Adult frogs and tadpoles have different macroevolutionary patterns across the Australian continent

Abstract

Developmental changes through an animal’s life are generally understood to contribute to the resulting adult morphology. Possible exceptions are species with complex life cycles, where individuals pass through distinct ecological and morphological life stages during their ontogeny, ending with metamorphosis to the adult form. Antagonistic selection is expected to drive low genetic correlations between life stages, theoretically permitting stages to evolve independently. Here we describe, using Australian frog radiation, the evolutionary consequences on morphological evolution when life stages are under different selective pressures. We use morphometrics to characterize body shape of tadpoles and adults across 166 species of frog and investigate similarities in the two resulting morphological spaces (morphospaces) to test for concerted evolution across metamorphosis in trait variation during speciation. A clear pattern emerges: Australian frogs and their tadpoles are evolving independently; their markedly different morphospaces and contrasting estimated evolutionary histories of body shape diversification indicate that different processes are driving morphological diversification at each stage. Tadpole morphospace is characterized by rampant homoplasy, convergent evolution and high lineage density. By contrast, the adult morphospace shows greater phylogenetic signal, low lineage density and divergent evolution between the main clades. Our results provide insight into the macroevolutionary consequences of a biphasic life cycle.

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Fig. 1: Morphometric variables characterizing body shape in tadpoles and adult frogs.
Fig. 2: Evolutionary phylomorphospaces of tadpoles and adult frogs.

References

  1. 1.

    Schmalhausen, I. I. Factors of Evolution: the Theory of Stabilizing Selection (Blakiston, Philadelphia, 1949).

    Google Scholar 

  2. 2.

    deBeer, G. R. Embryos and Ancestors 3rd edn (Clarendon Press, Oxford, 1958).

    Google Scholar 

  3. 3.

    Gould, S. J. & Eldredge, N. Punctuated equilibria: the tempo and mode of evolution reconsidered. Paleobiology 3, 115–151 (1977).

    Article  Google Scholar 

  4. 4.

    Raff, R. A. The Shape of Life; Genes, Development and the Evolution of Animal Form (Chicago Univ. Press, Chicago, 1996).

    Google Scholar 

  5. 5.

    Alberch, P., Gould, S. J., Oster, G. F. & Wake, D. B. Size and shape in ontogeny and phylogeny. Paleobiology 5, 296–317 (1979).

    Article  Google Scholar 

  6. 6.

    Gould, S. J. Ontogeny and Phylogeny (Harvard Univ. Press, Cambridge, 1977).

    Google Scholar 

  7. 7.

    Sanger, T. J. et al. Convergent evolution of sexual dimorphism in skull shape using distinct developmental strategies. Evolution 67, 2180–2193 (2013).

    Article  PubMed  Google Scholar 

  8. 8.

    Zelditch, M. L., Sheets, H. D. & Fink, W. L. The ontogenetic dynamics of shape disparity. Paleobiology 29, 139–156 (2003).

    Article  Google Scholar 

  9. 9.

    Adams, D. C. & Nistri, A. Ontogenetic convergence and evolution of foot morphology in European cave salamanders (family: Plethodontidae). BMC Evol. Biol. 10, 216 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Raff, R. A. Origins of the other metazoan body plans: the evolution of larval forms. Phil. Trans. R. Soc. B 363, 1473–1479 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Moran, N. A. Adaptation and constraint in the complex life cycles of animals. Annu. Rev. Ecol. Syst. 25, 573–600 (1994).

    Article  Google Scholar 

  12. 12.

    Ebenman, B. Evolution in organisms that change their niches during the life cycle. Am. Nat. 139, 990–1021 (1992).

    Article  Google Scholar 

  13. 13.

    Aguirre, J. D., Blows, M. W. & Marshall, D. J. The genetic covariance between life cycle stages separated by metamorphosis. Proc. R. Soc. B 281, 20141091 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Blouin, M. S. Genetic correlations among morphometric traits and rates of growth and differentiation in the green tree trog, Hyla cinerea. Evolution 46, 735–744 (1992).

