1 | INTRODUCTION
The spread of infectious diseases is recognised as one of the most pressing global threats to biodiversity and ecosystem function (Daszaket al. 2000; Tompkins et al. 2015; Cunningham et al. 2017). In recent decades, infectious diseases have devastated a range of wildlife groups (Berger et al. 1998; Kim & Harvell 2004; Hansen et al. 2005; Lorch et al. 2016), often exacerbating species declines in ecosystems already stressed by climate change and habitat destruction (Harvell et al. 2002; Brearleyet al. 2013; Bosch et al. 2018). The future persistence of many species will likely depend on their ability to adapt to environmental changes associated with increased disease prevalence, although selection for disease resistance or tolerance may not keep pace with rates of pathogen evolution and the emergence and turn-over of novel diseases (Hawley et al. 2013; Ujvari et al. 2014).
Detecting evolutionary changes in disease affected populations is challenging but has been greatly assisted by modern genomic technologies (Blanchong et al. 2016; Storfer et al. 2020). These technologies now allow for rapid and cost-effective estimates of genome wide variation among populations spanning disease infection gradients and individuals with distinctive phenotypes related to disease response (Elbers et al. 2018; Grogan et al. 2018; Margres et al. 2018; Auteri & Knowles 2020). Importantly, a number of studies using these technologies have reported rapid evolutionary changes across several generations in natural populations of non-model organisms impacted by disease, including Tasmanian devils (Sarcophilus harrisii ) (Epstein et al. 2016; Hubert et al. 2018; Margres et al. 2018) and North American house finches (Carpodacus mexicanus ) (Bonneaud et al. 2011). Additionally, recent studies have reported evidence of rapid selection for disease resistant genotypes across a single generation in North American sea stars (Pisaster ochraceus ) and little brown bats (Myotis lucifugus ), following rapid and severe population crashes due to infectious diseases (Schiebelhut et al. 2018; Auteri & Knowles 2020). Such studies are pivotal in highlighting the pace at which selection can act to counter disease in wildlife communities and opening up opportunities for interventions, such as deliberate translocations of adaptive phenotypes, that can increase the adaptability of threatened populations (Hohenlohe et al. 2019; Hoffmann et al. 2020). Despite this progress, the number of studies demonstrating rapid evolutionary responses to infectious diseases in natural populations remains limited and biased towards terrestrial systems.
Marine infectious diseases are responsible for incremental and mass mortalities in a variety of wildlife groups, including keystone and habitat forming taxa (Harvell et al. 2007; Clemente et al.2014; Martin et al. 2016; Montecino-Latorre et al. 2016; Harvell & Lamb 2020), and species supporting wild commercial fisheries (Marty et al. 2010; Cawthorn 2011; Lafferty et al. 2015; Crosson et al. 2020). The Australian blacklip abalone (Haliotis rubra ), a species targeted by the world’s largest wild abalone fisheries and a rapidly expanding aquaculture industry (FAO Fishstat 2021), was heavily impacted by disease between 2006 and 2010 (Mayfield et al. 2012). Abalone viral ganglioneuritis (AVG) caused by the haliotid herpesvirus-1 (HaHV-1) spread along the western coastline of Victoria in south-eastern Australia, causing rapid and severe population collapses (> 90% mortality in some areas) and devastating both wild and farmed abalone stocks (Hooperet al. 2007). Despite the impact of AVG, abalone stocks in the Western Zone fishery have seen significant recovery, and are considered sustainable (Mundy et al. 2020). Given the short generation time of the species (~4 years; Andrews 1999), large population sizes, and high levels of genetic variability that contribute to existing patterns of adaptation across the fishery (Miller et al. 2019), it is possible that rapid evolutionary responses have contributed to this recovery.
Previous research has demonstrated heritable genetic variation relating to herpesvirus immunity in Haliotid species. Challenge tests performed on New Zealand paua (H. iris ) and Japanese black abalone (H. discus ), involving controlled exposure to Haliotid herpesvirus-1 (HaHV-1), indicated complete immunity to AVG (Changet al. 2005; Corbeil et al. 2017), with complementary transcriptomic analyses helping to characterise the genetic basis of the resistance (Bai et al. 2019b; Neave et al. 2019). Similar tests on H. rubra yielded no evidence of resistance to AVG (Craneet al. 2013; Corbeil et al. 2016), however, these experiments were performed on a small number of animals from a limited number of locations affected by AVG. While complete immunity may not occur in H. rubra , the presence of AVG immunity in sister taxa hints at the potential for some level of resistance developing through standing genetic variation following AVG exposure.
In this study, we explore the possibility of a rapid evolutionary response in recovering H. rubra fishing stocks devastated by AVG. Specifically, we performed a genome wide association study (GWAS) using pooled whole genome re-sequencing data on H. rubra specimens from fishing stocks varying in disease exposure. Our findings point to rapid changes in population-level allele frequencies over a single generation time-scale in virus affected fishing stocks, with stock recovery determined by rapid evolutionary changes leading to virus resistance. This study highlights the pace at which adaptive phenotypes can potentially evolve and spread in wildlife communities to counter threats from infectious diseases. We discuss these findings in the context of future biosecurity management of Australian abalone fisheries and wildlife conservation more generally.