Abstract
Evolutionary radiations have been a key paradigm in studying species richness and their temporal and geographic variation. These patterns have been associated with the interaction between the rate at which species originate and the rate at which phenotypic traits evolve. Nevertheless, despite extensive empirical testing, questions remain regarding the prevalence of the coupling between these rates within lineages. Climatic niche evolution is an important driver of speciation since niche divergence and niche conservatism may result in reproductive isolation. Here, we test whether the rate of climatic niche evolution influences the speciation rate for a globally distributed venomous snakes’ clade, the Viperidae family. Contrary to expectations, we found no general relationship between climatic niche evolution rates and vipers’ speciation rates. Our results showed that speciation during the radiation of vipers could have occurred without strong ecological niche divergence, perhaps through a non-adaptive process that could still include a complex pattern of iterated adaptive and non-adaptive radiations.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abbott, R., Albach, D., Ansell, S., Arntzen, J. W., Baird, S. J. E., Bierne, N., Boughman, J., Brelsford, A., Buerkle, C. A., Buggs, R., Butlin, R. K., Dieckmann, U., Eroukhmanoff, F., Grill, A., Cahan, S. H., Hermansen, J. S., Hewitt, G., Hudson, A. G., Jiggins, C., & Zinner, D. (2013). Hybridization and speciation. Journal of Evolutionary Biology, 26(2), 229–246. https://doi.org/10.1111/j.1420-9101.2012.02599.x.
Ahmadi, M., Hemami, M. R., Kaboli, M., Malekian, M., & Zimmermann, N. E. (2019). Extinction risks of a Mediterranean neo-endemism complex of mountain vipers triggered by climate change. Scientific Reports, 9(1), 1–12. https://doi.org/10.1038/s41598-019-42792-9.
Ahmadi, M., Hemami, M. R., Kaboli, M., Nazarizadeh, M., Malekian, M., Behrooz, R., Geniez, P., Alroy, J., & Zimmermann, N. E. (2021). The legacy of Eastern Mediterranean mountain uplifts: Rapid disparity of phylogenetic niche conservatism and divergence in mountain vipers. BMC Ecology and Evolution, 21(1), 1–13. https://doi.org/10.1186/s12862-021-01863-0.
Alencar, L. R. V., Quental, T. B., Grazziotin, F. G., Alfaro, M. L., Martins, M., Venzon, M., & Zaher, H. (2016). Diversification in vipers: Phylogenetic relationships, time of divergence and shifts in speciation rates. Molecular Phylogenetics and Evolution, 105, 50–62. https://doi.org/10.1016/j.ympev.2016.07.029.
Alencar, L. R. V., Martins, M., Burin, G., & Quental, T. B. (2017). Arboreality constrains morphological evolution but not species diversification in vipers. Proceedings of the Royal Society B: Biological Sciences, 284(1869). https://doi.org/10.1098/rspb.2017.1775
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(10), 718–725. https://doi.org/10.1038/s41561-018-0236-z.
Bauwens, D., & Claus, K. (2019). Seasonal variation of mortality, detectability, and body condition in a population of the adder (Vipera berus). Ecology and Evolution, 9(10), 5821–5834. https://doi.org/10.1002/ece3.5166.
Birskis-Barros, I., Alencar, L. R. V., Prado, P. I., Böhm, M., & Martins, M. (2019). Ecological and conservation correlates of rarity in New World pitvipers. Diversity, 11(9), 1–15. https://doi.org/10.3390/d11090147.
Blair, C., & Sánchez-Ramírez, S. (2016). Diversity-dependent cladogenesis throughout western Mexico: Evolutionary biogeography of rattlesnakes (Viperidae: Crotalinae: Crotalus and Sistrurus). Molecular Phylogenetics and Evolution, 97, 145–154. https://doi.org/10.1016/j.ympev.2015.12.020.
