Abstract
Anuran amphibians undergo major morphological transitions during development, but the contribution of their markedly different life-history phases to macroevolution has rarely been analysed. Here we generate testable predictions for coupling versus uncoupling of phenotypic evolution of tadpole and adult life-history phases, and for the underlying expression of genes related to morphological feature formation. We test these predictions by combining evidence from gene expression in two distantly related frogs, Xenopus laevis and Mantidactylus betsileanus, with patterns of morphological evolution in the entire radiation of Madagascan mantellid frogs. Genes linked to morphological structure formation are expressed in a highly phase-specific pattern, suggesting uncoupling of phenotypic evolution across life-history phases. This gene expression pattern agrees with uncoupled rates of trait evolution among life-history phases in the mantellids, which we show to have undergone an adaptive radiation. Our results validate a prevalence of uncoupling in the evolution of tadpole and adult phenotypes of frogs.
Highlights
Anuran amphibians undergo major morphological transitions during development, but the contribution of their markedly different life-history phases to macroevolution has rarely been analysed
A comparison of all genes with developmental timing of expression compiled in a Xenopus laevis database (Xenbase.org; see Methods) revealed that genes associated with morphological feature formation are expressed phase- in tadpoles and adult frogs (Fig. 2; Supplementary Table 1)
Two-sided Z-tests found genes associated with morphological feature formation to make up a significantly higher proportion of genes expressed during specific life phases, than of those expressed across all phases, in both Mantidactylus and Xenopus (Supplementary Table 2)
Summary
Anuran amphibians undergo major morphological transitions during development, but the contribution of their markedly different life-history phases to macroevolution has rarely been analysed. We generate testable predictions for coupling versus uncoupling of phenotypic evolution of tadpole and adult life-history phases, and for the underlying expression of genes related to morphological feature formation. Genes linked to morphological structure formation are expressed in a highly phase-specific pattern, suggesting uncoupling of phenotypic evolution across life-history phases. The lipid-like juvenile hormone in Drosophila melanogaster has pleiotropic phenotypic effects both pre- and post metamorphosis[3] Such linked or coupled evolution of life-history phases, where selection events targeting one life-history phase affect traits in another phase, can best be studied in organisms with discrete phases, such as those with larvae differing considerably from the adult body plan. Harris[11], building on Falconer[12], used data on tadpoles to propose models of evolution of traits coded by the same gene in both phases of the anuran life cycle. A similar alternative heuristic model that considers uncoupling itself as a trait[11,12] led to a partly similar prediction, that is, uncorrelated traits affecting only one of the phases are fixed at higher frequency than traits correlated across phases
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