Articles
Can neutral genetic differentiation explain geographical variation in body size of the natterjack toad, Epidalea calamita?
Published 2023-12-27
Keywords
- Epidalea,
- FST,
- microsatellite loci,
- population differentiation,
- body size
How to Cite
Marangoni, F. (2023). Can neutral genetic differentiation explain geographical variation in body size of the natterjack toad, Epidalea calamita?. Acta Herpetologica, 18(2), 69–78. https://doi.org/10.36253/a_h-13774
Copyright (c) 2023 Federico Marangoni
This work is licensed under a Creative Commons Attribution 4.0 International License.
Abstract
Population genetic studies are crucial for evolutionary biologists because the population is the basic substrate on which evolution is forged. However little empirical evidence has been able to demonstrate the role that isolation and gene flow play in maintaining differentiation in populations at short geographic scales. Epidalea calamita exhibits a steep variation in body size and reproductive traits in southwestern Spain, associated with changes in the geological substrate. This implies a decrease of 70.9% of body mass and 28.5% in snout-vent length, on a micro-geographic scale of only 60 km. Previous results from both metamorphic and juvenile common garden experiments showed that genetic differentiation may be a causal determinant of geographic variation in adult. This study tested whether neutral genetic differentiation can explain the geographical variation in the body size observed in E. calamita. It was addressed analyzing the level of genetic structuring and gene flow among populations along the cline, comparing the genetic diversity between and within populations, as well as between ecological environments. The study showed that the geographic variation in body size observed in E. calamita has evolved in absence of geographic isolation, with moderate gene flow connecting the populations. Thus, neutral genetic differentiation cannot explain the geographical variation observed. Future studies are needed on the interaction between the genetic component with the environmental factors and will be necessary to analyze the contribution of the maternal effects in the origin and evolution of the geographical variation in the body size observed in E. calamita from southern Spain.
References
Adams, D.C., Church, J.O. (2008): Amphibians do not follow Bergmann’s rule. Evolution. 62: 413-420.
Albert, E.M., García‑Navas, V. (2022): Population structure and genetic diversity of the threatened pygmy newt Triturus pygmaeus in a network of natural and artificial ponds. Conserv. Genet. 23: 575-588.
Ashton, K.G. (2002): Do amphibians follow Bergmann’s rule? Can. J. Zool. 80: 708-716.
Avise, J.C. (1994): Molecular markers, natural history and evolution. Kluwer Academic Publishers, Boston.
Beebee, T.J.C., Rowe, G. (2000): Microsatellite analysis of natterjack toad Bufo calamita Laurenti populations: consequences of dispersal from a Pleistocene refugium. Biol. J. Linn. Soc. 69: 367-381.
Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N., Bonhomme, F. (2002): GENETIX 4.04, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier.
Bensch, S., Andersson, T., Akesson, S. (1999): Morphological and molecular variation across a migratory divide in willow warblers, Phylloscopus trochilus. Evolution. 53: 1925-1935.
Bergmann, C. (1847): Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Göttinger Studien. 3: 595.
Bernardo, J. (1996): Maternal effects in animal ecology. Am. Zool. 36: 83-105.
Bradshaw, A.D. (1965): Evolutionary significance of phenotypic plasticity in plants. Adv. Genet. 13: 115-155.
Cvetkovic, D., Tomasevic, N., Ficetola, G.F., Crnobrnja-Isailovic, J., Miaud, C. (2009): Bergmann’s rule in amphibians: combining demographic and ecological parameters to explain body size variation among populations in the common toad Bufo bufo. J. Zool. Syst. Evol. Res. 47: 171-180.
Endler, J.A. (1977): Geographic variation, speciation, and clines. Princeton University Pess, Princeton, New Jersey.
Excoffier, J., Smouse, P., Quattro, J. (1992): Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics. 136: 343-359.
