Genomic and phenotypic adaptation in a widespread passerine

Abstract

A fundamental goal in biological research is to gain deeper understanding of the ecological and evolutionary processes that drive speciation. Speciation occurs through a complex combination of phenomena that act between and within individuals, across time and space, driven by biotic and abiotic factors. Characterising these drivers is a challenging task that requires powerful analytic tools and strong study systems. Incipient species that are yet to become fully independent groups offer valuable opportunities to understand speciation by exploring it as it progresses. The Eastern Yellow Robin, a widespread Australian passerine, has a discordant pattern of genetic and phenotypic variation that makes it an ideal candidate to study speciation in action. On one hand, according to nuclear genetic markers and plumage colouration, the species varies along its range in a north-south direction. On the other hand, according to mitochondrial genetic markers, the species has a major, species-level disjunction in an east-west direction, resulting into two highly divergent mitochondrial lineages (mitolineages). The species presents a notable example of mitochondrial-nuclear (mitonuclear) discordance: a pattern in which mitochondrial gene and nuclear gene variation have discordant patterns of geographic differentiation. By disentangling this complex pattern of variation and testing hypotheses about causation, I revealed significant events during the Eastern Yellow Robins evolutionary history and proposed a mechanism by which the mitolineages are currently undergoing speciation. The Eastern Yellow Robin started to differentiate more than 1.3 million years ago into two geographically northern and southern isolated populations. During this period, much of the nuclear DNA and plumage colouration differentiation accumulated. Subsequently, these two populations came into secondary contact, generating the current pattern of north-south nuclear genetic and colour variation. After secondary contact, two independent events of adaptive mitochondrial introgression generated the current pattern of east-west mitochondrial genetic variation. According to this scenario, northern mitochondria introgressed southwards along the west and southern mitochondria introgressed northwards along the east. Mitochondrial introgression introduced adaptive genetic variation that assisted west and east mitolineages to thrive in their local environments. However, mitolineages are currently undergoing nuclear gene flow (dispersal and mating), therefore, a more complicated mechanism must be in place that prevents the two mitolineages from becoming unified. Mitochondrial and nuclear genes co-evolve to maintain essential cellular functions, such as gene expression, protein-complex assembly, metabolic, and physiological activities. By scanning thousands of genetic markers along the nuclear genome I found evidence that a subset of nuclear genetic variation accompanies the mitochondrial split. This is consistent with natural selection acting to avoid mitonuclear combinations being disrupted in intermediate forms between west and east mitolineages (i.e. hybrids). The great majority of the highly differentiated nuclear genes between mitolineages are clustered in one large genomic region. This region contains closely-linked, putatively co-adapted genes (i.e. it functions as a supergene) that are related to essential metabolic and physiological functions. This thesis contributes to a growing appreciation that interacting mitochondrial and nuclear genes involved in metabolism can influence the pattern and process of species formation.