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Within-Population Developmental and Morphological Plasticity is Mirrored in Between-Population Differences: Linking Plasticity and Diversity

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Abstract

It has been suggested that phenotypic plasticity can facilitate evolutionary diversification of organisms. If life-history and morphological diversification across a lineage is mirrored in diversification in the same traits due to phenotypic plasticity within a lineage it fulfils one of the expectations that are needed to support this diversification hypothesis. We carried out a laboratory study to examine development rate and morphology between and within populations of the parsley frog, Pelodytes punctatus. We found that frogs reared in the laboratory had a longer development time, relatively longer hind legs and relatively narrower heads under constant water level compared to those under decreasing water level simulating pool drying. This adaptive phenotypic plasticity response to pool drying was mirrored across populations because frogs from permanent waters had longer development times, relatively longer hind legs and relatively narrower heads compared to frogs from temporary waters. Hence the developmental and morphological plasticity observed within populations was also observed between populations as constitutive expressed traits. We suggest that the morphology pattern observed was driven by a common developmental process (time to metamorphosis), indicating that plasticity may contribute to evolutionary change, ultimately resulting in genetic accommodation of the morphological traits.

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References

  • Abramoff, M. D., Magelhaes, P. J., & Ram, S. J. (2004). Image processing with ImageJ. Biophotonics International, 11, 36–42.

    Google Scholar 

  • Agrawal, A. A. (2001). Phenotypic plasticity in the interactions and evolution of species. Science, 294, 321–326.

    Article  PubMed  CAS  Google Scholar 

  • Altwegg, R., & Reyer, H. U. (2003). Patterns of natural selection on size at metamorphosis in water frogs. Evolution, 57, 872–882.

    PubMed  Google Scholar 

  • Badyaev, A. V. (2009). Evolutionary significance of phenotypic accommodation in novel environments: an empirical test of the Baldwin effect. Philosophical Transactions of the Royal Society B: Biological Sciences, 364, 1124–1141.

    Google Scholar 

  • Blem, C. R., Steiner, J. W., & Miller, M. A. (1978). Comparison of jumping abilities of the cricket frogs Acris gryllus and Acris crepitans. Herpetologica, 34, 288–291.

    Google Scholar 

  • Blouin, M. S., & Brown, T. S. (2000). Effects of temperature-induced variation in anuran larval growth rate on head width and leg length at metamorphosis. Oecologia, 125, 358–361.

    Article  Google Scholar 

  • Blouin, M. S., & Loeb, L. G. (1991). Effects of environmentally induced development-rate variation on head and limb morphology in the green tree frog, Hyla cinerea. American Naturalist, 138, 717–728.

    Article  Google Scholar 

  • Boersma, M., Spaak, P., & De Meester, L. (1998). Predator-mediated plasticity in morphology, life history, and behavior of Daphnia: the uncoupling of responses. American Naturalist, 152, 237–248.

    Article  PubMed  CAS  Google Scholar 

  • Conover, D. O., & Heins, S. W. (1987). Adaptive variation in environmental and genetic sex determination in a fish. Nature, 326, 496–498.

    Article  PubMed  CAS  Google Scholar 

  • Crawley, M. J. (2002). Statistical computing: An introduction to data analysis using S-plus. Chichester, UK: Wiley.

    Google Scholar 

  • Denver, R. J., Mirhadi, N., & Phillips, M. (1998). Adaptive plasticity in amphibian metamorphosis: response of Scaphiopus hammondii tadpoles to habitat desiccation. Ecology, 79, 1859–1872.

    Google Scholar 

  • Emerson, S. B. (1985). Skull shape in frogs – correlations with diet. Herpetologia, 41, 177–188.

    Google Scholar 

  • Ghalambor, C. K., Mckay, J. K., Carroll, S. P., & Reznick, D. N. (2007). Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology, 21, 394–407.

    Article  Google Scholar 

  • Gomez-Mestre, I., & Buchholz, D. R. (2006). Developmetal plasticity mirrors differences among taxa in spadefoot toads linking plasticity and diversity. Proceedings of the National Academy of Sciences of the United States of America, 103, 19021–19026.

    Article  PubMed  CAS  Google Scholar 

  • Gomez-Mestre, I., Saccoccio, V. L., Iijima, T., Collins, E. M., Rosenthal, G. G., & Warkentin, K. M. (2010). The shape of things to come: linking developmental plasticity to postmetamorphic morphology in anurans. Journal of Evolutionary Biology, 23, 1364–1373.

    Article  PubMed  CAS  Google Scholar 

  • Gosner, K. L. (1960). A simple table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16, 183–190.

    Google Scholar 

  • Guyétant, R., Temmermans, W., & Avrillier, J. N. (1999). Phénologie de la reproduction chez Pelodytes punctatus Daudin, 1802 (Amphibia, Anura). Amphibia-Reptilia, 20, 149–160.

