Brasil II, 1, 117–126.

[29]

Cruz, C. A. G., Feio, R. N., Caramaschi, U., & Murta, R. (2009). Anfíbios do ibitipoca. Bicho do Mato Editora.

[30]

de Almeida, F. F. M., & Carneiro, C. D. R. (1998). Origem e evolução Da Serra do Mar. Brazilian Journal of Geology, 28(2), 135–150.

[31]

De Mello Martins, F. (2011). Historical biogeography of the Brazilian Atlantic forest and the Carnaval–Moritz model of pleistocene refugia: What do phylogeographical studies tell us? Biological Journal of the Linnean Society, 104(3), 499–509. 10.1111/j.1095-8312.2011.01745.x

[32]

Di Cola, V., Broennimann, O., Petitpierre, B., Breiner, F. T., D’Amen, M., Randin, C., Engler, R., Pottier, J., Pio, D., Dubuis, A., Pellissier, L., Mateo, R. G., Hordijk, W., Salamin, N., & Guisan, A. (2017). Ecospat: An R package to support Spatial analyses and modeling of species niches and distributions. Ecography, 40(6), 774–787. https://doi.org/10.1111/ecog.02671 10.1111/ecog.02671

[33]

Dolan, A. M., Haywood, A. M., Hunter, S. J., Tindall, J. C., Dowsett, H. J., Hill, D. J., & Pickering, S. J. (2015). Modelling the enigmatic late pliocene glacial event—Marine isotope stage M2. Global and Planetary Change, 128, 47–60. 10.1016/j.gloplacha.2015.02.001

[34]

Drummond, A. J., Rambaut, A., Shapiro, B., & Pybus, O. G. (2005). Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution, 22(5), 1185–1192. https://doi.org/10.1093/molbev/msi103 10.1093/molbev/msi103

[35]

Bayesian Phylogenetics with BEAUti and the BEAST 1.7

Alexei J. Drummond, Marc A. Suchard, Dong Xie et al.

Molecular Biology and Evolution 2012 10.1093/molbev/mss075

[36]

MUSCLE: multiple sequence alignment with high accuracy and high throughput

R. C. Edgar

Nucleic Acids Research 2004 10.1093/nar/gkh340

[37]

Excoffier, L., & Lischer, H. E. L. (2010). Arlequin suite v. 3.5: A new series of programs to perform population genetics analyses under Linux and windows. Molecular Ecology Resources, 10, 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x 10.1111/j.1755-0998.2010.02847.x

[38]

Faivovich, J., Garcıa, P. C., Ananias, F., Lanari, L., Basso, N. G., & Wheeler, W. C. (2004). A molecular perspective on the phylogeny of the Hyla pulchella species group (Anura, Hylidae). Molecular Phylogenetics and Evolution, 32(3), 938–950. https://doi.org/10.1016/j.ympev.2004.03.008 10.1016/j.ympev.2004.03.008

[39]

Faivovich, J., Haddad, C. F. B., Garcia, P. C., Frost, D. R., Campbell, J. A., & Wheeler, W. C. (2005). Systematic review of the frog family hylidae, with special reference to hylinae: Phylogenetic analysis and taxonomic revision. Bulletin of the American Museum of Natural History, (294), 1–240. https://doi.org/10.1206/0003-0090(2005)294[0001:SROTFF]2.0.CO;2 10.1206/0003-0090(2005)294[0001:srotff]2.0.co;2

[40]

Faivovich, J., Mcdiarmid, R. W., & Myers, C. W. (2013). Two new species of Myersiohyla (Anura: Hylidae) from Cerro de La neblina, venezuela, with comments on other species of the genus. American Museum Novitates, 2013(3792), 1–63. https://doi.org/10.1206/3792.1 10.1206/3792.1

[41]

Faivovich, J., Pinheiro, P. D., Lyra, M. L., Pereyra, M. O., Baldo, D., Muñoz, A., Reichle, S., Brandão, R. A., Giaretta, A. A., Thomé, M. T. C., Chaparro, J. C., Baêta, D., Widholzer, R. L., Baldo, J., Lehr, E., Wheeler, W. C., Garcia, P. C. A., & Haddad, C. F. B. (2021). Phylogenetic relationships of the Boana pulchella group (Anura: Hylidae). Molecular Phylogenetics and Evolution, 155, 106981. https://doi.org/10.1016/j.ympev.2020.106981 10.1016/j.ympev.2020.106981

[42]

