Heritable variation in bleaching responses and its functional genomic basis in reef-building corals (Orbicella faveolata)

Abstract

Reef-building corals are highly sensitive to rising ocean temperatures, and substantial adaptation will be required for corals and the ecosystems they support to persist in changing ocean conditions. Genetic variation that might support adaptive responses has been measured in larval stages of some corals, but these estimates remain unavailable for adult corals and the functional basis of this variation remains unclear. In this study, we focused on the potential for adaptation in Orbicella faveolata, a dominant reef-builder in the Caribbean. We conducted thermal stress experiments using corals collected from natural populations in Bocas del Toro, Panama, and used multilocus SNP genotypes to estimate genetic relatedness among samples. This allowed us to estimate narrow-sense heritability of variation in bleaching responses, revealing that variation in these responses was highly heritable (h2=0.58). This suggests substantial potential for adaptive responses to warming by natural populations of O. faveolata in this region. We further investigated the functional basis for this variation using genomic and transcriptomic approaches. We used a publicly available genetic linkage map and genome assembly to map markers associated with bleaching responses, identifying twelve markers associated with variation in bleaching responses. We also profiled gene expression in corals with contrasting bleaching phenotypes, uncovering substantial differences in transcriptional stress responses between heat-tolerant and heat-susceptible corals. Together, our findings contribute to the growing body of evidence that natural populations of corals possess genetic variation in thermal stress responses that may potentially support adaptive responses to rising ocean temperatures.

Role of host genetics and heat‐tolerant algal symbionts in sustaining populations of the endangered coral Orbicella faveolata in the Florida Keys with ocean warming

“…This means that host genetics factor into the resultant symbiont assemblages even when larvae do not acquire symbionts maternally. Our heritability estimates for bleaching resistance and the proportion of D. trenchii in the symbiont population were high, as were values obtained in a heat stress experiment on O. faveolata (Dziedzic, Elder, & Meyer, ). This suggests that the potential for adaptive responses to warming in O. faveolata do exist, but more work is required to better understand the real‐world ramifications of these heritability estimates relative to the rate and magnitude of present‐day warming and environmental degradation.…”

Resilience in reef‐building corals: The ecological and evolutionary importance of the host response to thermal stress

“…A selection experiment on larvae from parental crosses on the GBR also showed significant, reproducible changes in allele frequencies after larval cultures had undergone mortality related to temperature (Dixon et al, ), indicating selection against certain paternal haplotypes. Survivorship duration under ongoing heat stress also varies dramatically by genotype, where certain SNPs are strongly correlated with highly heritable differences in tolerance in Orbicella faveolata (Dziedzic, Elder, Tavalire, & Meyer, ). Another study of 18 populations of Acropora millepora along the GBR found allele frequencies in antioxidant genes correlated with temperature (Jin et al, ) and a similar study in several species targeting SNPs putatively related to thermal tolerance found that some were significantly correlated with temperature, suggesting they may be selected by the coral's environment (Lundgren, Vera, Peplow, Manel, & van Oppen, ).…”

“…Standing variation in coral populations has been resolved in studies both within and among populations for many species (Ayre & Hughes, , ; Barshis et al, ; Baums, Boulay, Polato, & Hellberg, ; Baums, Johnson, Devlin‐Durante, & Miller, ; Baums, Miller, & Hellberg, , ; Bay & Palumbi, ; Cros, Toonen, Davies, & Karl, ; Davies, Treml, Kenkel, & Matz, ; Dixon et al, ; Drury et al, ; Drury, Schopmeyer, et al, ; Dziedzic et al, ; Hemond & Vollmer, ; Howells et al, ; Kenkel, Goodbody‐Gringley, et al, ; Rippe et al, ; Serrano et al, , ; Smith‐Keune & van Oppen, ; Vollmer & Palumbi, ). Although these differences are putatively neutral, they are indicative of the genetic mosaic that most coral reefs represent.…”

The active spread of adaptive variation for reef resilience

“…Genetic diversity describes the level of variation in genetic regions (polymorphic loci) and among individuals within populations. While there are a number of candidate adaptive loci (Kenkel et al, 2014), and particularly those loci correlated with thermal tolerance (Dixon et al, 2015;Dziedzic, Elder, Tavalire, & Meyer, 2019;Jin et al, 2016), more work is needed to ground truth these putatively adaptive loci (PALs). Adaptive diversity is a subset of total genetic diversity and describes variants of genes that are directly associated with tolerance and survival (adaptive loci; Ahrens et al, 2018).…”