Understanding how and why intraspecific genetic diversity arises

Abstract

Understanding the reasons why intraspecific diversity arises and how populations adapt to spatial variation in environmental conditions continues to be a major focus of evolutionary biology. Recently, inversion polymorphisms have become an active area of research focused on understanding how sympatric, local adaptation occurs especially when adaptation occurs at microgeographic scales (i.e., below the scale of gene flow). However, we are still lacking a comprehensive understanding of the conditions (e.g, strength of selection, migration rate, architecture of the evolving trait) needed for inversions to facilitate local adaptation, the traits underlying adaptation, and how well we can detect them empirically. To address these gaps, my dissertation takes three distinct, but complementary approaches to understanding adaptation below the scale of gene flow in my study species Atlantic cod (Gadus morhua). Atlantic cod in the US Gulf of Maine (GOM) and Iceland harbor putative ecotypes (i.e., coastal, stationary cod and offshore, migratory cod), but we have limited genomic and phenotypic understanding for how they have evolved in these regions. To assess this, Chapter 2 is an empirical assessment of population genomic structure using high-resolution whole genome sequencing and phenotypic differentiation using body morphometric analyses. I show that although fine-scale population structure may be present between locations within the GOM, inversion haplotypes are not segregating (meaning present as uninverted in one group and as inverted in the other) between putative ecotypes (i.e., GOM color morphs) and morphological data suggest a lack of a migratory body shape in the GOM. In Iceland, however, inversions underlying ecotype differences do segregate and correspond with a more streamlined body shape found in offshore ecotypes compared to coastal ecotypes. When comparing across locations, GOM cod showed both body shape variation and inversion haplotype structure that was more closely related to coastal Icelandic cod further suggesting that GOM may be less migratory than offshore Icelandic cod. In Chapter 3, I built on these findings by comparing empirical results to theoretical expectations for the role of inversions in adaptation using forward-time simulations. With these simulations, I explored the conditions needed for inversion polymorphisms to facilitate local adaptation under gene flow (as we would expect in Atlantic cod ecotypes) and identified whether specific inversion characteristics (i.e., age, size, and evolutionary origin) evolved when they harbored the genetic basis of local adaptation. Inversions facilitated adaptation under high gene flow when selection was strong for the trait involved in adaptation and when the trait was governed by a polygenic architecture. I also identified that all locally-adaptive inversions were large in size, arose early in divergence when they captured loci at the time of mutation, and continued to gain additional adaptive loci over time. These results give a more robust understanding of how and why genomes with multiple, large inversions evolve across many species with locally-adapted ecotypes and the specific conditions needed for inversions to be involved in adaptation. Finally, in Chapter 4, I complement spatial analyses with a temporal reconstruction of historical thermal regimes experienced by Icelandic cod populations. I took advantage of a collection of archeological Icelandic cod otoliths that spanned the mid 14th century through the 19th century, excavated from historical middens of fishing villages along the coast of Iceland. Through microchemical analysis of oxygen stable isotopes in these otoliths, I revealed that Icelandic cod experienced cooling conditions over this time period that was equivocal between adult and juvenile cod. Our results suggest that adult cod may not have undergone migrations to escape the rapid cooling that occurred during the "Little Ice Age" and increases in their thermal habitat predicted under climate change will be temperatures that these populations have not experienced over the last six centuries. Combining data from my dissertation, I found interesting and complex patterns of genomic and morphometric differentiation in Atlantic cod both within and across regions, outlined specific conditions for inversions to facilitate adaptation, and identified variation in thermal environments over an evolutionarily relevant timescale by using historical samples. --Author's abstract