    Article  PubMed  Google Scholar 

  15. 15.

    Johansson, F. Trait performance correlations across life stages under environmental stress conditions in the common frog, Rana temporaria. PLoS ONE 5, e11680 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. 16.

    Anderson, B. B., Scott, A. & Dukas, R. Social behavior and activity are decoupled in larval and adult fruit flies. Behav. Ecol. 27, 820–828 (2016).

    Article  Google Scholar 

  17. 17.

    Phillips, P. C. Genetic constraints at the metamorphic boundary: morphological development in the wood frog, Rana sylvatica. J. Evol. Biol. 11, 453–463 (1998).

    Article  Google Scholar 

  18. 18.

    Watkins, T. B. 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 (2001).

    Article  PubMed  CAS  Google Scholar 

  19. 19.

    Wilson, A. D. M. & Krause, J. Personality and metamorphosis: is behavioral variation consistent across ontogenetic niche shifts? Behav. Ecol. 23, 1316–1323 (2012).

    Article  Google Scholar 

  20. 20.

    Parichy, D. M. Experimental analysis of character coupling across a complex life cycle: pigment pattern metamorphosis in the tiger salamander, Ambystoma tigrinum tigrinum. J. Morphol. 237, 53–67 (1998).

    Article  PubMed  CAS  Google Scholar 

  21. 21.

    Crean, A. J., Monro, K. & Marshall, D. J. Fitness consequences of larval traits persist across the metamorphic boundary. Evolution 65, 3079–3089 (2011).

    Article  PubMed  Google Scholar 

  22. 22.

    Wray, G. A. The evolution of larval morphology during the post-Paleozoic radiation of echinoids. Paleobiology 18, 258–287 (1992).

    Article  Google Scholar 

  23. 23.

    Smith, A. B. & Littlewood, D. T. J. Comparing patterns of evolution: larval and adult life history stages and ribosomal RNA of post-Palaeozoic. Phil. Trans. R. Soc. B 349, 11–18 (1995).

    Article  Google Scholar 

  24. 24.

    Katz, H. R. & Hale, M. E. A large-scale pattern of ontogenetic shape change in ray-finned fishes. PLoS ONE 11, e0150841 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. 25.

    Strathmann, R. R. & Eernisse, D. J. What molecular phylogenies tell us about the evolution of larval forms. Am. Zool. 34, 502–512 (1994).

    Article  Google Scholar 

  26. 26.

    Wollenberg Valero, K. C. et al. Transcriptomic and macroevolutionary evidence for phenotypic uncoupling between frog life history phases. Nat. Commun. 8, 15213 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. 27.

    van Buskirk, J. Getting in shape: adaptation and phylogenetic inertia in morphology of Australian anuran larvae. J. Evol. Biol. 22, 1326–1337 (2009).

    Article  PubMed  Google Scholar 

  28. 28.

    Arendt, J. Morphological correlates of sprint swimming speed in five species of spadefoot toad tadpoles: comparison of morphometric methods. J. Morphol. 271, 1044–1052 (2010).

    Article  PubMed  Google Scholar 

  29. 29.

    van Buskirk, J. A comparative test of the adaptive plasticity hypothesis: relationships between habitat and phenotype in anuran larvae. Am. Nat. 160, 87–102 (2002).

    Article  PubMed  Google Scholar 

  30. 30.

    Roelants, K., Haas, A. & Bossuyt, F. Anuran radiations and the evolution of tadpole morphospace. Proc. Natl Acad. Sci. USA 108, 8731–8736 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Vidal‐García, M. & Keogh, J. S. Convergent evolution across the Australian continent: ecotype diversification drives morphological convergence in two distantly related clades of Australian frogs. J. Evol. Biol. 28, 2136–2151 (2015).

    Article  PubMed  Google Scholar 

  32. 32.