Feng, B., Zhao, Q., Xu, J. P., Qin, J., & Yang, Z. L. (2016). Drainage isolation and climate change-driven population expansion shape the genetic structures of Tuber indicum complex in the Hengduan mountains region. Scientific Reports, 6, 1–10. https://doi.org/10.1038/srep21811 10.1038/srep21811

[43]

Fitzpatrick, S. W., Brasileiro, C. A., Haddad, C. F. B., & Zamudio, K. R. (2009). Geographical variation in genetic structure of an Atlantic coastal forest frog reveals regional differences in habitat stability. Molecular Ecology, 18(13), 2877–2896. https://doi.org/10.1111/j.1365-294X.2009.04245.x 10.1111/j.1365-294x.2009.04245.x

[44]

Fjeldså, J., Bowie, R. C., & Rahbek, C. (2012). The role of mountain ranges in the diversification of birds. Annual Review of Ecology Evolution and Systematics, 43, 249–265. https://doi.org/10.1146/annurev-ecolsys-102710-145113 10.1146/annurev-ecolsys-102710-145113

[45]

Flouri, T., Jiao, X., Rannala, B., & Yang, Z. (2018). Species tree inference with BPP using genomic sequences and the multispecies coales-cent. Molecular Biology and Evolution, 35, 2585–2593. https://doi.org/10.1093/molbev/msy147 10.1093/molbev/msy147

[46]

Fordham, D. A., Saltré, F., Haythorne, S., Wigley, T. M. L., 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 10.1111/ecog.03031

[47]

Fu, Y. X. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147(2), 915–925. https://doi.org/10.1093/genetics/147.2.915 10.1093/genetics/147.2.915

[48]

Gehara, M., Crawford, A. J., Orrico, V. G. D., Rodríguez, A., Lötters, S., Fouquet, A., Barrientos, L. S., Brusquetti, F., De la Riva, I., Ernst, R., Urrutia, G., Glaw, G., Guayasamin, F., Hölting, J. M., Jansen, M., Kok, M., Kwet, P. J. R., Lingnau, A., Lyra, R., Moravec, M., Rojas-Runjaic, J. P. Jr., Schulze, F. J. M., Señaris, A., Solé, J. C., Rodriguez, M. T., Twomey, M., Haddad, E., Vences, C. F. B., 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, e103958. https://doi.org/10.1371/journal.pone.0103958 10.1371/journal.pone.0103958

[49]

Gehara, M., Barth, A., de Oliveira, E. F., Costa, M. A., Haddad, C. F. B., & Vences, M. (2017). Model-based analyses reveal insular population diversification and cryptic frog species in the Ischnocnema parva complex in the Atlantic forest of Brazil. Molecular Phylogenetics and Evolution, 112, 68–78. https://doi.org/10.1016/j.ympev.2017.04.007 10.1016/j.ympev.2017.04.007

[50]

Graham, C. H., Carnaval, A. C., Cadena, C. D., Zamudio, K. R., Roberts, T. E., Parra, J. L., Mccain, C. M., Bowie, R. C. K., Moritz, C., Baines, S. B., Schneider, J. C., Vanderwal, J., Rahbek, C., Kozak, K. H., & Sanders, N. J. (2014). The origin and maintenance of montane diversity: Integrating evolutionary and ecological processes. Ecography, 37, 711–719. https://doi.org/10.1111/ecog.00578 10.1111/ecog.00578

Showing 50 of 147 references

Metrics

1

Citations

147

References

Details

Published: Aug 07, 2025
Vol/Issue: 52(3)
Pages: 161-181
License: View

Authors

I

Ibrahim Kamel Rodrigues Nehemy

Funding

Conselho Nacional de Desenvolvimento Cientifico e Tecnologico Award: CNPQ 133940/2020-9

Fundação de Amparo a Pesquisa do Estado de São Paulo Award: FAPESP 2022/15106-8

Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul Award: #71/700.083/2020

Cite This Article

Ibrahim Kamel Rodrigues Nehemy, Felipe Camurugi, Diego José Santana (2025). Pleistocene Climatic Changes Drove Genetic Variation in Southern Atlantic Forest Treefrogs Boana polytaenia (Anura, Hylidae). Evolutionary Biology, 52(3), 161-181. https://doi.org/10.1007/s11692-025-09653-y

Pleistocene Climatic Changes Drove Genetic Variation in Southern Atlantic Forest Treefrogs Boana polytaenia (Anura, Hylidae)

You May Also Like