Boucher, F. C., Zimmermann, N. E., & Conti, E. (2016). Allopatric speciation with little niche divergence is common among alpine Primulaceae. Journal of Biogeography, 43(3), 591–602. https://doi.org/10.1111/jbi.12652.
Burbrink, F. T., & Guiher, T. J. (2015). Considering gene flow when using coalescent methods to delimit lineages of north american pitvipers of the genus Agkistrodon. Zoological Journal of the Linnean Society, 173(2), 505–526. https://doi.org/10.1111/zoj.12211.
Colwell, R. K., & Rangel, T. F. (2009). Hutchinson’s duality: The once and future niche. Proceedings of the National Academy of Sciences of the United States of America, 106(SUPPL. 2), 19651–19658. https://doi.org/10.1073/pnas.0901650106
Cooney, C. R., & Thomas, G. H. (2021). Heterogeneous relationships between rates of speciation and body size evolution across vertebrate clades. Nature Ecology and Evolution, 5(1), 101–110. https://doi.org/10.1038/s41559-020-01321-y.
Cooney, C. R., Seddon, N., & Tobias, J. A. (2016). Widespread correlations between climatic niche evolution and species diversification in birds. Journal of Animal Ecology, 85(4), 869–878. https://doi.org/10.1111/1365-2656.12530.
Couvreur, T. L. P. (2015). Odd man out: Why are there fewer plant species in african rain forests? Plant Systematics and Evolution, 301(5), 1299–1313. https://doi.org/10.1007/s00606-014-1180-z.
Couvreur, T. L. P., Chatrou, L. W., Sosef, M. S. M., & Richardson, J. E. (2008). Molecular phylogenetics reveal multiple tertiary vicariance origins of the african rain forest trees. BMC Biology, 6, 1–10. https://doi.org/10.1186/1741-7007-6-54.
Coyne, J. A., Coyne, H. A., & Orr, H. A. (2004). Speciation. Incorporated: Oxford University Press. https://books.google.com.mx/books?id=Hq9RswEACAAJ.
Crouch, N. M. A., & Ricklefs, R. E. (2019). Speciation rate is independent of the rate of evolution of morphological size, shape, and absolute morphological specialization in a large clade of birds. American Naturalist, 193(4), https://doi.org/10.1086/701630.
Czekanski-Moir, J. E., & Rundell, R. J. (2019). The Ecology of Nonecological Speciation and Nonadaptive Radiations. Trends in Ecology and Evolution, 34(5), 400–415. https://doi.org/10.1016/j.tree.2019.01.012.
D’Elía, G., Fabre, P. H., & Lessa, E. P. (2019). Rodent systematics in an age of discovery: Recent advances and prospects. Journal of Mammalogy, 100(3), 852–871. https://doi.org/10.1093/jmammal/gyy179.
Dolédec, S., Chessel, D., & Gimaret-Carpentier, C. (2000). Niche separation in community analysis: A new method. Ecology, 81(10), 2914–2927. https://doi.org/10.1890/0012-9658(2000)081[2914:NSICAA]2.0.CO;2.
Douglas, M. E., Douglas, M. R., Schuett, G. W., & Porras, L. W. (2006). Evolution of rattlesnakes (Viperidae; Crotalus) in the warm deserts of western North America shaped by Neogene vicariance and quaternary climate change. Molecular Ecology, 15(11), 3353–3374. https://doi.org/10.1111/j.1365-294X.2006.03007.x.
Drovetski, S. V., Semenov, G., Drovetskaya, S. S., Fadeev, I. V., Red’kin, Y. A., & Voelker, G. (2013). Geographic mode of speciation in a mountain specialist avian family endemic to the Palearctic. Ecology and Evolution, 3(6), 1518–1528. https://doi.org/10.1002/ece3.539.
