Evolutionary Biology

, Volume 43, Issue 2, pp 242–256 | Cite as

Morphological Consequences of Developmental Plasticity in Rana temporaria are not Accommodated into Among-Population or Among-Species Variation

  • Frank Johansson
  • Alex Richter-Boix
  • Ivan Gomez-Mestre
Research Article

Abstract

Environmental induced developmental plasticity occurs in many organisms and it has been suggested to facilitate biological diversification. Here we use ranid frogs to examine whether morphological changes derived from adaptive developmental acceleration in response to pool drying within a species are mirrored by differences among populations and across species. Accelerated development in larval anurans under pool drying conditions is adaptive and often results in allometric changes in limb length and head shape. We examine the association between developmental rate and morphology within population, among populations in divergent environments, and among species inside the Ranidae frog family, combining experimental approaches with phylogenetic comparative analyses. We found that frogs reared under decreasing water conditions that simulated fast pool drying had a faster development rate compared to tadpoles reared on constant water conditions. This faster developmental rate resulted in different juvenile morphologies between the two pool drying conditions. The association between developmental rate and morphology found as a result of plasticity was not mirrored by differences among populations that differed in development, neither was it mirrored among species that differed in development rate. We conclude that morphological differences among populations and species were not driven by variation in developmental time per se. Instead, selective factors, presumably operating on locomotion and prey choice, seem to have had a stronger evolutionary effect on frog morphology than evolutionary divergences in developmental rate in the ranid populations and species studied.

Keywords

Development time Temporary pools Morphology Ranidae Tadpoles Phenotypic plasticity 

Notes

Acknowledgments

We thank J.J. Wiens for assistance in deriving the phylogeny used in this article from a previously published large-scale phylogeny. We also tank J. Cabot and M. Calvo for granting access to the herpetological collections at Estación Biológica de Doñana and Museo Nacional de Ciencias Naturales, respectively. FJ was supported by The Swedish Research Council.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11692_2015_9363_MOESM1_ESM.docx (260 kb)
Supplementary material 1 (DOCX 260 kb)

