Theory suggests that the direct transmission of beneficial endosymbionts (mutualists) from parents to offspring (vertical transmission) in animal hosts is advantageous and evolutionarily stable, yet many host species instead acquire their symbionts from the environment (horizontal acquisition). An outstanding question in marine biology is why some scleractinian corals do not provision their eggs and larvae with the endosymbiotic dinoflagellates that are necessary for a juvenile's ultimate survival. We tested whether the acquisition of photosynthetic endosymbionts (family Symbiodiniaceae) during the planktonic larval stage was advantageous, as is widely assumed, in the ecologically important and threatened Caribbean reef-building coral Orbicella faveolata. Following larval acquisition, similar changes occurred in host energetic lipid use and gene expression regardless of whether their symbionts were photosynthesizing, suggesting the symbionts did not provide the energetic benefit characteristic of the mutualism in adults. Larvae that acquired photosymbionts isolated from conspecific adults on their natal reef exhibited a reduction in swimming, which may interfere with their ability to find suitable settlement substrate, and also a decrease in survival. Larvae exposed to two cultured algal species did not exhibit differences in survival, but decreased their swimming activity in response to one species. We conclude that acquiring photosymbionts during the larval stage confers no advantages and can in fact be disadvantageous to this coral host. The timing of symbiont acquisition appears to be a critical component of a host's life history strategy and overall reproductive fitness, and this timing itself appears to be under selective pressure.
Abstract Evolutionary tradeoffs between life-history strategies are central to animal evolution. However, because microbes can influence aspects of host physiology, behavior, and resistance to stress or disease, changes in animal-microbial symbioses have the potential to mediate life-history tradeoffs. Scleractinian corals provide a highly biodiverse and data-rich host system to test this idea, made more relevant by increases in coral disease outbreaks as a result of anthropogenic changes to climate and reef ecosystems. Identifying factors that determine coral disease susceptibility has therefore become a focus for reef conservation efforts. Using a comparative approach, we tested if coral microbiomes correlate with disease susceptibility across 425 million years of coral evolution by combining a cross-species coral microbiome survey (the “Global Coral Microbiome Project”) with long-term disease prevalence data at multiple sites. Interpreting these data in their phylogenetic context, we show that microbial dominance and composition predict disease susceptibility. We trace this dominance-disease association to a single putatively beneficial bacterial symbiont, Endozoicomonas, whose relative abundance in coral tissue explained 30% of variation in disease susceptibility and 60% of variation in microbiome dominance across 40 coral genera. Conversely, Endozoicomonas abundances in coral tissue strongly correlated with high growth rates. These results demonstrate that the evolution of microbial symbiosis in corals correlates with both disease prevalence and growth rate. Exploration of the mechanistic basis for these findings will be important for our understanding of how microbial symbiosis influences animal life-history tradeoffs, and in efforts to use microbes to increase coral growth or disease resistance in-situ.
Tropical reef-building corals exist in intimate symbiosis with diverse microbes and viruses. Coral microbiomes are generally much less diverse than their environment, but across studied corals, the biodiversity of these microbiomes varies greatly. It has previously been hypothesized that differences in coral innate immunity in general, and the copy number of TIR-domain containing innate immune genes in particular, may drive interspecific differences in microbiome structure. Despite many existing studies of coral microbiomes, this hypothesis has previously been difficult to test due to a lack of consistently collected cross-species data on coral microbiomes. In this manuscript, we reannotate TIR-domain containing genes across diverse coral genomes, and use phylogenetic comparative methods to compare these innate immune gene copy numbers against 16S rRNA marker gene data on coral mucus, tissue, and skeleton microbiomes from the Global Coral Microbiome Project (GCMP). The copy number of Toll-like receptor (TLRs) and Interleukin-1 receptor (IL-1Rs) gene families, as well as the total genomic count of their constituent domains (LRR and TIR domains; and Ig and TIR domains, respectively), explained most interspecific differences in microbiome richness and beta-diversity among corals with sequenced genomes. We find that these correlations are also anatomically specific, with an especially strong correlation between IL-1R gene copy numbers and microbiome richness in the coral’s endolithic skeleton. Together, these results suggest innate immunity may play a key role in sculpting microbiome structure in corals.