Encarnación-Luévano, A., Peterson, A. T., & Rojas-Soto, O. R. (2021). Burrowing habit in Smilisca frogs as an adaptive response to ecological niche constraints in seasonally dry environments. Frontiers of Biogeography, 13(4), 1–14. https://doi.org/10.21425/F5FBG50517.
Esparza-Estrada, C. E., Terribile, L. C., Rojas-Soto, O., Yáñez-Arenas, C., & Villalobos, F. (2022). Evolutionary dynamics of climatic niche influenced the current geographical distribution of Viperidae (Reptilia: Squamata) worldwide. Biological Journal of the Linnean Society, 135(4), 665–678. https://doi.org/10.1093/biolinnean/blac012.
Fick, S. E., & Hijmans, R. J. (2017). WorldClim 2: New 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37(12), 4302–4315. https://doi.org/10.1002/joc.5086.
Fisher-Reid, M. C., Kozak, K. H., & Wiens, J. J. (2012). How is the rate of climatic-niche evolution related to climatic-niche breadth? Evolution, 66(12), 3836–3851. https://doi.org/10.1111/j.1558-5646.2012.01729.x.
Folk, R. A., Stubbs, R. L., Mort, M. E., Cellinese, N., Allen, J. M., Soltis, P. S., Soltis, D. E., & Guralnick, R. P. (2019). Rates of niche and phenotype evolution lag behind diversification in a temperate radiation. Proceedings of the National Academy of Sciences of the United States of America, 166(22), 10874–10882. https://doi.org/10.1073/pnas.1817999116.
Gouveia, S. F., Hortal, J., Tejedo, M., Duarte, H., Cassemiro, F. A. S., Navas, C. A., & Diniz-Filho, J. A. F. (2014). Climatic niche at physiological and macroecological scales: The thermal tolerance-geographical range interface and niche dimensionality. Global Ecology and Biogeography, 23(4), 446–456. https://doi.org/10.1111/geb.12114.
Guiller, G., Lourdais, O., & Ursenbacher, S. (2017). Hybridization between a Euro-Siberian (Vipera berus) and a para-mediterranean viper (V. aspis) at their contact zone in western France. Journal of Zoology, 302(2), 138–147. https://doi.org/10.1111/jzo.12431.
Hagen, O., Skeels, A., Onstein, R. E., Jetz, W., & Pellissier, L. (2021). Earth history events shaped the evolution of uneven biodiversity across tropical moist forests. Proceedings of the National Academy of Sciences of the United States of America, 118(40), https://doi.org/10.1073/pnas.2026347118.
Hua, X., & Wiens, J. J. (2013). How does climate influence speciation? American Naturalist, 182(1), 1–12. https://doi.org/10.1086/670690.
Jezkova, T., & Wiens, J. J. (2018). Testing the role of climate in speciation: New methods and applications to squamate reptiles (lizards and snakes). Molecular Ecology, 27(12), 2754–2769. https://doi.org/10.1111/mec.14717.
Kissling, W. D., Eiserhardt, W. L., Baker, W. J., Borchsenius, F., Couvreur, T. L. P., Balslev, H., & Svenning, J. C. (2012). Cenozoic imprints on the phylogenetic structure of palm species assemblages worldwide. Proceedings of the National Academy of Sciences of the United States of America, 109(19), 7379–7384. https://doi.org/10.1073/pnas.1120467109.
Koch, E. L., Neiber, M. T., Walther, F., & Hausdorf, B. (2020). Patterns and processes in a non-adaptive radiation: Alopia (Gastropoda, Clausiliidae) in the Bucegi Mountains. Zoologica Scripta, 49(3), 280–294. https://doi.org/10.1111/zsc.12406.
Lee, M. S. Y., Sanders, K. L., King, B., & Palci, A. (2016). Diversification rates and phenotypic evolution in venomous snakes (Elapidae). Royal Society Open Science, 3(1), https://doi.org/10.1098/rsos.150277.
