Title: Evolutionary Effects of Hybridization
Abstract: Though any particular individual is extremely unlikely to mate with a member of a different species, rare hybridization can have profound effects on adaptation and evolution. As more whole genome comparative analyses are published, scientists are learning that the genomes of many species have mosaic histories, with a substantial share of alleles derived from interspecific introgression.
In Chapter 1, I review current literature on the prevalence of introgression in genomic studies, and examine mechanisms by which introgressed loci can be adaptive. Researchers have used patterns of asymmetry and expectations of branch lengths in local gene trees, as well as full network models, to identify such loci. The proportion of genomes that have a history of hybridization can be as low as a single gene and as high as 60\%. Though it is not easy to assign adaptive significance to these proportions, introgressed loci can be beneficial by contributing genetic variation, masking recessive deleterious alleles, or impacting particular traits. All of these effects are greatly influenced by the particular demographic histories of the participating populations, and at present it is difficult to estimate the impact of introgression in adaptive evolution.
In Chapter 2, I aim to characterize introgressed variation across the Heliconius butterfly radiation. Although hybridization has long been known to occur in this group, only closely related species that hybridized in the relatively recent past had been systematically investigated, and then often only for a small subset of genes. An internationally collaborative study, this project consists of assembling the genomes of 20 Heliconiini species, generating a multi-species alignment, and characterizing the extent of interspecific gene sharing across the clade and throughout the history of the radiation. I construct a whole-genome species tree and find that there is a high level of phylogenetic discordance among trees generated from different segments of the genome. This leads me to re-conceptualize the evolution of Heliconius as a network instead of a bifurcating tree, and I generate reticulate evolutionary hypotheses for the group. I next describe how loci with alternative evolutionary histories are distributed across the genome for one tractable clade. Because we generated de novo assemblies, I am able to detect two major chromosomal inversions that have histories discordant with the species tree. One of these has a history of ancestral polymorphism and incomplete lineage sorting (ILS), and I show the other to be an introgressed, convergent inversion that captures a color pattern switch locus. I next describe the general distribution of introgressed loci across the genome, in which introgression probability is strongly positively correlated with recombination rate.
In Chapter 3, I turn from large-scale genomic patterns of introgression to a case study of two sub-species of Heliconius pardalinus which, when mated together, yield sterile female offspring which produce no eggs. This phenomenon is consistent with Haldane`s rule, as females are the heterogametic sex in the lepidopteran ZZ/ZW system. Most hybrid incompatibility genes have been identified in model organisms such as Drosophila and Mus, both XX/XY sex determination systems. We have very little information about mechanisms of hybrid incompatibility in Lepidoptera. With collaborators, I generate a population of backcross individuals using the fertile F1 males. I dissect the ovaries of over 100 backcross females and score their morphological phenotypes. I also extract and sequenced RNA from a subset of the backcross and pure subspecies females. The intersection of RNA-sequencing, QTL mapping, and cross-referencing with known Lepidoptera oogenesis genes points to one candidate gene, tral, whose underexpression may be responsible for the hybrid sterility phenotype. If this is validated, it will be the first molecular characterization of hybrid sterility in a lepidopteran system.
Committee: Jim Mallet (advisor), John Wakeley, Naomi Pierce