Foster, S.A., Endler, J.A. (1999): Thoughts on geographic variation in behavior. In: Geographic variation in behaviour, pp. 287-307. Foster, S.A, Endler, J.A, Eds, Oxford University Press, New York, Oxford.
Garant, D., Kruuk, L.E.B, Wilkin, T.A., McCleery, R.H., Sheldon, B.C. (2005): Evolution driven by differential dispersal within a wild bird population. Nature. 433: 60-65.
García-París, M., Alcobendas, M., Alberch, P. (1998): Influence of the Guadalquivir river basin on Mitocondrial DNA evolution of Salamandra salamandra (Caudata: Salamandridae) from Southern Spain. Copeia. 1: 174-176.
Gomez-Mestre, I. (2001): Variación geográfica y adaptación local al estrés osmótico en el sapo corredor, Bufo calamita. Unpublished doctoral dissertation. University of Seville, Spain.
Gomez-Mestre I., Tejedo, M. (2004): Contrasting patterns of quantitative and neutral genetic variation in locally adapted populations of the natterjack toad Bufo calamita. Evolution. 58: 2343-2352.
Goudet, J. (2001): FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available at: http://www.unil.ch/izea/softwares/fstat-html.
Harper, J. (1977): Population biology of plants. Academic Press, New York, USA.
Hewitt, G.M. (1996): Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linn. Soc. 58: 247-276.
Jensen, J.L., Bohonak, A.J., Kelley, S.T. (2005): Isolation by distance, web service. BMC Genetics 6:13.
Kennington, W. J., Gockel, J., Partridge, L. (2002). Testing for asymmetrical gene flow in a Drosophila melanogaster body-size cline. Genetics. 165: 667-673.
Leblois, R., Rousset, F., Tikel, D., Moritz, C. (2000). Absence of evidence for isolation by distance in an expanding cane toad (Bufo marinus) population: an individual-based analysis of microsatellite genotypes. Mol. Ecol. 9: 1905-1909.
Lee, H.J., Broggi, J., Sánchez-Montes, G., Díaz-Paniagua, C., Gomez-Mestre, I. (2020): Dwarfism in close continental amphibian populations despite lack of genetic isolation. Oikos. 129: 1243-1256.
Lenormand, T. (2002): Gene flow and the limits to natural selection. Trends Ecol. Evol. 17: 183-189.
Lindsey, C.C. (1966): Body sizes of poikilotherm vertebrates at different latitudes. Evolution. 20: 456-465.
López-Martínez, N. (1989): Tendencias en paleobiogeografia. El futuro de la biogeografía del pasado. In: Paleontologia, pp. 271-296. Aguirre, E., Coord, C.S.I.C., Madrid, Spain.
Marangoni, F. 2006. Variación clinal en el tamaño del cuerpo a escala microgeográfica en dos especies de anuros (Pelobates cultripes y Bufo calamita). Unpublished doctoral dissertation. University of Seville, Spain.
Marangoni, F., Tejedo, M. (2008): Variation in body size and metamorphic traits of Iberian spadefoot toads over a short geographic distance. J. Zool. 275: 97-105.
Marangoni, F., Tejedo, M., Cogălniceanu, D. (2021): Can age and growth patterns explain the geographical variation in the body size of two toad species? An. Acad. Bras. Cienc. (2021) 93(2): e20190470.
Marangoni, F., Tejedo, M., Gomez-Mestre, I. (2008): Extreme reduction in body size and reproductive output associated with sandy substrates in two anuran species. Amphibia-Reptilia. 29: 541-553.
Mayr, E. (1963): Animal Species and Evolution. Harvard University Press. Cambridge, UK.
Mousseau, T.E., Fox, C.W. (1998). Maternal effects as adaptations. Oxford University Press, New York.
Postma, E., Noordwijk van, A.J. (2005): Gene flow a large genetic difference in clutch size at a small spatial scale. Nature. 433: 65-68.
Räsänen, K., Laurila, A., Merilä, J. (2003): Geographic variation in acid stress tolerance of the moor frog, Rana arvalis. II. Adaptive maternal effects. Evolution. 57: 363-371.
