FROM GENES TO GENOMES: LOCAL ADAPTATION AND ADAPTIVE POTENTIAL IN TWO ARCTIC SEABIRDS

By investigating the mechanisms underlying the evolution and the maintenance of local adaptations we can help predict how species will adapt to future environmental change. In this thesis I investigate local adaptation and adaptive potential in thick-billed and common murres (Uria lomvia and U. aalge), two arctic seabirds of international conservation concern. Thanks to the recent development of new genomic methods, I address three major themes that are relevant for both the development of evolutionary theory and conservation: 1) the role of gene flow in the origin and maintenance of adaptation; 2) levels and distribution of standing genetic variation, and their contribution to adaptive potential; and 3) the genomic mechanisms maintaining an adaptive dimorphism within a single interbreeding population. First, I review the literature on genomics of local adaptation with gene flow and find that adaptation can be maintained despite gene flow, that gene flow itself can promote adaptation, and that genetic architecture is important in the origin and maintenance of local adaptations. Second, I genotype genome-wide markers and toll-like receptor genes (TLRs) to investigate local adaptation and adaptive potential in thick-billed murres. Thick-billed murres do not show signatures of local adaptation to their breeding grounds, but outlier loci group birds according to their non-breeding distributions, suggesting that selection and/or demographic connectivity in the winter may explain patterns of differentiation in this species. Genetic variation at TLRs does not decrease with increasing latitude as predicted, but tests of selection and measures of genetic diversity suggest differences in local selective regimes at most genes. Thick-billed murres show high levels of standing genetic variation and their adaptive potential will mostly depend on rate and magnitude of environmental change. Finally, I improve and annotate the assembly of the highly heterozygous genome of the thick-billed murre. Using this assembly as a reference, I perform whole genome analyses to investigate the genomic basis of an adaptive dimorphism in Atlantic common murres. I show for the first time that a 60 kb complex copy number variant in a non-coding region maintains differences in plumage and cold adaptation despite high gene flow.

The effects of sympatry on patterns of bill morphology between closely related species of birds, worldwide

When closely related species co-occur in sympatry, they face a significant challenge. They must adapt to the same local conditions in their shared environment, which favours the convergent evolution of traits, while simultaneously minimizing the costs of competition for shared resources that typically favours the divergent evolution of traits. Here, we use a comparative sister lineage approach to test how most species have responded to these conflicting selection pressures in sympatry, focusing on a key ecological trait: the bill morphology of birds. If similar bill morphologies incur fitness costs due to species interactions, then we predicted that the bill morphologies of closely related species would differ more in sympatry compared with allopatry. Alternatively, if similar bill morphologies incur fitness benefits due to local adaptation, then we predicted that the bill morphologies would be more similar in sympatry compared with allopatry. We used museum specimens to measure five aspects of bill (maxilla) morphology – depth, length, width, side shape, and bottom shape – in diverse bird species from around the world to test our alternative hypotheses. We found support for both divergent evolution and convergent evolution (or trait retention) in one ecological trait: closely related sympatric species diverged in bill depth, but converged in side shape. These patterns of bill evolution were influenced by the genetic distance between closely related sister taxa and the geographic distance between allopatric lineages. Overall, our results highlight species interactions as an important mechanism for the evolution of some (bill depth), but not all (bill shape), aspects of bill morphology in closely related species in sympatry, and provide strong support for the bill as a key ecological trait that can adapt in different ways to the conflicting challenges of sympatry.