The evolution and genetics of sexual dimorphism

Background

Males and females of the same species are often subject to different and even contradictory selection pressures. However, with the exception of the Y chromosome, the sexes share the vast majority of their genome. This intersexual genetic correlation creates the potential for sexual conflict, which in turn selects for conflict resolution and the evolution of sexual dimorphism. Conflict is typically thought to impede sex-specific responses to natural selection and act as an evolutionary brake, yet growing evidence indicates it can shape genetic diversity in populations and act as an important force in adaptation.

Identifying if, how, and when sexual conflict can be resolved has key implications for its role in ecological adaptation. It is widely assumed that gene regulation differences between females and males can resolve sexual conflict. However, this relationship has been the subject of considerable recent debate and the potential roles of different gene regulatory mechanisms have not been tested. Furthermore, genomic studies of sexual conflict focus primarily on adults yet many sexual dimorphisms are established during embryogenesis. As a result, we lack a detailed understanding of the developmental context of sexual conflict, and its persistence and manifestation through development.

Recent studies have shown that sex-biased genes are a key component of sex-specific fitness, but how these sex differences are established and change through development is unclear. Epigenetic modifications, such as methylation, are known to play important roles in regulating gene expression by influencing the structure of the genome without changing the DNA sequence. However, the relationship between epigenetic processes, the expression of sexually antagonistic genes, and conflict resolution has not yet been rigorously tested.

Finally, our understanding of the potential for conflict to be resolved is limited. In particular, one mechanism of gene regulation that has received little attention is alternative splicing. Splicing increases proteomic complexity by generating multiple transcripts from one locus, and varies substantially across species, sexes, and tissues, as well as playing a key role in sex determination pathways. However, the evolution of sex-specific splicing, its functional importance, and role in resolving conflict has yet to be tested.

Objectives
This project will combine state-of-the-art genomic tools and high-resolution sequencing data (RNA-seq, PacBio, WGBS) across the avian phylogeny to ask:

1. How does DNA methylation contribute to sex differences in expression?
2. What is the role of alternative splicing in sexual conflict resolution?
3. How is sexual conflict manifest during development?

Specifically, these questions will be addressed using somatic and gonadal tissues sampled from males and females at multiple developmental stages across four avian species; chicken, pheasant, guineafowl and mallard duck. We have already developed population genomic pipelines to identify signatures of sexual conflict (Wright et al 2018 Evol Letters) and study alternative splicing (Rogers et al in prep) and gene expression evolution (Wright et al 2017 Nat Commun).

Novelty and Timeliness

Despite considerable recent interest in the manifestation and persistence of sexual conflict, many questions remain unanswered, particularly the role of conflict in evolutionary change. There is mixed evidence whether conflict aids or impedes adaptation, and it is not clear whether unresolved conflict hinders adaptation more than it helps. This PhD will generate an integrated understanding of the relative roles of gene regulation in resolving sexual conflict, and how these are manifest during development. In doing so, this work has broad implications for multiple fields of evolutionary biology, including phenotypic diversity, adaptation and speciation.