Räsänen, K., Laurila, A., Merilä, J. (2005): Maternal investment in egg size: environment- and population-specific effects on offspring performance. Oecologia. 142: 546-553.
Ray, C. (1960): The application of Bergmann's and Allen's rules to the poikilotherms. J. Morphol. 106: 85-108.
Raymond, M., Rousset, F. (1995): GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Heredity. 86: 248-249
Rousset, F. (1997): Genetic Differentiation and estimation on gene flow from F-statistics under isolation by distance. Genetics. 145: 1219-1228.
Rowe, G.T., Beebee, T.J.C, Burke, T. (1997): PCR primers for polymorphic microsatellite loci in the anuran amphibian Bufo calamita. Mol. Ecol. 6: 401-402.
Rowe, G.T., Beebee, T.J.C, Burke, T. (1998): Phylogeography of the natterjack toad Bufo calamita in Britain: genetic differentiation of native and translocated populations. Mol. Ecol. 7: 751-760.
Schmalhausen, I. (1949): Factor of evolution: The theory of stabilizing selection. Philadelphia: Blakiston.
Schneider, S., Roessli, D., Excoffier, L. (2000): Arlequin: a software for population genetics data analysis. Ver. 2.000. Genetics and Biometry Lab, Dept. of Anthropology, University of Geneva, Geneva, Switzerland.
Sinsch, U., Marangoni, F., Oromi, N., Leskovar, C., Sanuy, D., Tejedo, M. (2010): Proximate mechanisms determining size variability in natterjack toads. J. Zool. 281: 272-281.
Skelly, D.K. (2004): Microgeographic countergradient variation in the wood frog, Rana sylvatica. Evolution. 58: 160-165.
Slatkin, M. (1985): Gene flow in natural populations. Annu. Rev. Ecol. Syst. 16: 393-430.
Slatkin, M. (1987): Gene flow and the geographic structure of natural populations. Science. 236: 787-792.
Slatkin, M. (1995): A measure of population subdivision based on microsatellite allele frequencies. Genetics. 139: 457-462.
Sokal, R.R., Rohlf, F.J. (1995): Biometry. W. H. Freeman & Company. New York.
Stearns, S.C. (1989): The evolutionary significance of phenotypic plasticity. BioScience. 39: 436-445.
Stebbins, G.L. (1950): Variation and Evolution in Plants. Columbia University Press. New York.
Taberlet, P., Fumagalli, L., Wust-Scaucy, A.G., Cosson, J.F. (1998): Comparative phylogeography and postglacial colonisation routes in Europe. Mol. Ecol. 7: 453-464.
Via, S., Lande, R. (1985): Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution. 39: 505-523.
Weir, B.S., Cockerham, C.C. (1984): Estimating F-statistics for the analysis of populations structure. Evolution. 38: 358-1370.
Wright, S. (1951): The genetical structure of populations. Ann. Eugenic. 15: 323-354.
Albert, E.M., García‑Navas, V. (2022): Population structure and genetic diversity of the threatened pygmy newt Triturus pygmaeus in a network of natural and artificial ponds. Conserv. Genet. 23: 575-588.
Ashton, K.G. (2002): Do amphibians follow Bergmann’s rule? Can. J. Zool. 80: 708-716.
Avise, J.C. (1994): Molecular markers, natural history and evolution. Kluwer Academic Publishers, Boston.
Beebee, T.J.C., Rowe, G. (2000): Microsatellite analysis of natterjack toad Bufo calamita Laurenti populations: consequences of dispersal from a Pleistocene refugium. Biol. J. Linn. Soc. 69: 367-381.
Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N., Bonhomme, F. (2002): GENETIX 4.04, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier.
Bensch, S., Andersson, T., Akesson, S. (1999): Morphological and molecular variation across a migratory divide in willow warblers, Phylloscopus trochilus. Evolution. 53: 1925-1935.
