Abstract
The origin of evolutionary novelty is believed to involve both positive selection and relaxed developmental constraint. In flies, the redesign of anterior patterning during embryogenesis is a major developmental innovation and the rapidly evolving Hox gene, bicoid (bcd), plays a critical role. We report evidence for relaxation of selective constraint acting on bicoid as a result of its maternal pattern of gene expression. Evolutionary theory predicts 2-fold greater sequence diversity for maternal effect genes than for zygotically expressed genes, because natural selection is only half as effective acting on autosomal genes expressed in one sex as it is on genes expressed in both sexes. We sample an individual from ten populations of Drosophila melanogaster and nine populations of D. simulans for polymorphism in the tandem gene duplicates bcd, which is maternally expressed, and zerknüllt (zen), which is zygotically expressed. In both species, we find the ratio of bcd to zen nucleotide diversity to be two or more in the coding regions but one in the noncoding regions, providing the first quantitative support for the theoretical prediction of relaxed selective constraint on maternal-effect genes resulting from sex-limited expression. Our results suggest that the accelerated rate of evolution observed for bcd is owing, at least partly, to variation generated by relaxed selective constraint.
Highlights
The origin of novel structures and functions has long been problematic for evolutionary biology
We show how to test the hypothesis of relaxed constraint using population genetic theory and sequence data from the novel Hox gene, bicoid, a critical component of the redesign of anterior patterning during fly embryogenesis, a major developmental innovation [6,7]
The redesign of anterior patterning during embryogenesis is a major developmental innovation, involving both positive selection and the overcoming of developmental constraints
Summary
The origin of novel structures and functions has long been problematic for evolutionary biology. In modern parlance, ‘‘There are problems specific for the origin of novelties that are not the same as in the case of adaptive modification of existing structures ... Novelties apparently arise in spite of strong developmental constraints that generally canalize morphological evolution’’ [3]. How descendant lineages overcome ancestral constraint is a principal research objective in the study of evolutionary novelty. One route to gaining novel structures and functions is by relaxing ancestral evolutionary constraints. We show how to test the hypothesis of relaxed constraint using population genetic theory and sequence data from the novel Hox gene, bicoid (bcd), a critical component of the redesign of anterior patterning during fly embryogenesis, a major developmental innovation [6,7]
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