Intrapopulation adaptive variance supports selective breeding in a reef-building coral

Abstract

The long-term persistence of coral reefs under climate change requires heritable drivers of thermal tolerance which support adaptation. The genomic basis of thermal tolerance has been evaluated across strong spatial and environmental gradients, but this variation also exists within populations due to neutral evolutionary processes. Small scale heterogeneity in coral bleaching is ubiquitous, so we used corals from a single reef to examine genomic signatures of bleaching performance, their biochemical correlates and the downstream consequences of selective breeding. In the absence of directional selection due to environmental differences, adult corals from a single population exhibit strong genomic patterns related to natural bleaching tolerance and symbiosis state, including functional differentiation in signaling pathways, protein and amino acid modification and metabolism. Conversely, growth, development and innate immune responses did not distinguish bleaching tolerance in adult corals. The genomic signatures of these gene ontologies influence biochemical patterns in healthy corals, primarily via cell-signaling pathway impacts on peptides and amino acids. Thermal tolerance in this population is highly heritable, with significantly higher survivorship under temperature stress in larvae and juveniles reared from thermally tolerant parents than those from sensitive parents. Using a select and re-sequence approach, certain gene ontologies were reproducibly impacted, while antioxidant activity and cell signaling ontologies were disproportionately selected in thermally tolerant corals, demonstrating the genomic drivers of successful selective breeding. These data show that intrapopulation variance in the absence of historical selection supports the adaptive capacity of coral reefs under climate change.

Transcriptomic plasticity and symbiont shuffling underpin Pocillopora acclimatization across heat-stress regimes in the Pacific Ocean

“…In other cases, rapid thermal acclimation is achieved through altered gene expression in the host and/or symbiont (i.e., transcriptomic plasticity) resulting in increased whole organism (holobiont) thermal tolerance (Kenkel and Matz 2017;Savary et al 2021). Coral holobiont thermal sensitivity is therefore dependent on an array of interacting drivers, including environmental history (Middlebrook et al 2008;Safaie et al 2018;Schoepf et al 2020;Wall et al 2021;Savary et al 2021), endosymbiont community composition (Hoadley et al 2019;Qin et al 2019;Cunning and Baker 2020;Dilworth et al 2021), and host genotype (Barshis et al 2013;Dilworth et al 2021;Drury et al 2021). However, the relative role of each of these factors in determining holobiont expression in situ remains poorly resolved.…”

Genetic variation in heat tolerance of the coral Platygyra daedalea indicates potential for adaptation to ocean warming

“…For the subset of significant tags shared among crosses, 9 markers could be unambiguously assigned to a position in the transcriptome all of which were annotated (Table 5). Furthermore, two of these tags which were identified in three crosses were annotated as genes previously implicated in heat tolerance Monocarboxylate transporter 10 (K1PRR1) and Isocitrate dehydrogenase subunit 1 (E9C6G6) (Table 5) (Drury et al, 2021; Kenkel et al, 2013; Pathmanathan et al, 2021; Polato et al, 2010). In two tags that mapped to transcripts and overlapped in other crosses, we found consistent decrease in the major allele for the Monocarboxylate transporter and consistent increase of the major allele for the isocitrate dehydrogenase subunit (Table 5).…”

“…Three coral crosses had a SNP in the Krebs cycle enzyme isocitrate dehydrogenase (IDH) and a monocarboxylate transporter both of which are associated with this annotation. These proteins have been identified in gene expression studies as important to the coral thermal stress response (Drury et al, 2021; Kenkel et al, 2013; Pathmanathan et al, 2021; Polato et al, 2010). IDH participates in reducing reactive oxygen species and is one of the 44 proteins identified as the minimal stress proteome (Kultz, 2005).…”

“…The monocarboxylate transporter moves lactate, pyruvate, and ketone bodies across plasma membranes, thus it is associated with the regulation of metabolism (Halestrap, 2012). This transporter has been identified as important in recent coral heat stress studies and is upregulated under heat stress (Drury et al, 2021; Pathmanathan et al, 2021). The SNPs in IDH and the monocarboxylate transporter associated with heat tolerance in this study further strengthens their proposed role in the thermal stress response in corals.…”

Challenges of sperm cryopreservation in transferring heat adaptation of corals across ocean basins

“…Selective breeding of corals can be applied to accelerate adaptation by increasing the frequency of heat-tolerance alleles in target populations and as such enhance thermal tolerance traits ( Van Oppen et al, 2015 ; Voolstra et al, 2021 ). This involves cross-breeding individuals from a target population with heat tolerant genotype(s) sourced from the same ( Drury et al, 2021 ; Humanes et al, 2021 ) or a different population, typically from a warmer location ( Dixon et al, 2015 ; Howells et al, 2021 ; Quigley et al, 2020 ). When information on individual genotypes and phenotypes is unknown, cross-breeding with corals from a warmer location can enhance heat tolerance.…”