Losos, J. B. (2010). Adaptive radiation, ecological opportunity, and evolutionary determinism: American society of naturalists E. O. Wilson award address. American Naturalist, 175(6), 623–639. https://doi.org/10.1086/652433.
Lourenço-de-Moraes, R., Lansac-Toha, F. M., Schwind, L. T. F., Arrieira, R. L., Rosa, R. R., Terribile, L. C., Lemes, P., Rangel, F., Diniz-Filho, T., Bastos, J. A. F., R. P., & Bailly, D. (2019). Climate change will decrease the range size of snake species under negligible protection in the brazilian Atlantic Forest hotspot. Scientific Reports, 9(1), 1–14. https://doi.org/10.1038/s41598-019-44732-z.
Machado, T., Silva, V. X., & de Silva, M. J. J (2014). Phylogenetic relationships within Bothrops neuwiedi group (Serpentes, Squamata): Geographically highly-structured lineages, evidence of introgressive hybridization and Neogene/Quaternary diversification. Molecular Phylogenetics and Evolution, 71(1), 1–14. https://doi.org/10.1016/j.ympev.2013.10.003.
Maestri, R., Monteiro, L. R., Fornel, R., Upham, N. S., Patterson, B. D., & de Freitas, T. R. O. (2017). The ecology of a continental evolutionary radiation: Is the radiation of sigmodontine rodents adaptive? Evolution, 71(3), 610–632. https://doi.org/10.1111/evo.13155.
Mahler, D. L., Revell, L. J., Glor, R. E., & Losos, J. B. (2010). Ecological opportunity and the rate of morphological evolution in the diversification of greater Antillean anoles. Evolution, 64(9), 2731–2745. https://doi.org/10.1111/j.1558-5646.2010.01026.x.
Mammola, S., Piano, E., Malard, F., Vernon, P., & Isaia, M. (2019). Extending Janzen’s hypothesis to temperate regions: A test using subterranean ecosystems. Functional Ecology, 33(9), 1638–1650. https://doi.org/10.1111/1365-2435.13382.
Martínez-Freiría, F., Crochet, P. A., Fahd, S., Geniez, P., Brito, J. C., & Velo-Antón, G. (2017). Integrative phylogeographical and ecological analysis reveals multiple pleistocene refugia for Mediterranean Daboia vipers in north-west Africa. Biological Journal of the Linnean Society, 122(2), 366–384. https://doi.org/10.1093/biolinnean/blx038.
Martínez-Freiría, F., Freitas, I., Zuffi, M. A. L., Golay, P., Ursenbacher, S., & Velo-Antón, G. (2020). Climatic refugia boosted allopatric diversification in western Mediterranean vipers. Journal of Biogeography, 47(8), 1698–1713. https://doi.org/10.1111/jbi.13861.
Mason, N. A., Burns, K. J., Tobias, J. A., Claramunt, S., Seddon, N., & Derryberry, E. P. (2017). Song evolution, speciation, and vocal learning in passerine birds. Evolution, 71(3), 786–796. https://doi.org/10.1111/evo.13159.
Mason, A. J., Grazziotin, F. G., Zaher, H., Lemmon, A. R., Lemmon, M., E., & Parkinson, C. L. (2019). Reticulate evolution in nuclear Middle America causes discordance in the phylogeny of palm-pitvipers (Viperidae: Bothriechis). Journal of Biogeography, 46(5), 833–844. https://doi.org/10.1111/jbi.13542.
Moen, D. S., Irschick, D. J., & Wiens, J. J. (2013). Evolutionary conservatism and convergence both lead to striking similarity in ecology, morphology and performance across continents in Frogs. Proceedings of the Royal Society B: Biological Sciences, 280(1773). https://doi.org/10.1098/rspb.2013.2156
Myers, E. A. (2021). Genome-wide data reveal extensive gene flow during the diversification of the western rattlesnakes (Viperidae: Crotalinae: Crotalus). Molecular Phylogenetics and Evolution, 165, 107313. https://doi.org/10.1016/j.ympev.2021.107313.
