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Patterns of genomic differentiation and hybridization between two merging Emberizidae species implicate a sex chromosome inversion in plumage variation Nikelski, Ellen Glyn Marshall

Abstract

Hybrid zones offer researchers the opportunity to investigate how evolutionary processes interact to drive speciation forward. However, in these areas where genetic divergence competes against gene flow, speciation and population merging are both possible with the outcome dependent on the strength of reproductive barriers between groups. The yellowhammer (Emberiza citrinella) and pine bunting (Emberiza leucocephalos) are Palearctic songbirds with highly divergent plumage patterns. Despite their differences, these taxa hybridize extensively and show negligible differentiation in their mitochondrial genomes. These observations create a conflicting picture of the state of reproductive barriers between groups, raising the question whether yellowhammers and pine buntings are actually separate species. In this thesis, I examine patterns of genetic variation among phenotypically pure and hybrid individuals to assess the strength of reproductive isolation between taxa. I hypothesize that, unlike mitochondrial differentiation, nuclear differentiation will be moderate and that patterns of divergence will reflect some weak reproductive isolation between groups. I find that, in allopatry, yellowhammers and pine buntings separate into distinct genetic clusters based on an island of differentiation on the Z chromosome. Yet, in other parts of the genome, I find evidence of past mitonuclear gene introgression. In sympatry, I report a breakdown of allopatric genetic clusters driven by extensive interbreeding. These findings combined with the high number of late generation hybrids identified within the sympatric zone suggest that reproductive barriers are weak between taxa. Interestingly, I further find low recombination within the island of differentiation identified between allopatric populations implying that this region may house a chromosomal inversion. The inversion is highly associated with plumage variation and may be responsible for the maintenance of parental phenotypes within the sympatric zone. Because reproductive barriers are weak, it is likely that hybridization will continue between yellowhammers and pine buntings potentially leading to the merging of these groups, but that the putative inversion could preserve parental plumage phenotypes within this single species. Retention of such variation would increase the evolvability of the system such that the population could be safeguarded from extinction or, if evolutionary pressures change, could diverge again and move towards speciation.

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