The evolution of neo-sex chromosomes in Australian honeyeaters (Aves: Meliphagidae)

Abstract

Sex chromosomes display remarkable diversity across the tree of life, including extraordinary variation in their number, size, content, sex determining pathways, and rates of turnover, often even among closely related lineages. In birds, the Z and W sex chromosomes were thought to be stable and immune from evolutionary turnover events because they arose over 140 million years ago and appear to be present in all extant avian lineages. However, discoveries of neo-sex chromosomes, which constitute a type of turnover involving autosomal fusions with ancestral sex chromosomes, have begun to accumulate in various avian lineages. My dissertation focuses on describing the structure and phylogenetic distribution of neo-sex chromosomes in honeyeaters (Aves: Meliphagidae), investigating potential consequences of their formation in the context of gene expression, and finally examining their potential role in climate adaptation. In Chapter 1, I characterize the putative fusion and structure of the neo-Z chromosome with genomic data by creating a high quality long-read genome and comparing it with other avian genomes. In Chapter 2, I integrate cytogenetic data and whole genome resequencing data to validate the fusion and structure of both neo-Z and neo-W chromosomes and resolve the phylogenetic distribution of neo-sex chromosomes in this clade. I also conduct phylogenetic tests to determine the timing and extent of recombination suppression on the neo-W, which is a hallmark of sex chromosome evolution and over time results in degeneration of the W. In Chapter 3, I investigate the evidence for dosage compensation on the neo-sex chromosomes, which is a regulatory mechanism that can evolve in response to degeneration of the neo-W to restore ancestral gene expression levels. I find evidence of incomplete dosage compensation in both the ancestral and added region of the neo-sex chromosomes. In Chapter 4, I conduct genotype-environment association analyses in a honeyeater with neo-sex chromosomes distributed across an aridity gradient in New South Wales. I find the ancestral Z has more significant associations with climate than the added Z and unexpectedly discover a number of large outlier regions on autosomes, including a polymorphic inversion, that are highly associated with climate and likely facilitating local adaptation through recombination modification. Taken together, my dissertation leverages genomic, transcriptomic, and cytogenetic data to shed light on a novel avian sex chromosome system and explore effects of its formation.