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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Schmalhausen, I. I. Factors of Evolution: the Theory of Stabilizing Selection (Blakiston, Philadelphia, 1949).
deBeer, G. R. Embryos and Ancestors 3rd edn (Clarendon Press, Oxford, 1958).
Gould, S. J. & Eldredge, N. Punctuated equilibria: the tempo and mode of evolution reconsidered. Paleobiology 3, 115–151 (1977).
Raff, R. A. The Shape of Life; Genes, Development and the Evolution of Animal Form (Chicago Univ. Press, Chicago, 1996).
Alberch, P., Gould, S. J., Oster, G. F. & Wake, D. B. Size and shape in ontogeny and phylogeny. Paleobiology 5, 296–317 (1979).
Gould, S. J. Ontogeny and Phylogeny (Harvard Univ. Press, Cambridge, 1977).
Sanger, T. J. et al. Convergent evolution of sexual dimorphism in skull shape using distinct developmental strategies. Evolution 67, 2180–2193 (2013).
Zelditch, M. L., Sheets, H. D. & Fink, W. L. The ontogenetic dynamics of shape disparity. Paleobiology 29, 139–156 (2003).
Adams, D. C. & Nistri, A. Ontogenetic convergence and evolution of foot morphology in European cave salamanders (family: Plethodontidae). BMC Evol. Biol. 10, 216 (2010).
Raff, R. A. Origins of the other metazoan body plans: the evolution of larval forms. Phil. Trans. R. Soc. B 363, 1473–1479 (2008).
Moran, N. A. Adaptation and constraint in the complex life cycles of animals. Annu. Rev. Ecol. Syst. 25, 573–600 (1994).
Ebenman, B. Evolution in organisms that change their niches during the life cycle. Am. Nat. 139, 990–1021 (1992).
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).
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).
Johansson, F. Trait performance correlations across life stages under environmental stress conditions in the common frog, Rana temporaria. PLoS ONE 5, e11680 (2010).
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).
Phillips, P. C. Genetic constraints at the metamorphic boundary: morphological development in the wood frog, Rana sylvatica. J. Evol. Biol. 11, 453–463 (1998).
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).
Wilson, A. D. M. & Krause, J. Personality and metamorphosis: is behavioral variation consistent across ontogenetic niche shifts? Behav. Ecol. 23, 1316–1323 (2012).
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).
Crean, A. J., Monro, K. & Marshall, D. J. Fitness consequences of larval traits persist across the metamorphic boundary. Evolution 65, 3079–3089 (2011).
Wray, G. A. The evolution of larval morphology during the post-Paleozoic radiation of echinoids. Paleobiology 18, 258–287 (1992).
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).
Katz, H. R. & Hale, M. E. A large-scale pattern of ontogenetic shape change in ray-finned fishes. PLoS ONE 11, e0150841 (2016).
Strathmann, R. R. & Eernisse, D. J. What molecular phylogenies tell us about the evolution of larval forms. Am. Zool. 34, 502–512 (1994).
Wollenberg Valero, K. C. et al. Transcriptomic and macroevolutionary evidence for phenotypic uncoupling between frog life history phases. Nat. Commun. 8, 15213 (2017).
van Buskirk, J. Getting in shape: adaptation and phylogenetic inertia in morphology of Australian anuran larvae. J. Evol. Biol. 22, 1326–1337 (2009).
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).
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).
Roelants, K., Haas, A. & Bossuyt, F. Anuran radiations and the evolution of tadpole morphospace. Proc. Natl Acad. Sci. USA 108, 8731–8736 (2011).
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).
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).
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).
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).
Haas, A. Phylogeny of frogs as inferred from primarily larval characters (Amphibia: Anura). Cladistics 19, 23–89 (2003).
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).
Altig, R. & Johnston, G. F. Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats. Herpetol. Monogr. 3, 81–109 (1989).
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).
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).
Hetherington, A. J. et al. Do cladistic and morphometric data capture common patterns of morphological disparity? Palaeontology 58, 393–399 (2015).
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).
Anderson, P. S. & Friedman, M. Using cladistic characters to predict functional variety: experiments using early gnathostomes. J. Vertebr. Paleontol. 32, 1254–1270 (2012).
Callebaut, W. & Rasskin-Gutman, D. Modularity: Understanding the Development and Evolution of Natural Complex Systems (MIT press, Cambridge, 2005).
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).
Callery, E. M., Fang, H. & Elinson, R. P. Frogs without polliwogs: evolution of anuran direct development. BioEssays 23, 233–241 (2001).
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).
Wray, G. A. & Raff, R. A. The evolution of developmental strategy in marine invertebrates. Trends Ecol. Evol. 6, 45–50 (1991).
Hanken, J. in The Origin and Evolution of Larval Forms 61–108 (Academic Press, 1999).
Hanken, J. Life history and morphological evolution. J. Evol. Biol. 5, 549–557 (1992).
Pyron, R. A. Biogeographic analysis reveals ancient continental vicariance and recent oceanic dispersal in amphibians. Syst. Biol. 63, 779–797 (2014).
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2016); http://www.R-project.org/
Anstis, M. Tadpoles and Frogs of Australia (New Holland Publishers, Chatswood, New South Wales, 2013).
Rohlf, F. J. tpsDig v.2.26 (Stony Brook, New York, USA, 2016); http://life.bio.sunysb.edu/ee/rohlf/software.html
Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).
Rohlf, F. J. & Slice, D. Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst. Zool. 39, 40–59 (1990).
geomorph: geometric morphometric analyses of 2D/3D landmark data. R package v.3.0.2 (2016); https://cran.r-project.org/package=geomorph
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).
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).
Klingenberg, C. P. Size, shape, and form: concepts of allometry in geometric morphometrics. Dev. Genes Evol. 226, 113–137 (2016).
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).
Adams, D. C. A method for assessing phylogenetic least squares models for shape and other high-dimensional multivariate data. Evolution 68, 2675–2688 (2014).
vegan: community ecology package. R package v.2.4-0 (2016); https://cran.r-project.org/package=vegan
Sidlauskas, B. Continuous and arrested morphological diversification in sister clades of characiform fishes: a phylomorphospace approach. Evolution 62, 3135–3156 (2008).
cluster: cluster analysis basics and extensions. R package v.2.0.4 (2016); https://cran.r-project.org/package=cluster
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).
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.
The authors declare no competing financial interests.
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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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