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.