Co-evolution of Rabbits and the Rabbit Haemorrhagic Disease Virus (RHDV) in Australia

Abstract

The European rabbit is a keystone prey species in its native range on the Iberian Peninsula, where it is under threat from two viral diseases - myxomatosis and the rabbit haemorrhagic disease virus (RHDV). However, in its alien range the rabbit is considered one of the most damaging pest species, due to overgrazing of pastures and native vegetation. In these areas myxomatosis and RHDV have been deployed as biocontrols for landscape-scale rabbit management. Despite the initial success of viral biocontrols, increases in rabbit abundance were observed between 2003 and 2015, and evolving rabbit genetic resistance to RHDV was proposed as a key cause. Although substantial investment has been made in offsetting such resistance, through the development and introduction of new RHDV strains, the existing co-evolutionary dynamic between rabbits and RHDV in Australia is poorly understood. My thesis uses next-generation sequencing technology to explore the co-evolution of rabbits and RHDV through three approaches, presented as three publication-style manuscripts. In Chapter 2, I pilot the use of blowfly vectors to monitor spatial and temporal variation in RHDV strains. I find that wind-oriented fly traps provide improved efficiency and viral detection rates that exceed previously used rabbit carcass searches. Shotgun sequencing of RHDV capsid amplicons indicated multiple co-circulating local RHDV variants with evidence of recombination between them. This implies that intraspecific competition may play a substantial role in the direction of RHDV evolution, in addition to host resistance. In Chapter 3, I examine the underlying genetic structure of Australia’s rabbit population through a genome-wide selection of SNP loci produced through reduced representation sequencing. I find strong support for three geographically widespread rabbit lineages, as well as three individual sites with strong local differentiation. This genetic structuring is consistent with an invasion history of multiple introductions, rather than the previously assumed single primary invasion front, and may contribute to geographic variance in RHDV resistance. In Chapter 4, I combine long-term capture-mark-recapture data from a single rabbit population with a SNP-based pedigree using reduced representation sequencing. I find evidence of socially structured polygynandry with male-biased dispersal and an unexpectedly high rate of breeding outside warren-based social groups. I also examine the influence on offspring survival of warren size, birth dates and maternal antibodies to RHDV and myxomatosis. This thesis contributes to our understanding of rabbit and RHDV co-evolution by validating a more effective RHDV monitoring tool, characterising the underlying genetic variation in both host and pathogen, and analysing the pressures that drive evolution of this host-pathogen system. These insights provide the building blocks for further research to understand the mechanisms of genetic resistance to RHDV in rabbits, the extent of influence of resistance on rabbit fitness and abundance, and the impacts of current and future biocontrol activities.