Nordberg, E. J., & Cobb, V. A. (2016). Midwinter Emergence in hibernating timber rattlesnakes (Crotalus horridus). Journal of Herpetology, 50(2), 203–208. https://doi.org/10.1670/14-113.
Pagel, M., & Meade, A. (2006). Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. American Naturalist, 167(6), 808–825. https://doi.org/10.1086/503444.
Peixoto, F. P., Villalobos, F., & Cianciaruso, M. V. (2017). Phylogenetic conservatism of climatic niche in bats. Global Ecology and Biogeography, 26(9), 1055–1065. https://doi.org/10.1111/geb.12618.
Peterson, A. T., Soberón, J., & Sánchez-Cordero, V. (1999). Conservatism of ecological niches in evolutionary time. Science, 285(5431), 1265–1267. https://doi.org/10.1126/science.285.5431.1265.
Plana, V. (2004). Mechanisms and tempo of evolution in the african guineo-congolian rainforest. Philosophical Transactions of the Royal Society B: Biological Sciences, 359(1450), 1585–1594. https://doi.org/10.1098/rstb.2004.1535.
Price, S. L., Etienne, R. S., & Powell, S. (2016). Tightly congruent bursts of lineage and phenotypic diversification identified in a continental ant radiation. Evolution, 70(4), 903–912. https://doi.org/10.1111/evo.12894.
Puttick, M. N., Ingram, T., Clarke, M., & Thomas, G. H. (2020). MOTMOT: Models of trait macroevolution on trees (an update). Methods in Ecology and Evolution, 11(3), 464–471. https://doi.org/10.1111/2041-210X.13343.
Pyron, R. A., Costa, G. C., Patten, M. A., & Burbrink, F. T. (2015). Phylogenetic niche conservatism and the evolutionary basis of ecological speciation. Biological Reviews, 90(4), 1248–1262. https://doi.org/10.1111/brv.12154.
Rabosky, D. L. (2014). Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. Plos One, 9(2), https://doi.org/10.1371/journal.pone.0089543.
Rabosky, D. L., & Adams, D. C. (2012). Rates of morphological evolution are correlated with species richness in salamanders. Evolution, 66(6), 1807–1818. https://doi.org/10.1111/j.1558-5646.2011.01557.x.
Ramírez-Reyes, T., Velasco, J. A., Flores-Villela, O., & Piñero, D. (2022). Decoupling in diversification and body size Rates during the Radiation of Phyllodactylus: Evidence suggests minor role of Ecology in shaping phenotypes. Evolutionary Biology, 49(3), 373–387. https://doi.org/10.1007/s11692-022-09575-z.
Reis, J., Bidau, C. J., Maestri, R., & Martinez, P. A. (2018). Diversification of the climatic niche drove the recent processes of speciation in Sigmodontinae (Rodentia, Cricetidae). Mammal Review, 48(4), 328–332. https://doi.org/10.1111/mam.12128.
Reznick, D. N., & Ricklefs, R. E. (2009). Darwin’s bridge between microevolution and macroevolution. Nature, 457(7231), 837–842. https://doi.org/10.1038/nature07894.
Roll, U., Feldman, A., Novosolov, M., Allison, A., Bauer, A. M., Bernard, R., Böhm, M., Castro-Herrera, F., Chirio, L., Collen, B., Colli, G. R., Dabool, L., Das, I., Doan, T. M., Grismer, L. L., Hoogmoed, M., Itescu, Y., Kraus, F., Lebreton, M., & Meiri, S. (2017). The global distribution of tetrapods reveals a need for targeted reptile conservation. Nature Ecology and Evolution, 1(11), 1677–1682. https://doi.org/10.1038/s41559-017-0332-2.
