Gene flow is important for maintaining the genetic diversity required for adaptation to environmental disturbances, though gene flow may be limited by site fidelity in small coastal sharks. Bonnethead sharks (Sphyrna tiburo) - a small coastal hammerhead species - demonstrate site fidelity, as females are philopatric while males migrate to mediate gene flow. Consequently, bonnetheads demonstrate population divergence with distance and Atlantic populations are genetically distinct from those of the Gulf of Mexico. Indeed, Florida forms a vicariant zone between these two bodies of water for many marine species, including some sharks. However, while bonnetheads are expected to have limited dispersal, the extent and rate of bonnethead migration remains uncertain. Thus, we aimed to determine their dispersal capacity by evaluating connectivity between disparate populations from the Gulf of Mexico and Atlantic Ocean. Using 10,733 SNPs derived from 2bRAD sequences, we evaluated genetic connectivity between Tampa Bay on the Gulf Coast of Florida and Biscayne Bay on the Atlantic coast of Florida. While standard analyses of genetic structure revealed little differentiation between Tampa Bay and Biscayne Bay populations, demographic history inference based on the site frequency spectrum favored the model with divergence between 2000 - 6000 years ago, with continuous unidirectional gene flow from Tampa Bay to Biscayne Bay. Combined with prior findings of small-scale genetic divergence in bonnethead mitochondrial (female-transmitted) loci, our findings support the hypothesis that female bonnetheads are highly philopatric while male bonnetheads often migrate over relatively large distances (>300 miles) to find mates. Together, these results provide optimism that under proper management, a small-bodied globally Endangered shark can undergo long migrations to sustain genetic diversity.

Coral populations across the Great Barrier Reef (GBR) could rapidly adapt to the warming climate if they have standing genetic variation for thermal adaptation. Here, we describe a locus likely involved in acclimatization and adaptation of Acropora millepora to cooler temperatures at higher latitudes. This locus shows a strong signal of selection in the A. millepora genome, with a steep latitudinal gradient of derived allele frequency, and harbors a cluster of eight tandemly repeated Δ9-desaturase genes adjacent to a region where a hard sweep likely occurred. In colonies reciprocally transplanted across 4.5 degrees of latitude, the expression of Δ9-desaturase was upregulated at the cooler high-latitude reef. Furthermore, corals from the warmer low-latitude reef with one or two copies of the “cold-adapted” Δ9-desaturase allele expressed the gene more and grew faster than their peers when transplanted to the cooler reef. In other organisms ranging from bacteria to fish, Δ9-desaturase is upregulated under cold conditions to adjust membrane fluidity by introducing double bonds into fatty acid chains of membrane lipids. While all these lines of evidence are suggestive rather than conclusive, they collectively make Δ9-desaturase a strong candidate marker gene for coral thermal acclimatization and adaptation.

Global environmental change is rapidly driving deterioration of many ecosystems- such as coral reefs- though the rate of decline could be offset by genetic adaptation. We aimed to identify which environmental gradients drive local adaptation in two common corals across the Florida Keys Reef Tract, Porites astreoides and Agaricia agaricites. Both species contained three genetically distinct lineages distributed across depths in a remarkably similar way. Additionally, each lineage harbored genetic variation that aligned with other environmental gradients. The most commonly highlighted driver of within-lineage genetic structure was temperature during the coldest winter month, which is warmer at offshore sites especially in the upper Keys. Other repeatedly highlighted environmental drivers were high variation in bottom temperature at nearshore sites along the main island chain, more pronounced ocean stratification west of Key West, and outlying values of several water quality parameters (such as dissolved oxygen, carbon, turbidity, and salinity) at nearshore and Florida Bay locations of the lower and middle Keys. Synthesizing these results, we provide a map of adaptive neighborhoods in the Florida Keys that are likely to harbor differentially adapted coral populations, which can be regarded as different genetic stocks from the perspective of reef conservation and restoration.

As climate change progresses, reef-building corals face multiple environmental stressors that they must adapt to. Can corals adapt to all these stressors at the same time, or would some adaptations exclude others (i.e., a genetic tradeoff)? Here, we reanalyzed RNA-seq and Tag-seq data from four studies that compared gene expression in corals from tidal pools of different daily heat stress levels, with varying proximity to a CO2 seep, containing different kinds of algal symbionts, and separated by 15 degrees of latitude. We computed both the genetic divergence (FST) and log-fold expression change per gene for each contrast, and then compared these results to see whether the same genes were involved in adaptation and/or acclimatization to different environmental gradients. We find that genetic divergence patterns are entirely independent from each other (with the exception of just two shared FST outliers between the two cases of CO2 adaptation), while at the gene expression level there is significant overlap in up- and down-regulated genes among multiple environmental contrasts. These results suggest that coral populations maximize their local fitness predominantly via gene expression plasticity (involving similar pathways) rather than through selection-driven genetic divergence. Still, there remains the possibility of highly polygenic adaptation with extensive redundancy (many alternative genetic ways to achieve the same phenotype). Regardless of the mechanism, the overall lack of tradeoffs that we observed here suggests that corals have substantial capacity to withstand multiple simultaneous stressors.