    Google Scholar 

  • Hallatschek, O., & Nelson, D. R. (2008). Gene surfing in expanding populations. Theoretical Population Biology, 73, 158–170.

    Article  PubMed  Google Scholar 

  • Johansson, F., Lind, M. I., & Lederer, B. (2010). Trait performance correlations across life stages under environmental stress conditions in the common frog, Rana temporaria. PLoS One, 5(7), e11680.

    Article  PubMed  Google Scholar 

  • Jourdan-Pileau, H., David, P., & Crochet, P.-A. (2012). Phenotypic plasticity allows the Mediterranean parsley frog Pelodytes punctatus to exploit two temporal niches under continuous gene flow. Molecular Ecology, 21, 876–886.

    Article  Google Scholar 

  • Kondrashov, A. S. (2003). Accumulation of Dobzhansky-Muller incompatibilities within a spatially structured population. Evolution, 52, 151–153.

    Google Scholar 

  • Laugen, A. T., Kruuk, L. E. B., Laurila, A., Räsänen, K., Stone, J., & Merilä, J. (2005). Quantitative genetics of larval life-history traits in Rana temporaria in different environmental conditions. Genetical Research, 86, 161–170.

    Article  PubMed  CAS  Google Scholar 

  • Ledon-Retting, C. C., Pfennig, D. W., & Nascone-Yoder, N. (2008). Ancestral variation and the potential for genetic accommodation in larval amphibians: implications for the evolution of novel feeding strategies. Evolution & Development, 10, 316–325.

    Article  Google Scholar 

  • Lind, M. I., Ingvarsson, P. K., Johansson, H., Hall, D., & Johansson, F. (2011). Gene flow and selection on phenotypic plasticity in an island system of Rana temporaria. Evolution, 65, 684–697.

    Article  PubMed  Google Scholar 

  • Lind, M., & Johansson, F. (2007). The degree of adaptive phenotypic plasticity is correlated with spatial environmental heterogeneity experienced by island populations of Rana temporaria. Journal of Evolutionary Biology, 20, 1288–1297.

    Article  PubMed  CAS  Google Scholar 

  • Losos, J., et al. (1999). Evolutionary implications of phenotypic plasticity in the hindlimb of the lizard Anolis sagrei. Evolution, 54, 301–305.

    Google Scholar 

  • Mantel, N. (1967). The detection of disease of clustering and a generalized regression approach. Cancer Research, 27, 209–220.

    PubMed  CAS  Google Scholar 

  • Moczek, A. P., Sultan, S., Foster, S., Ledon-Rettig, C., Dworkin, I., Nijhout, H. F., et al. (2011). The role of developmental plasticity in evolutionary innovation. Proceedings of the Royal Society of London. Series B: Biological Sciences, 278, 2705–2713.

    Article  PubMed  Google Scholar 

  • Morey, S. R., & Reznick, D. N. (2004). The relationship between habitat permanence and larval development in California spadefoot toads: field and laboratory comparisons of developmental plasticity. Oikos, 104, 172–190.

    Article  Google Scholar 

  • Nauwelaerts, S., Ramsay, J., & Aerts, P. (2007). Morphological correlates of aquatic and terrestrial locomotion in a semi-aquatic frog, Rana esculenta: no evidence for a design conflict. Journal of Anatomy, 210, 304–317.

    Article  PubMed  Google Scholar 

  • Newman, R. A. (1992). Adaptive plasticity in amphibian metamorphosis. BioScience, 42, 671–678.

    Article  Google Scholar 

  • Nöllert, A., & Nöllert, C. (1992). Die Amphibien Europas. Stuttgart: Franckh-Kosmos.

    Google Scholar 

  • Nosil, P., Egan, S. P., Funk, D. J., & Hoekstra, H. (2007). Heterogeneous genomic differentiation between walking-stick ecotypes: “Isolation by Adaptation” and multiple roles for divergent selection. Evolution, 62, 316–336.

    Article  PubMed  Google Scholar 

  • Nosil, P., Vines, T., & Funk, D. J. (2005). Perspective: Reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution, 59, 705–719.

    PubMed  Google Scholar 

  • Oksanen, J., Kindt, R., Legendre, P., O’Hara, B., Simpson, G. L., Solymos, P., et al. (2009). Community Ecology Package, version 1.15-3. http://vegan.r-forge.r-project.org/.

  • Orizaola, G., & Laurila, A. (2009). Microgeographic variation in temperature-induced plasticity in an isolated amphibian metapopulation. Evolutionary Ecology, 26, 979–991.

    Article  Google Scholar 

  • Pfennig, D., Wund, M. A., Snell-Rood, E. C., Cruickshank, T., Schlichting, C. D., & Moczek, A. P. (2010). Phenotypic plasticity’s impacts on diversification and speciation. Trends in Ecology & Evolution, 25, 459–467.