Bergmann, C. (1847): Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Göttinger Studien. 3: 595.
Bernardo, J. (1996): Maternal effects in animal ecology. Am. Zool. 36: 83-105.
Bradshaw, A.D. (1965): Evolutionary significance of phenotypic plasticity in plants. Adv. Genet. 13: 115-155.
Cvetkovic, D., Tomasevic, N., Ficetola, G.F., Crnobrnja-Isailovic, J., Miaud, C. (2009): Bergmann’s rule in amphibians: combining demographic and ecological parameters to explain body size variation among populations in the common toad Bufo bufo. J. Zool. Syst. Evol. Res. 47: 171-180.
Endler, J.A. (1977): Geographic variation, speciation, and clines. Princeton University Pess, Princeton, New Jersey.
Excoffier, J., Smouse, P., Quattro, J. (1992): Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics. 136: 343-359.
Foster, S.A., Endler, J.A. (1999): Thoughts on geographic variation in behavior. In: Geographic variation in behaviour, pp. 287-307. Foster, S.A, Endler, J.A, Eds, Oxford University Press, New York, Oxford.
Garant, D., Kruuk, L.E.B, Wilkin, T.A., McCleery, R.H., Sheldon, B.C. (2005): Evolution driven by differential dispersal within a wild bird population. Nature. 433: 60-65.
García-París, M., Alcobendas, M., Alberch, P. (1998): Influence of the Guadalquivir river basin on Mitocondrial DNA evolution of Salamandra salamandra (Caudata: Salamandridae) from Southern Spain. Copeia. 1: 174-176.
Gomez-Mestre, I. (2001): Variación geográfica y adaptación local al estrés osmótico en el sapo corredor, Bufo calamita. Unpublished doctoral dissertation. University of Seville, Spain.
Gomez-Mestre I., Tejedo, M. (2004): Contrasting patterns of quantitative and neutral genetic variation in locally adapted populations of the natterjack toad Bufo calamita. Evolution. 58: 2343-2352.
Goudet, J. (2001): FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available at: http://www.unil.ch/izea/softwares/fstat-html.
Harper, J. (1977): Population biology of plants. Academic Press, New York, USA.
Hewitt, G.M. (1996): Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linn. Soc. 58: 247-276.
Jensen, J.L., Bohonak, A.J., Kelley, S.T. (2005): Isolation by distance, web service. BMC Genetics 6:13.
Kennington, W. J., Gockel, J., Partridge, L. (2002). Testing for asymmetrical gene flow in a Drosophila melanogaster body-size cline. Genetics. 165: 667-673.
Leblois, R., Rousset, F., Tikel, D., Moritz, C. (2000). Absence of evidence for isolation by distance in an expanding cane toad (Bufo marinus) population: an individual-based analysis of microsatellite genotypes. Mol. Ecol. 9: 1905-1909.
Lee, H.J., Broggi, J., Sánchez-Montes, G., Díaz-Paniagua, C., Gomez-Mestre, I. (2020): Dwarfism in close continental amphibian populations despite lack of genetic isolation. Oikos. 129: 1243-1256.
Lenormand, T. (2002): Gene flow and the limits to natural selection. Trends Ecol. Evol. 17: 183-189.
Lindsey, C.C. (1966): Body sizes of poikilotherm vertebrates at different latitudes. Evolution. 20: 456-465.
López-Martínez, N. (1989): Tendencias en paleobiogeografia. El futuro de la biogeografía del pasado. In: Paleontologia, pp. 271-296. Aguirre, E., Coord, C.S.I.C., Madrid, Spain.
Marangoni, F. 2006. Variación clinal en el tamaño del cuerpo a escala microgeográfica en dos especies de anuros (Pelobates cultripes y Bufo calamita). Unpublished doctoral dissertation. University of Seville, Spain.
Marangoni, F., Tejedo, M. (2008): Variation in body size and metamorphic traits of Iberian spadefoot toads over a short geographic distance. J. Zool. 275: 97-105.
