Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer

By Y. F. Chan, M. Marks, F. Jones, Guadalupe Villarreal, M. Shapiro, S. Brady, A. Southwick, D. Absher, J. Grimwood, J. Schmutz and 6 more. Science, 2009

1,037 citations recorded by the source corpus.

Adaptive Girdle Loss in Sticklebacks How do molecular changes give rise to phenotypic adaptation exemplified by the repeated reduction in the pelvic girdle observed in separate populations of sticklebacks? Now Chan et al. (p. 302, published online 10 December) have identified the specific DNA changes that control this major skeletal adaptation. The key locus controlling pelvic phenotypes mapped to a noncoding regulatory region upstream of the Pituitary homeobox transcription factor 1 gene, which drives a tissue-specific pelvic enhancer. Multiple populations showed independent deletions in this region and enhancer function was inactivated. Reintroduction of the enhancer restored pelvic development in a pelvic-reduced stickleback. Loss of a tissue-specific enhancer explains multiple parallel losses of the pelvic girdle in stickleback populations. The molecular mechanisms underlying major phenotypic changes that have evolved repeatedly in nature are generally unknown. Pelvic loss in different natural populations of threespine stickleback fish has occurred through regulatory mutations deleting a tissue-specific enhancer of the Pituitary homeobox transcription factor 1 (Pitx1) gene. The high prevalence of deletion mutations at Pitx1 may be influenced by inherent structural features of the locus. Although Pitx1 null mutations are lethal in laboratory animals, Pitx1 regulatory mutations show molecular signatures of positive selection in pelvic-reduced populations. These studies illustrate how major expression and morphological changes can arise from single mutational leaps in natural populations, producing new adaptive alleles via recurrent regulatory alterations in a key developmental control gene.

Subfields: Genetics, Molecular Biology

View Paper: https://www.semanticscholar.org/paper/3b054cd3df2798db921eb860f35802611e25328d

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In Genetics

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Citations in the corpus

• Adaptive Radiation, Ecological Opportunity, and Evolutionary Determinism (2010, background): “…Derome et al. 2006; Hoek-stra et al. 2006; Protas et al. 2006; Shapiro et al. 2006; Whittall et al. 2006; Baxter et al. 2008; Gross et al. 2009; Chan et al. 2010; of course, this is not always the case: sometimes convergent phenotypic evolution is accomplished by different genetic changes,…”
• Contemporary evolution, allelic recycling, and adaptive radiation of the threespine stickleback (2013, methodology): “If recycled freshwater-adapted alleles are absent in a founding population, new mutations in freshwater populations may form the basis for adaptation (Chan et al., 2010; Leinonen et al., 2012), but that would generally delay adaptation (Barrett and Schluter, 2007; Hunt et al., 2008).”
• Functional and mechanistic diversity of distal transcription enhancers (2011, neutral): “In stickleback fish that have pelvic fins, this enhancer specifically activates Pitx1 gene expression in the pelvic fins during development (Chan et al., 2010; Levine, 2010).”
• CONVERGENCE, ADAPTATION, AND CONSTRAINT (2011, neutral): “…argu-ment that repeated recruitment of the same gene or even the same mutation suggests the possibility of a bias in the way that variation is produced, thus constraining selection (Cooley and Willis 2009; Chan et al. 2010). twist results from the hierarchical nature of genetic variation (Fig.”
• Stickleback research: the now and the next (2013, background): “…to alternative genetic routes to the same phenotype) and, in either case, the extent to which it reflects repeated mutations at the same locus (e.g. Chan et al., 2010), new mutations at different loci, or selection on standing genetic variation that differs among source populations (e.g. Jones et…”