Introduction
Coral reefs globally are
undergoing significant degradation due to mass coral mortality driven by
high sea surface temperatures (Heron et al., 2017; Hughes et al., 2018).
Increasingly warm seawater temperatures and losses in coral cover are
also leading to changes in fundamental reproductive processes (Baums et
al., 2019; Hughes et al., 2019; Shlesinger & Loya, 2019), with major
implications for ecosystem resilience and recovery in the aftermath of
severe, acute events such as mass coral bleaching. To safeguard the
persistence and resilience of coral reefs, assisted evolution
interventions to increase the heat tolerance of corals at the early
life-history stages as well as in adults are being tested in the
laboratory and the field (National Academies of Sciences and Medicine,
2019; Reef Restoration and Adaptation Program: Intervention Technical
2019). These interventions may also protect populations of high
importance. Assisted evolution
interventions include selective breeding within species, hybridisation
between species, and microbial manipulations (Chakravarti, Beltran, &
Oppen, 2017; Chan, Peplow, Menéndez, Hoffmann, & van Oppen, 2019;
Damjanovic, Blackall, Webster, & Oppen, 2017; Morgans, Hung, Bourne, &
Quigley, 2019; Quigley, Bay, & van Oppen, 2019; van Oppen, Oliver,
Putnam, & Gates, 2015). The knowledge gained from experimentation of
genetic interventions will facilitate optimisation of breeding designs,
reduce the incidences and impacts of trait trade-offs and the help to
determine the probabilities of success and timeframes associated with
genetic gains.
Improved forecasting of future coral reef health based on the scope and
rates of recovery is urgently needed. This will rely on estimating rates
of acclimatisation and adaptation to predict how populations will
respond to a suite of selective pressures. The incorporation of the
effects of selection and adaptation to understand population
evolutionary trajectories has been applied to the conservation of
species like Eltham’s butterfly and bighorn sheep (Creech et al., 2017;
Roitman et al., 2017). Corals exist close to their thermal limits
(reviewed in Drury, 2019) but exhibit a wide range of phenotypes in
response to heat stress (Ainsworth et al., 2015; Kenkel et al., 2013),
suggestive of a high adaptive capacity predicated on genetic diversity
across populations and species (Matz, Treml, Aglyamova, & Bay, 2018).
There is evidence that corals have increased their heat tolerance by
~0.5°C in the last decade, which suggests substantial
capacity to adapt to increasing temperatures (Sully, Burkepile, Donovan,
Hodgson, & van Woesik, 2019). Part of this heat tolerance can be
attributed to the diversity and relative abundance of dinoflagellate
symbionts (family Symbiodiniaceae) that inhabit coral tissues (Baird,
Bhagooli, Ralph, & Takahashi, 2009; reviewed in Quigley, Baker,
Coffroth, Willis, & van Oppen, 2018). In particular, changes in
symbiont community composition can attribute 1.0-1.5°C of increased
tolerance to adults (Berkelmans & van Oppen, 2006) and 26x increased
tolerance in juvenile corals relative to warm-warm and cool-warm crosses
(Quigley, Randall, van Oppen, & Bay, 2020) and has been found to
explain up to 24% of bleaching variability (Mizerek, Baird, & Madin,
2018). The genomic architecture of heat tolerance is often polygenic
(Bay & Palumbi, 2015; Jin et al., 2016). Multiple candidate genes of
varying effect sizes have been examined, including heat shock proteins
and genes involved in immunity (Louis, Bhagooli, Kenkel, Baker, &
Dyall, 2017), although some target genes may more broadly be associated
with stress tolerance generally and not heat tolerance specifically.
Therefore, to understand corals adaptive capacity, comprehensive
knowledge is needed concerning the variation in alleles at particular
loci and the topology of polymorphic genomic regions. This knowledge can
then be used to understand their influence in driving the emergence of
different phenotypes that ultimately enable adaptation in populations
over ecological and evolutionary time frames.
Evolutionary genetics describes gene frequency changes across
populations and over time. The analysis of genetic diversity in wild and
artificially-bred populations is central to understanding the rates and
potential of adaptation. Shallow and deep whole genome sequencing is now
widely available and relatively cost effective, including sequencing
whole genome single-nucleotide polymorphisms (SNPs) (Davey et al., 2011;
Helyar et al., 2011) and are increasingly illuminating the ecological
and evolutionary mechanisms coral use to respond to their environment
(Dixon et al., 2015; Fuller et al., 2019; Palumbi, Barshis,
Traylor-Knowles, & Bay, 2014). SNPs are particularly valuable for
identifying common variants underlying trait variation and can be
applied to genetic conservation practices through breeding programs that
utilize quantitative genetic principles, breeding values, and narrow and
broad-sense heritability (h2, H2)
(Visscher, Hill, & Wray, 2008). SNPs are intrinsically linked to the
h2 given the proportionality to the product of SNP
quantity and effect size (Holland et al., 2019). This marker-assisted
selection approach identifies markers ultimately underlying the
heritability estimates, although single alleles may explain only a small
proportion of the measured heritable variation (Manolio et al., 2009).
Specifically, SNPs provide the marker data used as inputs for
relatedness models, that when combined with phenotypic data, are used to
calculate additive genetic effects and variances and finally,
heritability and the potential for selection (O’hara, Cano, Ovaskainen,
Teplitsky, & Alho, 2008).
Here we apply high-density
genome-wide marker sequencing to samples collected from selectively bred
reproductive crosses to elucidate how artificially produced corals may
evolve under heat stress. Selective breeding of corals from historically
warmer reefs with others sourced from cooler reefs and then exposing
juveniles to temperature tolerant symbionts like Durusdinium
trenchii significantly improved coral fitness when exposed to 31°C
(e.g. increased survival, growth and bleaching tolerance (Quigley,
Randall, van Oppen, & Bay, 2020)), even upon inspection of a limited
number of crosses produced from only five parents. Here we link those
traits measured in the five reproductive crosses to their underlying
allele frequency changes and genomic contribution (h2)
and identify the putative causative variants separating the five
families to explain and potentially link these heritability estimates at
both ambient and elevated temperatures to explain the genetic variation
in these three quantitative traits.