Processes governing genetic diversity and adaptive potential in reef-building corals are of interest both for fundamental evolutionary biology and for reef conservation. Here, we investigated the possibility of “sweepstakes reproductive success” (SRS) in a broadcast spawning coral Acropora hyacinthus at Yap Island, Micronesia. SRS is an extreme yearly variation in the number of surviving offspring among parents. It is predicted to generate genetically differentiated, low genetic diversity recruit cohorts, containing close kin individuals. We have tested these predictions by comparing genetic composition of size classes (adults and juveniles) at several sites on the island of Yap, Micronesia. We did see the genome-wide dip in genetic diversity in juveniles compared to adults at two of the four sites; however, both adults and juveniles varied in genetic diversity across sites, and there was no detectable genetic structure among juveniles, which does not conform to the classical SRS scenario. Yet, we have identified a pair of juvenile siblings at the site where juveniles had the lowest genetic diversity compared to adults, an observation that is hard to explain without invoking SRS. While further support for SRS is needed to fully settle the issue, we show that incorporating SRS into the Indo-West Pacific coral metapopulation adaptation model had surprisingly little effect on mean rates of coral cover decline during warming. Still, SRS notably increases year-to-year variation in coral cover throughout the simulation.

As sea surface temperature increases, many coral species that used to harbor symbionts of the genus Cladocopium have become colonized with the thermally tolerant genus, Durusdinium. Here, we asked how symbionts of one genus react to the presence of another symbiont genus within the same coral host, and what effect this has on the host. We used previously published data from Acropora hyacinthus corals hosting Cladocopium and/or Durusdinium symbionts and looked at gene expression in all three symbiotic partners depending on the relative proportions of symbiont genera within the host. We find that both Cladocopium and Durusdinium change their expression most when their proportions are nearly equal (the state that we call “codominance”): both genera elevate expression of photosynthesis and ribosomal genes, suggesting increase in photosynthesis and growth (i.e. higher productivity). At the same time, the coral host also elevates production of ribosomes suggesting faster cellular growth, and, when heated, shows less pronounced stress response. These results can be explained in two ways. One explanation is that increased competition between symbionts heightens their productivity, which benefits the host, making it more resilient to stress. Alternatively, the symbionts’ elevated productivity might be the consequence of the host being particularly healthy. Under this explanation, rapid growth of the healthy host creates new space, lowering the symbionts’ competition and allowing for codominance. The latter explanation is supported by the fact that codominance is associated with lower symbiont densities. Irrespective of the causation, the presence of mixed symbiont communities could potentially be used as an instant indicator of coral well-being, which would be a useful tool for coral conservation and restoration.

Abstract: Interrogation of chromatin modifications, such as DNA methylation, has potential to improve forecasting and conservation of marine ecosystems. The standard method for assaying DNA methylation (Whole Genome Bisulfite Sequencing), however, is too costly to apply at the scales required for ecological research. Here we evaluate different methods for measuring DNA methylation for ecological epigenetics. We compare Whole Genome Bisulfite Sequencing (WGBS) with Methylated CpG Binding Domain Sequencing (MBD-seq), and a modified version of MethylRAD we term methylation-dependent Restriction site-Associated DNA sequencing (mdRAD). We evaluate these three assays in measuring variation in methylation across the genome, between genotypes, and between polyp types in the reef-building coral Acropora millepora. We find that all three assays measure absolute methylation levels similarly, with tight correlations for methylation of gene bodies (gbM), as well as exons and 1Kb windows. Correlations for differential gbM between genotypes were weaker, but still concurrent across assays. We detected little to no reproducible differences in gbM between polyp types. We conclude that MBD-seq and mdRAD are reliable cost-effective alternatives to WGBS. Moreover, the considerably lower sequencing effort required for mdRAD to produce comparable methylation estimates makes it particularly useful for ecological epigenetics.

Interrogation of chromatin modifications, such as DNA methylation, has potential to improve forecasting and conservation of marine ecosystems. The standard method for assaying DNA methylation (Whole Genome Bisulfite Sequencing), however, is too costly to apply at the scales required for ecological research. Here we evaluate different methods for measuring DNA methylation for ecological epigenetics. We compare Whole Genome Bisulfite Sequencing (WGBS) with Methylated CpG Binding Domain Sequencing (MBD-seq), and a modified version of MethylRAD we term methylation-dependent Restriction site-Associated DNA sequencing (mdRAD). We evaluate these three assays in measuring variation in methylation across the genome, between genotypes, and between polyp types in the reef-building coral Acropora millepora. We find that all three assays measure absolute methylation levels similarly, with tight correlations for methylation of gene bodies (gbM), as well as exons and 1Kb windows. Correlations for differential gbM between genotypes were weaker, but still concurrent across assays. We detected little to no reproducible differences in gbM between polyp types. We conclude that MBD-seq and mdRAD are reliable cost-effective alternatives to WGBS. Moreover, the considerably lower sequencing effort required for mdRAD to produce comparable methylation estimates makes it particularly useful for ecological epigenetics.