Transgenerational inheritance of shuffled symbiont communities in the coral Montipora digitata

Abstract

Adult organisms may \"prime\" their offspring for environmental change through a number of genetic and non-genetic mechanisms, termed parental effects. Some coral species can alter their thermal tolerance by shuffling the proportions of Symbiodinium types within their endosymbiotic communities, but it is unclear if this plasticity can be transferred to offspring in corals that have maternal symbiont transmission. We evaluated symbiont community composition in tagged colonies of Montipora digitata from Orpheus Island, Australia, over two successive annual spawning seasons, the second of which overlapped with the 2016 mass coral bleaching event on the Great Barrier Reef. We applied amplicon sequencing of the ITS2 locus to samples of four families (parent colonies and 10-12 eggs per family) to characterize their potential for symbiont shuffling and to determine if shuffled abundances were preserved in gametes. Symbiont cell densities and photochemical efficiencies of the symbionts photosystem II differed significantly among adults in 2016, suggesting differential responses to increased temperatures. Although abundances of the dominant symbiont haplotype, a representative of clade C15, did not differ among families or over time, low-abundance (\"background\") ITS2 types differed more among years (2015 vs. 2016) than between life stages (parent vs. offspring). Results indicate that background symbiont shuffling can occur in a canonically stable symbiosis, and that such plastic changes to the symbiont community are heritable. To our knowledge, this is the first evidence that shuffled Symbiodinium communities can be inherited by early life-history stages and supports the hypothesis that plastic changes in microbial communities may serve as a mechanism of rapid coral acclimation to changing environmental conditions.