References

  1. Abramoff, M. D., Magelhaes, P. J., & Ram, S. J. (2004). Image Processing with ImageJ. Biophotonics International, 11, 36–42.Google Scholar
  2. APHA. (1985). Standard methods for the examination of water and wastewater (16th ed.). Washington, DC: American Public Health Association.Google Scholar
  3. Altwegg, R., & Reyer, H. U. (2003). Patterns of natural selection on size at metamorphosis in water frogs. Evolution, 57, 872–882.CrossRefPubMedGoogle Scholar
  4. Anderson, D. R., & Burnhamn, K. P. (2002). Avoiding pitfalls when using information-theoretic methods. The Journal of Wildlife Management, 66, 912–918.CrossRefGoogle Scholar
  5. Baskett, M. L., Weitz, J. S., & Levin, S. A. (2007). The evolution of dispersal in reserve networks. The American Naturalist, 170, 59–78.CrossRefPubMedGoogle Scholar
  6. Benjamini, Y., & Hochenberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, 57, 289–300.Google Scholar
  7. 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
  8. Braendle, C., & Flatt, T. (2006). A role for genetic accommodation in evolution? BioEssays, 28, 868–873.CrossRefPubMedGoogle Scholar
  9. Buchholz, D. R., & Hayes, T. B. (2002). Evolutionary patterns of diversity in spadefoot toad metamorphosis (Anura: Pelobatidae). Copeia, 2002, 180–189.CrossRefGoogle Scholar
  10. Carvajal-Rodríguez, A., de Uña-Álvarez, J., & Rolán-Álvarez, E. (2009). A new multitest correction (SGoF) that increases its statistical power when increasing the number of tests. BMC Bioinformatics, 10, 1–14.CrossRefGoogle Scholar
  11. Crispo, E. (2007). The Baldwin effect and genetic assimilation: Revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity. Evolution, 61, 2469–2479.CrossRefPubMedGoogle Scholar
  12. 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
  13. Draghi, J. A., & Whitlock, M. C. (2012). Phenotypic plasticity facilitates mutational variance, genetic variance, and evolvability along the major axis of environmental variation. Evolution, 66, 2891–2902.CrossRefPubMedGoogle Scholar
  14. Ebenman, B. (1992). Evolution in organisms that change their niches during the life-cycle. American Naturalist, 139, 990–1021.CrossRefGoogle Scholar
  15. Emerson, S. B. (1978). Allometry and jumping in frogs: Helping the twain to meet. Evolution, 32, 551–564.CrossRefGoogle Scholar
  16. Emerson, S. B. (1986). Heterochrony and frogs: The relationship of a life history trait to morphological form. American Naturalist, 127, 167–183.CrossRefGoogle Scholar
  17. Frost, D. R., Grant, T., Faivovich, J., Bain, R. H., Haas, A., et al. (2006). The amphibian tree of life. Bulletin of the American Museum of Natural History, 297, 1–370.CrossRefGoogle Scholar
  18. Fusco, G., & Minelli, A. (2010). Phenotypic plasticity in development and evolution: Facts and concepts. Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 547–556.CrossRefGoogle Scholar
  19. 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 USA, 103, 19021–19026.CrossRefGoogle Scholar
  20. Gomez-Mestre, I., & Jovani, R. (2013). A heuristic model on the role of plasticity in adaptive evolution: Plasticity increases adaptation, population viability and genetic variation. Proceedings of the Royal Society of London B, 280, 1869.CrossRefGoogle Scholar
  21. 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 post-metamorphic morphology in anurans. Journal of Evolutionary Biology, 23, 1364–1373.CrossRefPubMedGoogle Scholar
  22. Gosner, K. L. (1960). A simple table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16, 183–190.Google Scholar
  23. Hanken, J. (1992). Life history and morphological evolution. Journal of Evolutionary Biology, 5, 549–557.CrossRefGoogle Scholar
  24. Hoskin, C. (2010). Breeding behaviour of the Barred frog Mixophyes coggeri. Memoirs of the Queensland Museum—Nature, 55, 1–7.Google Scholar
  25. James, R., & Wilson, R. (2008). Explosive jumping: Extreme morphological and physiological specializations of Australian rocket frogs (Litoria nasuta). Physiological and Biochemical Zoology, 81, 176–185.CrossRefPubMedGoogle Scholar
  26. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Johansson, F., & Richter-Boix, A. (2013). Within-population developmental and morphological plasticity is mirrored in between- population differences: Linking plasticity and diversity. Evolutionary Biology, 40, 494–503.CrossRefGoogle Scholar
  28. Johansson, F., Veldhoen, N., Lind, M. I., & Helbing, C. (2013). Phenotypic plasticity in the hepatic transcriptome of the European common frog (Rana temporaria): The interplay between environmental induction and geographic lineage on developmental response. Molecular Ecology, 22, 5608–5623.CrossRefPubMedGoogle Scholar
  29. Kulkarni, S., Gomez-Mestre, I., Moskalik, C., Storz, B., & Buchholz, D. (2011). Evolutionary reduction of developmental plasticity in desert spadefoot toads. Journal of Evolutionary Biology, 24, 2445–2455.CrossRefPubMedGoogle Scholar
  30. Laugen, A. T., Kruuk, L. E., 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.CrossRefPubMedGoogle Scholar
  31. Laurila, A., & Kujasalo, J. (1999). Habitat duration, predation risk and phenotypic plasticity in common frog tadpoles. Journal of Animal Ecology, 68, 1123–1132.CrossRefGoogle Scholar
  32. Lewis, B., & Rohweder, D. (2005). Distribution, habitat, and conservation status of the Giant Barred Frog, Mixophyes iteratus in the Bungawalbin catchment, northeastern New South Wales. Pacific Conservation Biology, 11, 189–197.Google Scholar
  33. Lind, M. I., Ingvarsson, P. K., Johansson, H., Hall, D., & Johansson, F. (2011). Gene flow and selection on phenotypic plasticity in an island system. Evolution, 65, 684–697.CrossRefPubMedGoogle Scholar
  34. 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.CrossRefPubMedGoogle Scholar
