Genetic Variation in Heat Tolerance of the Coral Platygyra Daedalea Indicates Potential for Adaptation to Ocean Warming

Abstract

Ocean warming represents the greatest threat to the persistence of reef ecosystems. Most coral populations are projected to experience temperatures above their current bleaching thresholds annually by 2050. Adaptation to higher temperatures is necessary if corals are to persist in a warming future. While many aspects of heat stress have been well studied, few data are available for predicting the capacity for adaptive cross-generational responses in corals. Consistent sets of heat tolerant genomic markers that reliably predict thermal tolerance have yet to be identified. To address this knowledge gap, we quantified the heritability and genetic variation associated with heat tolerance in Platygyra daedalea from the Great Barrier Reef. We tracked the survival of ten quantitative genetic crosses of larvae produced form six parental colonies in a heat tolerance selection experiment. We also identified allelic shifts in heat-selected (35°C) survivors compared with paired, non-selected controls (27°C). The narrow-sense heritability of survival under heat stress was 0.66 and a total of 1,069 single nucleotide polymorphisms (SNPs) were associated with different survival probabilities. While 148 SNPs were shared between several experimental crosses, no common SNPs were identified for all crosses, which suggests that specific combinations of many markers are responsible for heat tolerance. However, we found two regions that overlap with previously identified loci associated with heat tolerance in Persian Gulf populations of P. daedalea, which reinforces the importance of these markers for heat tolerance. These results illustrate the importance of high heritability and the complexity of the genomic architecture underpinning host heat tolerance. These findings suggest that this P. daedalea population has the genetic prerequisites for adaptation to increasing temperatures. This study also provides knowledge for the development of high throughput genomic tools which may screen for variation within and across populations to enhance adaptation through assisted gene flow and assisted migration.

Screening for climate adaptative loci using seascape genomics resolves phenotypic variation in heat tolerance of the coral Acropora millepora.

“…Interactions between loci (e.g. antagonist, synergistic, neutral) as well as functional redundancy between genomic regions or with other holobiont partners 57 , may also explain why direction of changes in allele frequencies are not necessarily consistent with changes in phenotypic response 43 . The thermal tolerance benefit arising from having a certain allele may therefore depends on allelic combinations at many other loci as well as transcriptional and post-transcriptional regulation such as epigenetics 33 .…”

“…Despite evidences of contemporary increases in coral heat tolerance 40,41 , whether or not genetic adaptation through natural selection of beneficial host and symbiont traits can keep pace with global warming is still unknown. It depends in particular on several parameters that are undetermined in most taxa such as heat tolerance heritability [42][43][44] , selection differential 43 , covariance between traits 45 and potential tradeoffs 46,47 . Identifying genetic markers involved in heat tolerance and understanding their distribution through time and space is therefore crucial to predict the future of coral reefs [48][49][50][51][52] as well as targeting tolerant populations and individuals for conservation 53,54 and restoration 44,55,56 .…”

Climate adaptive loci revealed by seascape genomics corroborate phenotypic variation in heat tolerance of the coral Acropora millepora

“…Heat tolerance in corals is polygenic, thus driven by many loci of small effect size 36 , with possible epistasis (e.g., antagonist, synergistic, neutral) and functional redundancy between genomic regions and with other holobiont partners 61 . This may explain why direction of changes in allele frequencies are not necessarily consistent with changes in phenotypic response 45 . The thermal tolerance bene t arising from having a certain allele at a HAL may therefore depend on allelic combination at many other loci as well as transcriptional and post-transcriptional regulation such as epigenetics 34 .…”

“…Despite evidences for contemporary increases in coral heat tolerance [41][42][43] , whether or not genetic adaptation through natural selection of bene cial host and symbiont traits can keep pace with global warming is still unknown. It depends in particular on several parameters that are undetermined in most taxa such as heat tolerance heritability [44][45][46] , selection differential 45 , covariance between traits (e.g., growth and symbiont retention) 47 and potential tradeoffs 48,49 . Identifying genetic markers involved in heat tolerance and understanding their distribution through time and space is therefore crucial to predict the future of coral reefs [50][51][52][53][54] as well as targeting tolerant populations and individuals for conservation [55][56][57][58] and restoration 46,59,60 .…”

“…Identifying genetic markers involved in heat tolerance and understanding their distribution through time and space is therefore crucial to predict the future of coral reefs [50][51][52][53][54] as well as targeting tolerant populations and individuals for conservation [55][56][57][58] and restoration 46,59,60 . Some studies have begun to identify host genomic markers associated with heat tolerance using various methods including differential gene expression analysis in adults 31,61,62 and larvae 37 under heat stress, associations between allele frequencies and larval survival under thermal stress 45,46 and population genomics to identify signals of genetic differentiation associated with distinct thermal histories 39,40,63 .…”