Year of Award

2022

Document Type

Dissertation

Degree Type

Doctor of Philosophy (PhD)

Degree Name

Organismal Biology, Ecology, and Evolution

Department or School/College

Division of Biological Sciences

Committee Chair

Jeffrey M. Good

Commitee Members

Douglas J. Emlen, Lila Fishman, Travis Wheeler, Erica L. Larson

Keywords

Evolution, Gene expression evolution, Genomics, Speciation, Spermatogenesis

Publisher

University of Montana

Abstract

Reproductive traits are fascinating from an evolutionary perspective because they are necessary for individuals to produce offspring and increase their evolutionary fitness. Given the essentiality of reproduction to fitness, genes involved in reproduction may be expected to be highly conserved. However, some genes involved in reproduction evolve very rapidly, including many spermatogenesis genes. This rapid evolution may result from intense sexual selection acting on reproductive traits, particularly in species where females mate multiply thus creating the potential for sperm competition. In addition to sexual selection, other evolutionary forces may shape rapid spermatogenesis evolution, including genomic conflict and relaxed pleiotropic constraint due to the high specificity of genes involved in spermatogenesis. It is unclear how these forces may interact, their relative importance in spermatogenesis molecular evolution, and how the intensity of these forces changes across spermatogenesis developmental stages. Rapid spermatogenesis evolution is thought to have important downstream consequences, including rapid phenotypic evolution of male reproductive traits and reproductive barriers that contribute to speciation. However, direct connections between molecular evolution, phenotypic evolution, and speciation have rarely been made for male reproductive traits. Thus, my dissertation seeks to understand what are the causes and consequences of rapid spermatogenesis molecular evolution?

House mice (Mus musculus) and closely related species are an ideal system in which to address this question because they experience sperm competition, form natural hybrid zones and produce sterile hybrid males, readily breed and hybridize in the laboratory, and have extensive genomic resources available. Furthermore, house mice are part of the massive Murinae subfamily of rodents, which comprise over 10% of all mammal species and show remarkable variation in reproductive traits, including sperm morphology. Spermatogenesis is a complex developmental process, so understanding variation in the intensity of different evolutionary forces across spermatogenesis stages is critical to understanding spermatogenesis evolution. Fluorescenceactivated cell sorting is one way to generate enriched cell populations representing different spermatogenesis stages. In this dissertation, I use gene expression data from sorted cell populations in house mice, as well as genomic and phenotypic data from mice and other murine rodents to study mammalian spermatogenesis evolution.

In Chapter 1, I use data from enriched cell populations representing two different spermatogenesis stages and four different species of mice to investigate the relative rates of molecular evolution across spermatogenesis and the types of mutations underlying gene expression evolution in different spermatogenesis stages. I show that lineage-specificity of genes expressed, gene expression level divergence, and protein sequence divergence all increase during the late stages of spermatogenesis. I also show that protein coding divergence, but not gene expression divergence, is higher on the X chromosome than the autosomes across spermatogenesis cell types. Lastly, I use published data from F1 mouse crosses to do allelespecific expression analyses and show that the types of regulatory mutations underlieing expression divergence are strikingly different between early and late spermatogenesis. This study provides insight into mammalian spermatogenesis molecular evolution and shows the importance of developmental context in molecular evolutionary studies. In Chapter 2, I perform two genetic

experiments involving advanced-generation hybrid mouse crosses to explore hybrid incompatibilities on the sex chromosomes and their effects on hybrid male spermatogenesis expression and reproductive phenotypes. My results refute the hypothesis that genomic conflict between the sex chromosomes contributes to sex chromosome overexpression during late spermatogenesis in sterile mouse hybrids. However, they do show that incompatibilities between the X and Y chromosomes, between the Y chromosome and autosomes, or both likely contribute to male hybrid sterility in house mice. These findings advance our understanding of genetic incompatibilities contributing to male hybrid sterility, a common barrier to reproduction between species. In Chapter 3, I expand my research on spermatogenesis evolution to the Murinae subfamily, using exome capture and phenotype data to investigate the role of sexual selection in sperm morphological evolution and test for positive selection acting on male reproductive genes. My analyses indicate that relative testes mass is evolving indepently of phylogeny, and therefore may be evolving in response to sperm competition. Most Murinae sperm have a hook on the sperm head, and I show that hook length and angle are correlated with relative testes mass suggesting that these traits may also be selected on by sperm competition. Lastly, I find that genes expressed in rapidly evolving male reproductive tissues and spermatogenesis cell types, specifically seminal vesicles and postmeiotic spermatids, tend to experience more positive selection than other male reproductive genes, so their rapid evolution is likely due in part to positive selection. These findings contribute to our understanding of the underlieing causes of the rapid evolution of reproduction at both the phenotypic and molecular levels.

In addition to these three chapters, I contributed to several related projects that address the overarching questions of my dissertation: a review on sex chromosome evolution in mammals in the context of spermatogenesis (Larson, et al. 2018), two methodological papers on quantifying sperm morphology (Skinner, et al. 2019a; Skinner, et al. 2019b), a peer-reviewed research article on disrupted X chromosome expression at different spermatogenesis stages in sterile house mouse hybrids (Larson, et al. 2021), and a study on X chromosome evolution in dwarf hamsters (Moore, et al. 2022). Collectively, my dissertation and related projects contribute to our understanding of reproduction and molecular evolution in mammals.

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© Copyright 2022 Emily Emiko Konishi Kopania