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Testing evolutionary hypotheses about the phylotypic period of zebrafish

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Abstract

Vertebrate embryos pass through a period of morphological similarity, the phylotypic period. Since Haeckel's biogenetic law of recapitulation, proximate and ultimate evolutionary causes of such similarity of embryos were discussed. We test predictions about changes in phenotypic and genetic variances that were derived from three hypotheses about the evolutionary origin of the phylotypic stage, i.e. random, epigenetic effects, and stabilizing selection. The random hypothesis predicts increasing values for phenotypic variances and stable or increasing values for genetic variances; the epigenetic effects hypothesis predicts declining values for phenotypic variances but stable or increasing values of genetic variances, and the stabilizing selection predicts stable phenotypic variances but decreasing genetic variances. We studied zebrafish as a model species, because it can be bred in large numbers as necessary for a quantitative genetics breeding design. A half-sib breeding scheme provided estimates of additive genetic variances from 11 embryonic characters from 12 through to 24 hr after fertilization, i.e. before, during (15–19 hr), and after the phylotypic period. Because additive genetic variances are size dependent, we calculated narrow-sense heritabilities as a size independent gauge of genetic contributions to the phenotype. The results show declining phenotypic variances and stable heritabilities. In conclusion, we reject the random and the stabilizing selection hypotheses and favor ideas about epigenetic effects that constrain the early embryonic development. Additive genetic variance during the phylotypic stage makes it accessible for evolution, thus explaining in a simple and straightforward way why the phylotypic period differs among vertebrates in timing, duration, and morphologies. J. Exp. Zool. (Mol. Dev. Evol.) 316:319–329, 2011. © 2011 Wiley-Liss, Inc.

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