Enhanced gene expression plasticity as a mechanism of adaptation to a variable environment in a reef-building coral

Abstract

Local adaptation is ubiquitous, but the molecular mechanisms giving rise to this ecological phenomenon remain largely unknown. A year-long reciprocal transplant of mustard hill coral (Porites astreoides) between a highly environmentally variable inshore habitat and more stable offshore habitat demonstrated that both inshore and offshore populations exhibit elevated growth, protein and lipid content in their home reef environment, indicative of local adaptation. Here, we characterized the genomic basis of this adaptation in both coral hosts and their intracellular algal symbionts (Symbiodinium sp.) using genome-wide gene expression profiling and gene coexpression network analysis. Inshore and offshore coral populations differ primarily in their capacity for gene expression plasticity: upon transplantation to a novel environment inshore corals were able to match expression profiles of the local population significantly better than offshore corals. Furthermore, elevated plasticity in expression of environmental stress response (ESR) genes was adaptive in the inshore environment: it correlated with the least susceptibility to a natural summer bleaching event, whereas higher constitutive ESR gene expression ("frontloading" sensu Barshis et al. 2013) did not. Our results reveal a novel genomic mechanism of resilience to a variable environment, demonstrating that corals are capable of a more diverse molecular response to environmental stress than previously thought.