  35. Minelli, A., Brena, C., Deflorian, G., Maruzzo, D., & Fusco, G. (2006). From embryo to adult—beyond the conventional periodization of arthropod development. Development genes and evolution, 216, 373–383.CrossRefPubMedGoogle Scholar
  36. 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 B B, 278, 2705–2713.CrossRefGoogle Scholar
  37. Moran, N. A. (1994). Adaptation and constraint in the complex life cycles of animals. Annual Review of Ecology and Systematics, 25, 73–600.CrossRefGoogle Scholar
  38. Newman, R. A. (1992). Adaptive plasticity in amphibian metamorphosis. BioScience, 42, 671–678.CrossRefGoogle Scholar
  39. Orme, D., Freckleton, R., Thomas, G., Petzoldt, T., Fritz, S., Isaac, N., et al. (2012). Caper: Comparative analyses of phylogeneticsand evolution in R. version 0.5. http://CRAN.R-project.org/package=caper.
  40. Pechenik, J. A. (1999). On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Marine Ecology Progress Series, 177(1), 269–297.CrossRefGoogle Scholar
  41. Pechenik, J. A. (2006). Larval experience and latent effects—metamorphosis in not a new beginning. Integrative and Comparative Biology, 46, 323–333.CrossRefPubMedGoogle Scholar
  42. 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 and Evolution, 25, 459–467.CrossRefPubMedGoogle Scholar
  43. Pigliucci, M. (2001). Phenotypic plasticity: Beyond nature and nurture. Baltimore and London: The John Hopkiss University Press.328 pp.Google Scholar
  44. 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.Google Scholar
  45. Pyron, R. A., & Wiens, J. J. (2011). A large-scale phylogeny of Amphibia including over 2,800 species, and a revised classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution, 61, 543–583.CrossRefPubMedGoogle Scholar
  46. Pyron, R. A., & Wiens, J. J. (2013). Large-scale phylogenetic analyses reveal the causes of high tropical amphibian diversity. Proceedings of the Royal Society of London B: Biological Sciences, 280(1770), 20131622.CrossRefGoogle Scholar
  47. Revell, L. J. (2010). phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217–223.CrossRefGoogle Scholar
  48. Richter-Boix, A., Llorente, G. A., & Montori, A. (2006). 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
  49. Richter-Boix, A., Tejedo, M., & Rezende, E. L. (2011). Evolution and plasticity of anuran larval development in response to desiccation. A comparative analysis. A comparative analysis. Ecol Evol., 1, 15–25.CrossRefPubMedGoogle Scholar
  50. Rose, C. S. (2005). Integrating ecology and developmental biology to explain the timing of frog metamorphosis. Trends in Ecology and Evolution, 20, 129–135.CrossRefPubMedGoogle Scholar
  51. Savage, R. M. (1961). The ecology and life history of the common frog. London: Sir Isac Pitman and Sons.Google Scholar
  52. Snell-Rood, E. C., Van Dyken, J. D., Cruickshank, T., Wade, M. J., & Moczek, A. P. (2010). Toward a population genetic framework of developmental evolution: The costs, limits, and consequences of phenotypic plasticity. BioEssays, 32, 71–81.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Stoks, R., & Córdoba-Aguilar, A. (2012). Evolutionary ecology of odonata: A complex life cycle perspective. Annual Review of Entomology, 57, 249–265.CrossRefPubMedGoogle Scholar
  54. Suzuki, Y., & Nijhout, H. F. (2006). Evolution of polyphenism by genetic accommodation. Science, 311, 650–652.CrossRefPubMedGoogle Scholar
  55. 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.CrossRefGoogle Scholar
  56. Tejedo, M., & Reques, R. (1994). Plasticity in metamorphic traits of natterjack tadpoles: The interactive effects of density and pond duration. Oikos, 71, 295–304.CrossRefGoogle Scholar
  57. Vidal-García, M., Byrne, P. G., Roberts, J. D., & Keogh, J. S. (2014). The role of phylogeny and ecology in shaping morphology in 21 genera and 127 species of Australo-Papuan myobatrachid frogs. Journal of evolutionary biology, 27, 181–192.CrossRefPubMedGoogle Scholar
  58. Waddington, C. H. (1942). Canalization of development and the inheritance of acquired characters. Nature, 150, 563–565.CrossRefGoogle Scholar
  59. Waddington, C. H. (1952). Selection of the genetic basis for an acquired character. Nature, 169, 278.CrossRefPubMedGoogle Scholar
  60. Watkins, T. B. (2001). A quantitative genetic test of adaptive decoupling across metamorphosis for locomotor and life-history traits in the pacific tree frog, Hyla regilla. Evolution, 55, 1668–1677.CrossRefPubMedGoogle Scholar
  61. West-Eberhard, M. J. (2003). Developmental plasticity and evolution (p. 794). New York: Oxford University Press.Google Scholar
  62. West-Eberhard, M. J. (2005). Developmental plasticity and the origin of species differences. Proceedings of the National Academy of Sciences USA, 102, 6543–6549.CrossRefGoogle Scholar
  63. Wilbur, H. M., & Colins, J. P. (1973). Ecological aspects of amphibian metamorphosis. Science, 182, 1305–1314.CrossRefPubMedGoogle Scholar
  64. Wilson, A. D. M., & Krause, J. (2012). Personality and metamorphosis: Is behavioral variation consistent across ontogenetic niche shifts? Behavioral Ecology, 23, 1316–1323.CrossRefGoogle Scholar
  65. Wund, M. A., Baker, J. A., Clancy, B., Golub, J., & Fosterk, S. A. (2008). A test of the “Flexible stem” model of evolution: Ancestral plasticity, genetic accommodation, and morphological divergence in the threespine stickleback radiation. The American Naturalist, 172, 449–462.CrossRefPubMedGoogle Scholar
  66. Zeng, C., Gomez-Mestre, I., & Wiens, J. J. (2014). Evolution of rapid development in spadefoot toads is unrelated to arid environments. PLoS One, 9, e96673.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Frank Johansson
    • 1
  • Alex Richter-Boix
    • 1
  • Ivan Gomez-Mestre
    • 2
  1. 1.Department of Ecology and Genetics, Evolutionary Biology CentreUppsala UniversityUppsalaSweden
  2. 2.Ecology, Evolution, and Development GroupDoñana Biological Station (CSIC)SevilleSpain

Personalised recommendations