Maternal expression increases the rate of bicoid evolution by relaxing selective constraint
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Population genetic theory predicts that maternal effect genes will evolve differently than genes expressed in both sexes because selection is only half as effective on autosomal genes expressed in one sex but not the other. Here, we use sequences of the tandem gene duplicates, bicoid (bcd) and zerknüllt (zen), to test the prediction that, with similar coefficients of purifying selection, a maternal effect gene evolves more rapidly than a zygotic gene because of this reduction in selective constraint. We find that the maternal effect gene, bcd, is evolving more rapidly than zygotically expressed, zen, providing the first direct confirmation of this prediction of maternal effect theory from molecular evidence. Our results extend current explanations for the accelerated rate of bcd evolution by providing an evolutionary mechanism, relaxed selective constraint, that allows bcd the evolutionary flexibility to escape the typical functional constraints of early developmental genes. We discuss general implications of our findings for the role of maternal effect genes in early developmental patterning.
KeywordsMaternal effect genes bicoid zerknüllt Hox genes Developmental hourglass Molecular evolution Selective constraint
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Our thanks to: C. Hughes, M. Lynch, and E. Brodie III, for insightful critiques and discussion of the manuscript. JPD was supported by a National Science Foundation—Integrated Graduate Education and Research Traineeship in Evolution, Development, and Genomics #9972830, and Doctoral Dissertation Improvement Grant #0206628. MJW and JPD were supported by the National Institutes of Health under Grant GM065414-01A.
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