Genomic Consequences of Hybridization between Rainbow and Cutthroat Trout

Abstract

Introgressive hybridization creates novel gene combinations that may generate important evolutionary novelty and thus contribute to biological complexity and diversification. On the other hand, hybridization with introduced species can threaten native species, such as cutthroat trout (Oncorhynchus clarkii) following the introduction of rainbow trout (O. mykiss). While rainbow trout introgression in cutthroat trout is well documented, neither the evolutionary consequences nor conservation implications are well understood. Hybridization between rainbow and cutthroat trout occurs in the context of substantial chromosomal rearrangement, as well incompletely re-diploidized genomes. Rainbow and cutthroat trout are descended from an autopolyploid ancestor, and extensive chromosome arm rearrangements have occurred between the species following their divergence from the last common ancestor. Evidence for incomplete re-diploidization includes the occasional formation of multivalents and duplicated loci occasionally exhibit a mixture of disomic and tetrasomic inheritance. Thus, transmission genetics may be complicated by recombination between homeologs. Here, I evaluated the phenotypic and genetic consequences of introgression between rainbow trout and Yellowstone cutthroat trout (O. clarkii bouvieri) to provide insights into genome processes that may help explain how introgression affects hybrid genome evolution. The overall aim of the first part of this dissertation (Chapters 1 and 2) was to evaluate phenotypic variation and gene expression among parental species and hybrids to gain insight into the genetic basis of hybrid and parental morphologies. We constructed seven line crosses: both parental species, both reciprocal F1 hybrids, first-generation backcrosses, and F2 hybrids. In Chapter 1, we aimed to assess the role of introgression on growth (length and weight gain), morphology, and developmental instability among these seven crosses. Growth was related to the proportion of rainbow trout genome contained within crosses. Rainbow and cutthroat trout were morphologically divergent: rainbow trout were generally robust whereas cutthroat trout were typically more slender and their hybrids tended to be morphologically intermediate, although backcrosses were morphologically more similar to their backcrossing parental species. These differences in growth and body morphology may be maintained, in part, through the regulation of muscle growth-related genes. Therefore, in Chapter 2, we aimed to characterize the expression of muscle growth-related genes and to describe relationships between gene expression and growth patterns among parental species and hybrids to gain insight into the underlying genetic basis of the difference in their body shapes. Our findings suggest that rainbow and cutthroat trout exhibit differences in muscle growth regulation, that transcriptional networks may be modified by hybridization, and that hybridization disrupts intrinsic relationships between gene expression and growth patterns that may be functionally important for phenotypic adaptations. The overall aim of the second part of this dissertation (Chapters 3 and 4) was to assess the genetic consequences of introgression to determine how the genomic architecture of hybrids affects allelic inheritance, and thus their subsequent evolution. In Chapter 3, we generated a genetic linkage map for rainbow-Yellowstone cutthroat trout hybrids to evaluate genome process that may influence introgression genome evolution in hybrid populations. Our results suggest that few genomic incompatibilities exist between rainbow and cutthroat trout, allowing their to genomes introgress freely, with the exception that differences in chromosome arrangement between the species may act as barriers to introgression and enable large portions of non-recombined chromosomes to persist within admixed populations. In Chapter 4, we aimed to determine the effect of incomplete re-diploidization on transmission genetics in hybrids, compared to pure species. We used the parental gametic phase from existing genetic linkage maps to identify the homeologs that recombine, to characterize this recombination, and to verify meiotic models of residual tetrasomic inheritance in autotetraploids. Recombination between homeologs occurred frequently in hybrids and results in the non-random segregation of alleles across extended chromosomal regions as well as extensive double-reduction in hybrid parental gametes. Taken together, the results from Chapters 3 and 4 suggested that chromosome rearrangements and recombination of homeologs could influence genome evolution in admixed populations. The research presented in this dissertation indicated that the evolutionary fate of hybrid genomes is unpredictable. Some of our findings suggest that introgressions proceeds in a predictable fashion in admixed populations; rainbow and cutthroat genomes freely introgress, with the exception that chromosome rearrangements may suppress recombination across large chromosomal regions. However, homeologous recombination during meiosis in hybrids results in unpredictable segregation of chromosomes, and the segregation of these chromosomes may depend on the hybrid generation of each parent within an admixed population. Furthermore, phenotype and gene expression are quantitative traits, and expression of these traits may depend on hybrid genotypes across transcriptional networks that are controlled by genes distributed over the entire genome. Consequently, hybridization may alter transcriptional regulation of genes, resulting in unpredictable gene expression patterns, which, in turn, contribute to the high phenotypic variation in hybrids.