When divergent populations come into contact and interbreed, incompatible genotypes can result in decreased hybrid fitness and partial reproductive isolation. By studying patterns of gene flow between populations, we can identify the genetic, phenotypic, and ecological components of partial reproductive isolation. Using whole-genome sequence data generated from 1201 yellow-rumped warblers (Setophaga coronata coronata, S. c. auduboni, and their hybrids), we measure variation of a hybrid zone’s position in space and over time, identify genomic regions where gene flow is restricted, and compare the genetic basis of reproductive barriers to the genetic basis of plumage traits. We find that reproductive isolation is generated by the effects of many loci throughout the genome, with a large influence of the sex-chromosomes, that “barrier loci” cluster in some highly differentiated regions, and that gene flow and introgression are broadly asymmetric. Barrier loci show strong linkage disequilibrium, which augments the strength of the barrier to gene flow and may indicate the presence of genetic incompatibilities. Clines in plumage traits and their associated SNPs suggest strong selection against some hybrid phenotypes, although loci with the strongest associations with plumage color traits do not exhibit the strongest barrier to gene flow.

The study of speciation has expanded with the increasing availability and affordability of high-resolution genomic data. How the genome evolves throughout the process of divergence and which regions of the genome are responsible for causing and maintaining that divergence have been central questions in recent work. Here, we use three pairs of species from the recently diverged bee hummingbird clade to investigate differences in the genome at different stages of speciation, using divergence times as a proxy for the speciation continuum. We then use the same study system to compare populations in allopatry with populations in a hybrid zone for each sister species pair. We look for patterns of population structure and introgression across the genome and at different chromosome types. Finally, we use a single species to quantify variation in a species-diagnostic sexually-selected trait. Overall, we found different levels of differentiation and introgression across different chromosome types. Using FST as our relative measure of differentiation we found that the sex chromosome shows signs of divergence early in speciation. Next, small autosomes (microchromosomes) accumulate highly diverged genomic regions, while the large autosomes (macrochromosomes) accumulate genomic regions of divergence at a later stage of speciation. Our finding that genomic windows of elevated FST accumulate on small autosomes earlier in speciation than on larger autosomes is counter to the prediction that FST increases with size of chromosome (i.e. with decreased recombination rate), and is not represented when weighted average FST per chromosome is compared with chromosome size. The results of this dissertation suggest that multiple chromosome characteristics such as recombination rate and gene density combine to influence the genomic signatures of divergence and introgression.

Background

Results

Conclusions

In solitary sexually reproducing diploid organisms, frequency dependent selection maintains the population sex ratio at an equal proportion of male to female offspring. A 1:1 sex ratio equilibrium is expected because each sex contributes half of their ancestry to the following generation. Typically, selection occurs at the level of the parents. This contrasts sex ratio predictions in social Hymenoptera (ants, bees, and wasps), where there are two stark differences. 1) In social Hymenoptera, sex determination leads to a difference in ploidy level, where males are haploid, and females are diploid. 2) Selection on sex ratios is more complex in social Hymenoptera as brood care is primarily performed by sterile workers instead of the parents. As a result of these differences, reproductive queens and workers can be in conflict because diploid workers are more related to their diploid sisters than to their haploid brothers. Split sex ratio, where colonies produce only future queens (=gynes) or only males, is an extreme form of biased sex ratios and is observed throughout social Hymenoptera. But what leads to split sex ratios? A meta-analysis found the variance in split sex ratio can be explained, in part, by relatedness asymmetries (~20%) and colony queen number (~5%). A genetic polymorphism that predisposes colonies to produce only gynes or only males could explain some of the variance. In this dissertation, I aim to answer three overarching questions in Formica ants. In Chapter 1, I ask if a genetic polymorphism underlies colony sex ratio in two species. I find the presence of a non-recombining haplotype is associated with colony gyne-production in single-queen colonies. In Chapter 2, I ask how a gyne-producing haplotype originated within the genus. I find there are two origins for the gyne-producing haplotype that formed because of two different double-recombinant events. In Chapter 3, I expand to include multiple populations of the Chapter 1 species. I ask if multi-queen colonies also harbor the gyne-producing haplotype and whether population haplotype frequencies vary. I find species- and population-level variation exists in multi-queen colony sex ratios. I also find spatial variation in haplotype frequencies in one species but not the other. In summary, the presence of a non-recombining haplotype determines colony gyne production. The gyne-producing haplotype has at least two origins, one origin in Nearctic species and another origin in a Palearctic lineage. Intraspecific population frequency variation of the gyne-producing haplotype may lead to other colonies taking the role of gyne production.

My dissertation focuses on the evolutionary effects of introgression on a complex group of paradise spiders that experience strong sexual selection. I use an integrative approach to evaluate morphological, genetic, and behavioral consequences of gene flow across species boundaries in the Habronattus americanus subgroup. In Chapter 1, I uncover extensive genomic homogenization between members of the americanus subgroup, such that evolutionary lineages reflect geography rather than species or morph type. Despite the genomic homogenization, selective forces maintain the very diverse male courtship ornamentation of different species and morphs. In Chapter 2, behavioral analyses of courtship display traits indicate a geographical pattern with a southeastern display group and a western+northern display group. Courtship displays in the southeastern distribution include more fling repetitions and longer introductory motif times compared to courtship displays from other geographical areas. Patterns of courtship display diversity are discordant with patterns of morphological diversity and seem to align more with geographical location than morph or species identity. In Chapter 3, population genetic and morphological analyses from a H. americanus x H. kubai hybrid zone near Mt. Shasta, CA uncover very little genomic diversity but substantial morphological diversity of male courtship ornamentation traits, which seem easily introgressed across species boundaries. Hybrid zone dynamics at Mt. Shasta appear to act as a microcosm for periodic processes of divergence and reticulation in the entire americanus subgroup. In its entirety, my dissertation offers an integrative analysis of the effects introgression may have on diverging lineages and highlights the importance of new perspectives on how we think about speciation and lineage diversification.