    Moen, D. S., Irschick, D. J. & Wiens, J. J. Evolutionary conservatism and convergence both lead to striking similarity in ecology, morphology and performance across continents in frogs. Proc. R. Soc. B 280, 20132156 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Vidal‐García, M., Byrne, P., Roberts, J. & Keogh, J. S. The role of phylogeny and ecology in shaping morphology in 21 genera and 127 species of Australo‐Papuan myobatrachid frogs. J. Evol. Biol 27, 181–192 (2014).

    Article  PubMed  Google Scholar 

  34. 34.

    Moen, D. S., Morlon, H. & Wiens, J. J. Testing convergence versus history: convergence dominates phenotypic evolution for over 150 million years in frogs. Syst. Biol. 65, 146–160 (2016).

    Article  PubMed  Google Scholar 

  35. 35.

    Haas, A. Phylogeny of frogs as inferred from primarily larval characters (Amphibia: Anura). Cladistics 19, 23–89 (2003).

    Google Scholar 

  36. 36.

    Eterovick, P. C. et al. Lack of phylogenetic signal in the variation in anuran microhabitat use in southeastern Brazil. Evol. Ecol. 24, 1–24 (2010).

    Article  Google Scholar 

  37. 37.

    Altig, R. & Johnston, G. F. Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats. Herpetol. Monogr. 3, 81–109 (1989).

    Article  Google Scholar 

  38. 38.

    Gerber, S., Neige, P. & Eble, G. J. Combining ontogenetic and evolutionary scales of morphological disparity: a study of early Jurassic ammonites. Evol. Dev. 9, 472–482 (2007).

    Article  PubMed  Google Scholar 

  39. 39.

    Ivanović, A., Cvijanovic, M. & Kalezić, M. L. Ontogeny of body form and metamorphosis: insights from the crested newts. J. Zool. (Lond.) 283, 153–161 (2011).

    Article  Google Scholar 

  40. 40.

    Hetherington, A. J. et al. Do cladistic and morphometric data capture common patterns of morphological disparity? Palaeontology 58, 393–399 (2015).

    Article  Google Scholar 

  41. 41.

    Villier, L. & Eble, G. J. Assessing the robustness of disparity estimates: the impact of morphometric scheme, temporal scale, and taxonomic level in spatangoid echinoids. Paleobiology 30, 652–665 (2004).

    Article  Google Scholar 

  42. 42.

    Anderson, P. S. & Friedman, M. Using cladistic characters to predict functional variety: experiments using early gnathostomes. J. Vertebr. Paleontol. 32, 1254–1270 (2012).

    Article  Google Scholar 

  43. 43.

    Callebaut, W. & Rasskin-Gutman, D. Modularity: Understanding the Development and Evolution of Natural Complex Systems (MIT press, Cambridge, 2005).

    Google Scholar 

  44. 44.

    Eble, G. J. in Evolutionary Dynamics: Exploring the Interplay of Selection, Accident, Neutrality, and Function (eds Crutchfield, J.P. & Schuster, P.) 35–65 (Oxford Univ. Press, Oxford, 2003).

    Google Scholar 

  45. 45.

    Callery, E. M., Fang, H. & Elinson, R. P. Frogs without polliwogs: evolution of anuran direct development. BioEssays 23, 233–241 (2001).

    Article  PubMed  CAS  Google Scholar 

  46. 46.

    Wake, D. B. & Hanken, J. Direct development in the lungless salamanders: what are the consequences for developmental biology, evolution and phylogenesis? Int. J. Dev. Biol. 40, 859–869 (2004).

    Google Scholar 

  47. 47.

    Wray, G. A. & Raff, R. A. The evolution of developmental strategy in marine invertebrates. Trends Ecol. Evol. 6, 45–50 (1991).

    Article  PubMed  CAS  Google Scholar 

  48. 48.

    Hanken, J. in The Origin and Evolution of Larval Forms 61–108 (Academic Press, 1999).

