Microevolution in Natural and Experimental Hybrid Populations of Swordtail Fish

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2022-07-07

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Abstract

Hybridization is a common phenomenon that serves as an important evolutionary mechanism by which diversity can arise. When two genetically divergent species hybridize, the resulting admixture generates novel genotypic and phenotypic combinations. Depending on a host of demographic, genetic, and environmental conditions, hybrid zone evolution can have various evolutionary outcomes. Natural hybrid zones between two species can offer a unique opportunity to study how hybridization impacts adaptive evolution in admixed populations due to their natural history and ecological circumstances. In my dissertation, I use two freshwater species of fish, Xiphophorus birchmanni and X. malinche, that form replicated natural hybrid zones to address how hybrid populations evolve and to identify barriers that contribute to maintaining isolation between species. To uncover how morphology evolves in hybrid populations, I measured sexually selected male traits in three independent natural hybrid populations as well as three experimental, early generation hybrid populations located at different elevational treatments for approximately 5 years. Principal component analysis revealed the two natural hybrid populations located at lower elevations to share similar morphology with the lowland parental species X. birchmanni, and that the third natural hybrid population located at higher elevations shared more similarity with the highland parental species, X. malinche. Overall, I found in the lowland natural hybrid populations, environment drives morphology to resemble the lowland parental species. In the highland natural hybrid population, morphology aligns with genome-wide hybrid index. These findings reveal independent hybrid populations can exhibit similar morphometric combinations of traits despite genome-wide ancestry composition, but that it is context dependent. In other cases, morphology aligns with the genome-wide ancestry. Most notably, within the experimental hybrid populations, I found more variation was shared between sites than within sites. Across each experimental hybrid site, the amount of variation in morphology among replicates was relatively the same. Additionally, I make use of whole genome-wide sequence data for a subset of the individuals in the study and found the average hybrid index at each site trended in the direction that would be expected if environmental selection was driving genome-wide changes in ancestry. When species hybridize along climate gradients, selection should favor the introgression of alleles that mitigate the fitness cost of environmental change. Quantifying the introgression of loci associated with fitness in hybrid zones is critical to predicting how hybridization aligns with responses to climate change. To this end, we performed a QTL analysis on intercrossed experimental, early generation hybrids with the aim to identify genomic regions associated with interspecific differences in thermal tolerance and found an underdominant QTL located on chromosome 22. However, ancestry at this QTL did not significantly change over time in natural hybrid populations nor was it considered a candidate for selection after performing geographic cline analysis among two independent hybrid zone clines. Interestingly, however, I found several X. malinche heat-shock protein alleles to be introgressing downstream in one of the river drainages. Finally, despite abundant work on postmating-prezygotic sexual selection within the same genus of fishes, little is known about how sperm competition and cryptic female choice may mediate gene flow between species. This is particularly important as premating isolating mechanisms may be weak and are frequently susceptible to disruption of communication channels. I investigate the postmating-prezygotic barriers to reproduction and found females inseminated with equal proportions of conspecific and heterospecific sperm to bias fertilization towards the conspecific male sperm. These findings suggest postmating-prezygotic process has the potential to mediate the cost of hybridization.

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Hybridization, Speciation, Morphology, Introgression, Conspecific sperm precedence

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