Genomic Insights into Sexual Selection and the Evolution of Reproductive Genes in Teleost Fishes

Abstract

Sexual selection has long been a working explanation for the elaboration of appreciable traits in plants and animals, but the idea that it is an equally potent agent of change at the level of individual molecules is relatively recent. Indications that genes associated with reproductive biology evolve especially rapidly planted this notion, but many details about the genomics of sex remain elusive. Numerous studies have characterized rapid sequence and expression divergence of sex-related molecules, but few if any have demonstrated convincingly that these patterns exist as a result of sexual selection. This dissertation describes several genome-scale studies related to reproduction and the sexes in teleost fishes, a group of animals underexploited in regard to this topic.

Using commercial microarrays I measured the extent of sexually dimorphic gene expression in the zebrafish, Danio rerio. Sex-biased patterns of gene expression in this species are similar to those described in other animals. A number of genes expressed at high levels in ovaries and testes relative to the body were identified as a product of the study, and these data may be useful for future studies of reproductive genes in Danio fishes.

In a second study, the recent advent of high throughput cDNA pyrosequencing was leveraged to characterize the relationships between tissue-, sex-, and species-specific expression patterns of genes and rates of sequence evolution in swordtail fishes (Xiphophorus). I discovered ample evidence for expression biases of all three types, and a generally positive but idiosyncratic relationship between the magnitude of expression bias and rates of protein-coding sequence evolution.

Pyrosequencing of cDNA was also used to explore the possibility that postcopulatory sexual selection drives the rapid evolution of male pregnancy genes, a novel class of reproductive molecules unique to syngnathid fishes (seahorses and pipefishes). Genes differentially expressed in the male brooding tissues as a function of pregnancy status evolve more rapidly at the amino acid level than genes exhibiting static expression. Brooding tissue genes expressed during male pregnancy have evolved especially rapidly in polyandrous lineages, a finding that supports the hypothesized relationship between postcopulatory sexual selection and the adaptive evolution of reproductive molecules.