The comparative invasion genomics of widespread marine invaders

Abstract

Invasion genomics is a scientific discipline that advances our understanding of non-indigenous species (NIS), providing key insights into fundamental ecological / evolutionary mechanisms, and informing mitigation strategies for NIS. Despite its importance, the uptake of invasion genomics into studies of marine NIS is lacking. This is surprising as a growing number of studies show that NIS are major stressors of marine ecosystems due to their extensive ecological and environmental impacts. An ever-growing transoceanic shipping activity drives unprecedented connectivity among populations of marine NIS with unpredictable ecological and evolutionary consequences. Here I used genomic tools to investigate a number of fundamental aspects of marine biological invasions. I began by using neutral genomic markers to assess range-wide population structure of three highly invasive ascidians (Class Ascidiacea, Phylum Chordata), and how their differing levels of historical population connectivity affect the reconstruction of their invasion pathways. I then undertook a genome-wide scan of episodic selection across multiple ascidian species (including six NIS), finding that relaxation and intensification of selection induces ~30% of selective divergence. I then used genotype-environment interaction analyses to investigate the genomics of adaptation, finding common adaptive responses to temperature and salinity across multiple non-indigenous ascidians. I also investigated samples from the native and introduced ranges of the Australian ascidian species Microcosmus squamiger to identify candidate loci associated with abiotic factors within each range, including indirect evidence of enriched methylation processes within the introduced range. Lastly, I investigated how hybridisation affects local adaptation and the thermal tolerance of early life-history Ciona intestinalis. I sampled two genomically divergent populations locally adapted to different sea-surface temperature regimes (warmer and colder conditions). I found that when temperature increased, larval development success significantly increased in the warm-adapted population, but decreased in the cold-adapted population. I further probed the effects of hybridisation on locally-adapted fitness effects, finding that the effects of hybridisation (beneficial, negative, no effect) depend on the performance of the parents.
Taken together, this thesis demonstrates how genomic approaches can comprehensively advance knowledge of marine NIS, as well as how mechanisms pivotal to biological invasions such as hybridisation and adaptation can affect each other. For example, this work has provided key insights into the connectivity and movement of marine NIS. In addition, it has shown for the first time how historical population connectivity can affect the reconstruction of invasion routes based on genomic data, something key for biodiversity managers. Moreover, this thesis has shown the strength of selective forces in shaping common adaptive traits throughout multiple species, one
of the first marine studies to demonstrate this. Finally, this work shows the complex effects of hybridisation on locally-adapted fitness effects- vital considerations in biological invasions.

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