Rundell, R. J., & Price, T. D. (2009). Adaptive radiation, nonadaptive radiation, ecological speciation and nonecological speciation. Trends in Ecology and Evolution, 24(7), 394–399. https://doi.org/10.1016/j.tree.2009.02.007.
Schluter, D. (2009). Evidence for ecological speciation and its alternative. Science, 323(5915), 737–741. https://doi.org/10.1126/science.1160006.
Schnitzler, J., Graham, C. H., Dormann, C. F., Schiffers, K., & Linder, P., H (2012). Climatic niche evolution and species diversification in the cape flora, South Africa. Journal of Biogeography, 39(12), 2201–2211. https://doi.org/10.1111/jbi.12028.
Seeholzer, G. F., Claramunt, S., & Brumfield, R. T. (2017). Niche evolution and diversification in a neotropical radiation of birds (Aves: Furnariidae). Evolution, 71(3), 702–715. https://doi.org/10.1111/evo.13177.
Simões, M., Breitkreuz, L., Alvarado, M., Baca, S., Cooper, J. C., Heins, L., Herzog, K., & Lieberman, B. S. (2016). The evolving theory of evolutionary radiations. Trends in Ecology and Evolution, 31(1), 27–34. https://doi.org/10.1016/j.tree.2015.10.007.
Stephens, P. R., & Wiens, J. J. (2003). Explaining species richness from continents to communities: The time-for-speciation effect in emydid turtles. The American Naturalist, 161(1), 112–128. https://doi.org/10.1086/345091.
Stroud, J. T., & Losos, J. B. (2020). Bridging the process-pattern divide to understand the Origins and Early Stages of Adaptive Radiation: A review of approaches with insights from studies of Anolis Lizards. Journal of Heredity, 111(1), 33–42. https://doi.org/10.1093/jhered/esz055.
Svensson, E. I. (2012). Non-ecological speciation, niche conservatism and thermal adaptation: How are they connected? Organisms Diversity and Evolution, 12(3), 229–240. https://doi.org/10.1007/s13127-012-0082-6.
Tarroso, P., Pereira, R. J., Martínez-Freiría, F., Godinho, R., & Brito, J. C. (2014). Hybridization at an ecotone: Ecological and genetic barriers between three Iberian vipers. Molecular Ecology, 23(5), 1108–1123. https://doi.org/10.1111/mec.12671.
Terribile, L. C., Diniz-Filho, J. A. F., Rodríguez, M., & Rangel, T. F. L. V. B. (2009). Richness patterns, species distributions and the principle of extreme deconstruction. Global Ecology and Biogeography, 18(2), 123–136. https://doi.org/10.1111/j.1466-8238.2008.00440.x.
Timms, J., Chaparro, J. C., Venegas, P. J., Salazar-Valenzuela, D., Scrocchi, G., Cuevas, J., Leynaud, G., & Carrasco, P. A. (2019). A new species of pitviper of the genus Bothrops (Serpentes: Viperidae: Crotalinae) from the Central Andes of South America. Zootaxa, 4656(1), 99–120. https://doi.org/10.11646/zootaxa.4656.1.4.
Title, P. O., & Burns, K. J. (2015). Rates of climatic niche evolution are correlated with species richness in a large and ecologically diverse radiation of songbirds. Ecology Letters, 18(5), 433–440. https://doi.org/10.1111/ele.12422.
Turelli, M., Barton, N. H., & Coyne, J. A. (2001). Theory and speciation. Trends in Ecology and Evolution, 16(7), 330–343. https://doi.org/10.1016/S0169-5347(01)02177-2.
Uetz, P., Koo, M. S., Catenazzi, A., Aguilar, R., Brings, E., Chang, A. T., Chaitanya, R., Freed, P., Gross, J., Hammermann, M., Lambert, H. O. Å. E. K. J., Sergi, M., Spencer, Z., Summers, C. L., Tarvin, K., Vredenburg, R., V. T., & Wake, D. B. (2021). A quarter century of Reptile and Amphibian Databases. Herpetological Review, 52(2), 246–255.
