Evidence for Speciation With Gene Flow: An Examination of the Evolutionary Genetics of Blue-Footed and Peruvian Boobies

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Taylor, Scott Anthony
Molecular Ecology , Evolution , Speciation , Hybridization , Seabird Ecology , Population Differentiation
Successful preservation of Earth’s biodiversity requires an understanding of the processes that generate new species. The generation of species without gene exchange is considered predominant; however, a growing body of evidence indicates that populations can diverge while exchanging genes, and that this may be common. Previous research hypothesized that blue-footed (Sula nebouxii) and Peruvian (S. variegata) boobies diverged from their common ancestor while exchanging genes. Here, I combine ecological and genetic perspectives to thoroughly evaluate this hypothesis. Using a panel of eight molecular markers, I estimate population differentiation for each species. I find evidence of weak population differentiation for both species, an uncommon pattern in seabirds, and argue that specialization to an unpredictable food resource has shaped contemporary population differentiation. Next, I use molecular markers and morphology to evaluate the hybrid status of five morphologically aberrant individuals. I report that all are likely F1 (first generation) hybrids, and are the product of crosses between female Peruvian boobies and male blue-footed boobies. Sex biases in pairing may occur because of an underlying preference for elaborate courtship displays. I then expand the dataset to 19 loci and use cline theory and Bayesian assignment tests to characterize the hybrid zone, to examine introgression, and to evaluate the hybrid status of the aberrant individuals. The hybrid zone is most likely maintained by strong endogenous and exogenous selection against hybrids and dispersal of parentals into the hybrid zone (a tension zone), and introgression is low for nuclear loci and absent for mitochondrial loci. Finally, I test the hypothesis that this species pair diverged from their common ancestor with gene flow using recently developed analyses and multiple loci. Divergence without gene flow is rejected and unidirectional introgression of sex-linked loci during divergence is reported. The results of this study support the hypotheses that: 1) populations can diverge while exchanging genes; 2) the Z chromosome may play a role in avian speciation; and 3) organisms specialized to variable foraging environments should exhibit low population differentiation. This study adds to our understanding of both population differentiation and speciation in seabirds, and the generation of new species more generally.
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