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 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.