Genomic and transcriptomic signals of thermal tolerance in heat‐tolerant corals (Platygyra daedalea) of the Arabian/Persian Gulf

Abstract

Scleractinian corals occur in tropical regions near their upper thermal limits and are severely threatened by rising ocean temperatures. However, several recent studies have shown coral populations can harbour genetic variation in thermal tolerance. Here, we have extended these approaches to study heat tolerance of corals in the Persian/Arabian Gulf, where heat‐tolerant local populations experience extreme summer temperatures (up to 36°C). To evaluate whether selection has depleted genetic variation in thermal tolerance, estimate potential future adaptive responses and understand the functional basis for these corals’ unusual heat tolerance, we conducted controlled crosses in the Gulf coral Platygyra daedalea. Heat tolerance is highly heritable in this population (h 2 = 0.487–0.748), suggesting substantial potential for adaptive responses to selection for elevated temperatures. To identify genetic markers associated with this variation, we conducted genomewide SNP genotyping in parental corals and tested for relationships between paternal genotype and offspring thermal tolerance. Resulting multilocus SNP genotypes explained a large fraction of variation in thermal tolerance in these crosses (69%). To investigate the functional basis of these differences in thermal tolerance, we profiled transcriptional responses in tolerant and susceptible families, revealing substantial sire effects on transcriptional responses to thermal stress. We also studied sequence variation in these expressed sequences, identifying alleles and functional groups of differentially expressed genes associated with thermal tolerance. Our findings demonstrate that corals in this population harbour extensive genetic variation in thermal tolerance, and heat‐tolerant phenotypes differ in both gene sequences and transcriptional stress responses from their susceptible counterparts.

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

“…This tolerance arises from many genes of small effect (multilocus adaptation) and suggests that the lack of fixed differences mean there are tradeoffs to thermal tolerance. Similarly, Kirk et al () found 131 loci in Platygyra daedalea that were correlated with larval thermal tolerance, but that effect sizes were small, supporting the multilocus model for heat tolerance. Rose, Bay, Morikawa, and Palumbi () also documented polymorphisms associated with thermal tolerance between cryptic species and found expression quantitative trait loci (eQTLs) in the study populations.…”

“…The authors found that the transcriptomic responses to thermal stress of parents and offspring were broadly similar and demonstrated that maternal input was more important than paternal, but that having both parents from thermally tolerant populations further improved heat tolerance and accounted for 87% of deviance in larval survival under stress (Dixon et al, 2015). A similar result in heat stressed larvae of Platygyra daedalea showed that heat tolerance is highly heritable, with paternal genotype explaining ~70% of variation in thermal tolerance (Kirk, Howells, Abrego, Burt, & Meyer, 2018).…”

“…Additional evidence suggests that extracellular matrix proteins, cytoskeletal changes and calcium signaling are frequently impacted (Barshis et al, ; DeSalvo et al, ; Kaniewska et al, ; Kenkel et al, ; Pinzón et al, ; Polato et al, ; Portune, Voolstra, Medina, & Szmant, ; Rosic et al, ) and under severe stress, apoptotic and DNA damage/repair pathways are typically also upregulated (Davies et al, ; Maor‐Landaw et al, ; Seneca & Palumbi, ; Voolstra et al, ). The unfolded protein response, a conserved set of signaling pathways that are activated when unfolded proteins accumulate, is also typically involved (Hou et al, ; Kirk et al, ; Maor‐Landaw et al, ; Ruiz‐Jones & Palumbi, ; Thomas & Palumbi, ). Some evidence also shows that the host can regulate the translational response to heat stress through microRNAs (Gajigan & Conaco, ), which are differentially expressed during a stress test and serve to repress certain mRNA targets.…”

“…Although these differences are putatively neutral, they are indicative of the genetic mosaic that most coral reefs represent. Some variation has also been linked to differences in thermal tolerance across temperature gradients (Bay & Palumbi, ; Dixon et al, ; Howells et al, ; Jin et al, ; Kenkel et al, ; Kirk et al, ; Smith‐Keune & van Oppen, ). This variation (standing or created by novel mutations) is needed for additional adaptive capacity regardless of past selective pressure that may have produced it, but it could also influence heritable traits that have adaptive value.…”

Molecular tools for coral reef restoration: Beyond biomarker discovery

“…High‐throughput methods used to identify such biomarkers include whole genome/transcriptome sequencing and resequencing, genotyping by sequencing, restriction‐site associated DNA (RAD) sequencing, and amplicon sequencing (reviewed by Matz, ). One benefit of investing in the downstream development of genomic markers is that many studies aimed at uncovering the genomic basis of adaptive trait variation in corals have already identified putative markers for further development (e.g., Bay & Palumbi, , ; Dixon et al., ; Jin et al., ; Kirk, Howells, Abrego, Burt, & Meyer, ; Kitchen et al., ; Lundgren et al., ). Additionally, DNA sequences are more fixed than any other type of biomarker, and are therefore the most amenable to predictive assays.…”