    Article  Google Scholar 

  • Pinheiro, J., Bates, D.,DebRoy, S., Sarkar, D. & R. C. team. (2008). nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-90.

  • Price, T. D., Qvarnström, A., & Erwin, D. E. (2003). The role of phenotypic plasticity in driving genetic evolution. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270, 1433–1440.

    Article  PubMed  Google Scholar 

  • Queitsch, C., Sangster, T. A., & Lindquist, S. (2002). Hsp90 as a capacitor of phenotypic variation. Nature, 417, 618–624.

    Article  PubMed  CAS  Google Scholar 

  • Relyea, R. A. (2002). Local population differences in phenotypic plasticity: Predator-induced changes in wood frog tadpoles. Ecological Monographs, 72, 77–93.

    Article  Google Scholar 

  • Richter-Boix, A., Llorente, G. A., & Montori, A. (2006a). Effects of phenotypic plasticity on post-metamorphic traits during pre-metamorphic stages in the anuran Pelodytes punctatus. Evolutionary Ecology Research, 8, 309–320.

    Google Scholar 

  • Richter-Boix, A., Llorente, G. A., & Montori, A. (2006b). A comparative analysis of the adaptive developmental plasticity hypothesis in six Mediterranean anuran species along a pond permanency gradient. Evolutionary Ecology Research, 8, 1139–1154.

    Google Scholar 

  • Richter-Boix, A., Llorente, G. A., & Montori, A. (2007). Structure and dynamics of an amphibian metacommunity in two regions. Journal of Animal Ecology, 76, 607–618.

    Article  PubMed  Google Scholar 

  • Richter-Boix, A., Tejedo, M., & Rezende, E. (2011). Evolution and plasticity of anuran larval development in response to desiccation: a comparative analysis. Ecology and Evolution, 1, 15–25.

    Article  PubMed  Google Scholar 

  • Richter-Boix, A., Teplitsky, C., Rogell, B., & Laurila, A. (2010). Local selection modifies phenotypic divergence among Rana temporaria populations in the presence of gene flow. Molecular Ecology, 19, 716–731.

    Article  PubMed  Google Scholar 

  • Sánchez-Herráiz, M. J., Barbadillo, L. J., Machordom, A., & Sanchiz, B. (2000). A new species of Pelodytid frog from the Iberian Peninsula. Herpetologica, 56, 105–118.

    Google Scholar 

  • Suzuki, Y., & Nijhout, H. F. (2006). Evolution of polyphenism by genetic accommodation. Science, 311, 650–652.

    Article  PubMed  CAS  Google Scholar 

  • Tejedo, M., Marangoni, F., Pertoldi, C., Richter-Boix, A., Laurila, A., Orizaola, G., et al. (2010). Contrasting effects of environmental factors during larval stage on morphological plasticity in post-metamorphic frogs. Climate Research, 43, 31–39.

    Article  Google Scholar 

  • Vasemägi, A. (2006). The adaptive hypothesis of clinal variation revisited: Single-locus clines as a result of spatially restricted gene flow. Genetics, 173, 2411–2414.

    Article  PubMed  Google Scholar 

  • Waddington, C. H. (1953). Genetic assimilation of an acquired character. Evolution, 7, 118–126.

    Article  Google Scholar 

  • West, B., Welch, K. B., & Galecki, A. T. (2006). Linear mixed models: A practical guide using statistical software. Boca Raton: Chapman & Hall/CRC.

    Google Scholar 

  • West-Eberhard, M. J. (2005). Developmental plasticity and the origin of species differences. Proceedings of the National Academy of Sciences of the United States of America, 102, 6543–6549.

    Article  PubMed  CAS  Google Scholar 

  • Wilbur, H. M. (1987). Regulation of structure in complex systems: Experimental temporal pond communities. Ecology, 60, 1432–1437.

    Google Scholar 

  • Zuur, A. F., Leno, E. N., Walker, N. J., Saveliev, A. A., & Smith, G. M. (2009). Mixed effects models and extensions in ecology with R. New York, USA: Springer.

    Book  Google Scholar 

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Acknowledgments

We thank Anssi Laurila and German Orizaola for helpful comments on earlier drafts of the article. The research was funded by the Swedish Research Council to FJ. ARB was supported by a Spanish Ministry of Education and Culture postdoctoral grant (MEC2007-0944) and by a Beatriu de Pinós postdoctoral fellowship (2008 BP A 00032).

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  1. Department of Ecology and Genetics, Uppsala University, Uppsala, Sweden

    Frank Johansson & Alex Richter-Boix

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  1. Frank Johansson
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Correspondence to Frank Johansson.

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Johansson, F., Richter-Boix, A. Within-Population Developmental and Morphological Plasticity is Mirrored in Between-Population Differences: Linking Plasticity and Diversity. Evol Biol 40, 494–503 (2013). https://doi.org/10.1007/s11692-013-9225-8

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