Negative parental and offspring environmental effects of macroalgae on coral recruitment are linked with alterations in the coral larval microbiome

The persistence of reef-building corals is threatened by macroalgal
competitors leading to a major demographic bottleneck in coral
recruitment. Whether parental effects exist under coral-algal competition
and whether they influence offspring performance via microbiome
alterations represent major gaps in our understanding of the mechanisms by
which macroalgae may hinder coral recovery. We investigated the diversity,
variability and composition of the microbiome of adults and larvae of the
coral Pocillopora acuta and surrounding benthic substrate on algal-removed
and algal-dominated bommies. We then assessed the relative influence of
parental and offspring environmental effects on coral recruitment
processes by reciprocally exposing coral larvae from two parental origins
(algal-removed and algal-dominated bommies) to algal-removed and
algal-dominated environmental conditions. Dense macroalgal assemblages
impacted the microbiome composition of coral larvae. Larvae produced by
parents from algal-dominated bommies were depleted in putative beneficial
bacteria and enriched in opportunistic taxa. These larvae had a
significantly lower survival compared to larvae from algal-removed bommies
regardless of environmental conditions. In contrast, algal-induced
parental and offspring environmental effects interacted to reduce the
survival of coral recruits. Together our results demonstrate negative
algal-induced parental and offspring environmental effects on coral
recruitment that could be mediated by alterations in the offspring
microbiome.