  49. 49.

    Hanken, J. Life history and morphological evolution. J. Evol. Biol. 5, 549–557 (1992).

    Article  Google Scholar 

  50. 50.

    Pyron, R. A. Biogeographic analysis reveals ancient continental vicariance and recent oceanic dispersal in amphibians. Syst. Biol. 63, 779–797 (2014).

    Article  PubMed  Google Scholar 

  51. 51.

    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2016); http://www.R-project.org/

    Google Scholar 

  52. 52.

    Anstis, M. Tadpoles and Frogs of Australia (New Holland Publishers, Chatswood, New South Wales, 2013).

    Google Scholar 

  53. 53.

    Rohlf, F. J. tpsDig v.2.26 (Stony Brook, New York, USA, 2016); http://life.bio.sunysb.edu/ee/rohlf/software.html

    Google Scholar 

  54. 54.

    Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. 55.

    Rohlf, F. J. & Slice, D. Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst. Zool. 39, 40–59 (1990).

    Article  Google Scholar 

  56. 56.

    geomorph: geometric morphometric analyses of 2D/3D landmark data. R package v.3.0.2 (2016); https://cran.r-project.org/package=geomorph

    Article  Google Scholar 

  57. 57.

    Gunz, P., Mitterocker, P. & Bookstein, F. L. in Modern Morphometrics in Physical Anthropology (ed. Slice, D. E.) 73–98 (Kluwer Academic/Plenum Publishers, New York, 2005).

    Google Scholar 

  58. 58.

    Mosimann, J. E. Size allometry: size and shape variables with characterizations of the lognormal and generalized gamma distributions. J. Am. Stat. Assoc. 65, 930–945 (1970).

    Article  Google Scholar 

  59. 59.

    Klingenberg, C. P. Size, shape, and form: concepts of allometry in geometric morphometrics. Dev. Genes Evol. 226, 113–137 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  60. 60.

    Rosauer, D., Laffan, S. W., Crisp, M. D., Donnellan, S. C. & Cook, L. G. Phylogenetic endemism: a new approach for identifying geographical concentrations of evolutionary history. Mol. Ecol. 18, 4061–4072 (2009).

    Article  PubMed  Google Scholar 

  61. 61.

    Adams, D. C. A method for assessing phylogenetic least squares models for shape and other high-dimensional multivariate data. Evolution 68, 2675–2688 (2014).

    Article  PubMed  Google Scholar 

  62. 62.

    vegan: community ecology package. R package v.2.4-0 (2016); https://cran.r-project.org/package=vegan

  63. 63.

    Sidlauskas, B. Continuous and arrested morphological diversification in sister clades of characiform fishes: a phylomorphospace approach. Evolution 62, 3135–3156 (2008).

    Article  PubMed  Google Scholar 

  64. 64.

    cluster: cluster analysis basics and extensions. R package v.2.0.4 (2016); https://cran.r-project.org/package=cluster

  65. 65.

    Adams, D. C. A generalized K statistic for estimating phylogenetic signal from shape and other high-dimensional multivariate data. Syst. Biol. 63, 685–697 (2014).

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank T. J. Sanger for comments on the manuscript, and E. Walsh (http://www.negaleg.com/) for the beautiful adult frog drawings she produced for us and help with figure preparation. Funding came from the Australian Research Council DP150102403 to J.S.K.

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E.S. and J.S.K. conceived the study. E.S., M.A. and M.V.-G. collected the data. E.S. performed the analyses. E.S., J.S.K. and M.V.-G. wrote the paper. All authors read and approved the final manuscript.

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Correspondence to Emma Sherratt.

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Sherratt, E., Vidal-García, M., Anstis, M. et al. Adult frogs and tadpoles have different macroevolutionary patterns across the Australian continent. Nat Ecol Evol 1, 1385–1391 (2017). https://doi.org/10.1038/s41559-017-0268-6

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