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

Abstract

One of the main challenges in coral reef conservation and restoration is the identification of coral populations resilient under global warming. Seascape genomics is a powerful tool to uncover genetic markers potentially involved in heat tolerance among large populations without prior information on phenotypes. Here, we aimed to confirm the role of several candidate heat associated loci identified using this method in driving the phenotypic response of Acropora millepora from New Caledonia to thermal stress. We subjected 7 colonies to a long-term ex-situ heat stress assay (4°C above the Maximum Monthly Mean) and investigated their physiological response along with their Symbiodiniaceae communities and genotypes. Despite having similar thermal histories and associated symbionts, these conspecific individuals differed greatly in their tolerance to heat stress. More importantly, the clustering of individuals based on their alleles at the candidate loci was able to resolve most of the phenotypic variation in heat tolerance. Colonies harboring a higher proportion of beneficial alleles sustained on average lower mortality, higher Symbiodiniaceae/chlorophyll concentrations and photosynthetic efficiency under prolonged heat stress. Together these results support the relevance of seascape genomics to reveal candidate loci for heat adaptation in corals and develop predictive models of heat tolerance.

Environmental, host, and symbiont drivers of heat tolerance in a species complex of reef-building corals

“…Our results follow recent applications of standardized acute heat stress experiments to quantify population thermal thresholds (Cunning et al, 2021;Evensen et al, 2022;Marzonie et al, 2023;Nielsen et al, 2022;Voolstra et al, 2021), extend this approach to colony-level applications (Cunning et al, 2021;Klepac et al, 2023), and is the first to quantify individuallevel thresholds across environmental gradients in wild populations (but see Denis et al, 2024).…”

“…spathulata in a parallel study (Denis et al, 2024) and in other non-acroporid species (Evensen et al, 2022;Howells et al, 2016;Marzonie et al, 2023;Woolsey et al, 2015), highlighting the potential for high latitude populations to serve as refugia as sea temperatures continue to rise.…”

“…Further, more extreme heat stress would likely have opposite effects of mild heat stress and instead exacerbate damage to coral during subsequent experimental stress (Ainsworth et al, 2016;Denis et al, 2024). As heat tolerance varies with recent environmental conditions, acclimatization to these conditions may complicate understanding of heritable phenotypic variation available for natural or assisted evolution.…”

“…This method allows rapid high-throughput phenotyping of corals and has been shown to measure relative differences in heat tolerance between sites and among individuals in a short term assay (18 hours) comparable to a longer-term assay (21 days; Klepac et al, 2023;Voolstra et al, 2020). To date, six other studies have been published using experimental aquaria to generate an ED50 metric based on Fv/Fm measurements to compare thermal thresholds among populations (Evensen et al, 2022;Marzonie et al, 2023;Voolstra et al, 2021), among individuals in nurserybred colonies (Cunning et al, 2021;Klepac et al, 2023), or among and within wild reef populations (Denis et al, 2024). Previous work has shown agreeability in heat tolerance rankings among nursery-bred colonies during two seasons in the same year (Cunning et al, 2021) and with bleaching resistance during a natural bleaching event (Morikawa & Palumbi, 2019), but further work is required to conclude that experimental heat tolerance responses are consistent across time and are indicative of survival during bleaching events.…”