Marangoni, F., Tejedo, M., Cogălniceanu, D. (2021): Can age and growth patterns explain the geographical variation in the body size of two toad species? An. Acad. Bras. Cienc. (2021) 93(2): e20190470.
Marangoni, F., Tejedo, M., Gomez-Mestre, I. (2008): Extreme reduction in body size and reproductive output associated with sandy substrates in two anuran species. Amphibia-Reptilia. 29: 541-553.
Mayr, E. (1963): Animal Species and Evolution. Harvard University Press. Cambridge, UK.
Mousseau, T.E., Fox, C.W. (1998). Maternal effects as adaptations. Oxford University Press, New York.
Postma, E., Noordwijk van, A.J. (2005): Gene flow a large genetic difference in clutch size at a small spatial scale. Nature. 433: 65-68.
Räsänen, K., Laurila, A., Merilä, J. (2003): Geographic variation in acid stress tolerance of the moor frog, Rana arvalis. II. Adaptive maternal effects. Evolution. 57: 363-371.
Räsänen, K., Laurila, A., Merilä, J. (2005): Maternal investment in egg size: environment- and population-specific effects on offspring performance. Oecologia. 142: 546-553.
Ray, C. (1960): The application of Bergmann's and Allen's rules to the poikilotherms. J. Morphol. 106: 85-108.
Raymond, M., Rousset, F. (1995): GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Heredity. 86: 248-249
Rousset, F. (1997): Genetic Differentiation and estimation on gene flow from F-statistics under isolation by distance. Genetics. 145: 1219-1228.
Rowe, G.T., Beebee, T.J.C, Burke, T. (1997): PCR primers for polymorphic microsatellite loci in the anuran amphibian Bufo calamita. Mol. Ecol. 6: 401-402.
Rowe, G.T., Beebee, T.J.C, Burke, T. (1998): Phylogeography of the natterjack toad Bufo calamita in Britain: genetic differentiation of native and translocated populations. Mol. Ecol. 7: 751-760.
Schmalhausen, I. (1949): Factor of evolution: The theory of stabilizing selection. Philadelphia: Blakiston.
Schneider, S., Roessli, D., Excoffier, L. (2000): Arlequin: a software for population genetics data analysis. Ver. 2.000. Genetics and Biometry Lab, Dept. of Anthropology, University of Geneva, Geneva, Switzerland.
Sinsch, U., Marangoni, F., Oromi, N., Leskovar, C., Sanuy, D., Tejedo, M. (2010): Proximate mechanisms determining size variability in natterjack toads. J. Zool. 281: 272-281.
Skelly, D.K. (2004): Microgeographic countergradient variation in the wood frog, Rana sylvatica. Evolution. 58: 160-165.
Slatkin, M. (1985): Gene flow in natural populations. Annu. Rev. Ecol. Syst. 16: 393-430.
Slatkin, M. (1987): Gene flow and the geographic structure of natural populations. Science. 236: 787-792.
Slatkin, M. (1995): A measure of population subdivision based on microsatellite allele frequencies. Genetics. 139: 457-462.
Sokal, R.R., Rohlf, F.J. (1995): Biometry. W. H. Freeman & Company. New York.
Stearns, S.C. (1989): The evolutionary significance of phenotypic plasticity. BioScience. 39: 436-445.
Stebbins, G.L. (1950): Variation and Evolution in Plants. Columbia University Press. New York.
Taberlet, P., Fumagalli, L., Wust-Scaucy, A.G., Cosson, J.F. (1998): Comparative phylogeography and postglacial colonisation routes in Europe. Mol. Ecol. 7: 453-464.
Via, S., Lande, R. (1985): Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution. 39: 505-523.
Weir, B.S., Cockerham, C.C. (1984): Estimating F-statistics for the analysis of populations structure. Evolution. 38: 358-1370.
Wright, S. (1951): The genetical structure of populations. Ann. Eugenic. 15: 323-354.