Vaux, F., Trewick, S. A., & Morgan-Richards, M. (2016). Lineages, splits and divergence challenge whether the terms anagenesis and cladogenesis are necessary. Biological Journal of the Linnean Society, 117(2), 165–176. https://doi.org/10.1111/bij.12665.
Velasco, J. A., Martínez-Meyer, E., Flores-Villela, O., García, A., Algar, A. C., Köhler, G., & Daza, J. M. (2016). Climatic niche attributes and diversification in Anolis lizards. Journal of Biogeography, 43(1), 134–144. https://doi.org/10.1111/jbi.12627.
Vilela, B., & Villalobos, F. (2015). LetsR: A new R package for data handling and analysis in macroecology. Methods in Ecology and Evolution, 6(10), 1229–1234. https://doi.org/10.1111/2041-210X.12401.
Wiens, J. J. (2004). Speciation and ecology revisited: Phylogenetic niche conservatism and the origin of species. Evolution, 58(1), 193–197.
Wiens, J. J., & Donoghue, M. J. (2004). Historical biogeography, ecology and species richness. Trends in Ecology and Evolution, 19(12), 639–644. https://doi.org/10.1016/j.tree.2004.09.011.
Wüster, W., Peppin, L., Pook, C. E., & Walker, D. E. (2008). A nesting of vipers: Phylogeny and historical biogeography of the Viperidae (Squamata: Serpentes). Molecular Phylogenetics and Evolution, 49(2), 445–459. https://doi.org/10.1016/j.ympev.2008.08.019.
Xu, W., Dong, W. J., Fu, T. T., Gao, W., Lu, C. Q., Yan, F., Wu, Y. H., Jiang, K., Jin, J. Q., Chen, H. M., Zhang, Y. P., Hillis, D. M., & Che, J. (2021). Herpetological phylogeographic analyses support a Miocene focal point of himalayan uplift and biological diversification. National Science Review, 8(9), https://doi.org/10.1093/nsr/nwaa263.
Zelditch, M. L., Li, J., Tran, L. A. P., & Swiderski, D. L. (2015). Relationships of diversity, disparity, and their evolutionary rates in squirrels (Sciuridae). Evolution, 69(5), 1284–1300. https://doi.org/10.1111/evo.12642.
Zhou, Y., Duvaux, L., Ren, G., Zhang, L., Savolainen, O., & Liu, J. (2017). Importance of incomplete lineage sorting and introgression in the origin of shared genetic variation between two closely related pines with overlapping distributions. Heredity, 118(3), 211–220. https://doi.org/10.1038/hdy.2016.72.
Zinenko, O., Sovic, M., Joger, U., & Gibbs, H. L. (2016). Hybrid origin of european vipers (Vipera magnifica and Vipera orlovi) from the Caucasus determined using genomic scale DNA markers. BMC Evolutionary Biology, 16(1), 1–13. https://doi.org/10.1186/s12862-016-0647-7.
Acknowledgements
CEEE thanks the Doctoral Program of the Instituto de Ecología, A.C. (INECOL) and the support of the Consejo Nacional de Ciencia y Tecnología (CONACYT, México) for providing a scholarship (number 635993).
Author information
Authors and Affiliations
Contributions
CEEE and FV conceived and designed the study; CEEE collected and analyzed the data; CEEE led the writing with inputs from all authors. All authors contributed critically to the drafts and gave final approval for publication.
Corresponding authors
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Competing Interests
The authors declare no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Esparza-Estrada, C.E., Alencar, L.R., Terribile, L.C. et al. Vipers on the Scene: Assessing the Relationship Between Speciation and Climatic Niche Evolution in Venomous Snakes (Reptilia: Viperidae). Evol Biol 50, 264–273 (2023). https://doi.org/10.1007/s11692-023-09604-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11692-023-09604-5