Extensive transcriptional variation poses a challenge to thermal stress biomarker development for endangered corals

Abstract

As climate changes, sea surface temperature anomalies that negatively impact coral reef organisms continue to increase in frequency and intensity. Yet, despite widespread coral mortality, genetic diversity remains high even in those coral species listed as threatened. While this is good news in many ways it presents a challenge for the development of biomarkers that can identify resilient or vulnerable genotypes. Taking advantage of three coral restoration nurseries in Florida that serve as long-term common garden experiments, we exposed over thirty genetically distinct Acropora cervicornis colonies to hot and cold temperature shocks seasonally and measured pooled gene expression responses using RNAseq. Targeting a subset of twenty genes, we designed a high-throughput qPCR array to quantify expression in all individuals separately under each treatment with the goal of identifying thermal stress biomarkers. We observed extensive transcriptional variation in the population, suggesting abundant raw material is available for adaptation via natural selection. However, this high variation made it difficult to correlate gene expression changes with colony performance metrics such as growth, mortality, and bleaching susceptibility. Nevertheless, we identified several promising biomarkers for acute thermal stress that may improve coral restoration and climate change mitigation efforts in the future.

Genotype by environment interactions in coral bleaching

“…Learning methods may offer substantial advantages for ecological genetics [66] as they have in biomedical research, potentially increasing the predictive power of more traditional methods, such as using polygenic scores and linear models [25]. This strategy also de-emphasizes the importance of individual loci, which may be useful for overcoming the difficulties of developing biomarkers that are highly variable [67]. We only consider our residual prediction to be generalizable to this species in this population, but it serves to illustrate how genetic data can be used to generate 'confidence intervals' about the average likelihood of success in an unknown environment.…”

Increasing comparability among coral bleaching experiments

“…Temperature profiles of acute and short‐term heat‐stress experiments are either of a heat‐pulse or a heat‐hold design (Fig. 2; Mayfield et al 2011, Parkinson et al 2018, Morikawa and Palumbi 2019, Voolstra et al 2020). Heat‐pulse experiments are often designed to mimic natural temperature fluctuations over diel cycles, across tidal cycles, and during internal wave or upwelling events, but may also be used to rapidly test the response of corals to a range of elevated temperatures that are not typically recorded in a natural setting (Fig.…”

“…For example, there may be measurable differences in performance among genets when comparing the performance of their ramets (i.e., fragments, asexually produced, originating from the same genet) in different experimental conditions (Appendix : Fig. S1; Box 1) (Parkinson et al 2018, Muller et al 2018, Jury and Toonen 2019, Morikawa and Palumbi 2019, Wright et al 2019, Voolstra et al 2020). Investigating multiple ramets of the same genet across treatments allows for a more direct inference of treatment effects.…”

Molecular tools for coral reef restoration: Beyond biomarker discovery

“…Coral molecular biomarker discovery is not currently a bottleneck: many putative markers have already been proposed (Bay & Palumbi, 2014Downs, Mueller, Phillips, Fauth, & Woodley, 2000;Downs, Fauth, et al, 2005;Jin et al, 2016;Kenkel et al, 2011Kenkel et al, , 2014Lundgren, Vera, Peplow, Manel, & van Oppen, 2013;Parkinson et al, 2018;Wright et al, 2017). Furthermore, given the substantial progress in the field of coral ecological genomics, additional candidates could be identified through a larger meta-analysis of currently published studies that quantify both 'omic markers and phenotypes of interest.…”

“…Expression biomarkers have progressed furthest in terms of overall development, and have been investigated in the context of both diagnostic and predictive capacities for a variety of phenotypes in the coral host, and to a lesser extent in the algal symbiont (reviewed by Louis, Bhagooli, Kenkel, Baker, & Dyall, 2017). Barriers specific to gene expression biomarkers include the inherent variability of transcription over time and within colonies (Mayfield, Hsiao, Fan, & Chen, 2012;Parkinson et al, 2018); additional work is needed to understand how to control for these variables. Preliminary work has addressed barriers related to transferability and simplicity of assay design (Kenkel et al, 2011;Wright et al, 2017) and further progress in these areas will be facilitated by basic research, especially with high-throughput methods.…”