Reef‐building corals are highly sensitive to rising ocean temperatures, and substantial adaptation will be required for corals and the ecosystems they support to persist in changing ocean conditions. Genetic variation that might support adaptive responses has been measured in larval stages of some corals, but these estimates remain unavailable for adult corals and the functional basis of this variation remains unclear. In this study, we focused on the potential for adaptation in Orbicella faveolata, a dominant reef‐builder in the Caribbean. We conducted thermal stress experiments using corals collected from natural populations in Bocas del Toro, Panama, and used multilocus SNP genotypes to estimate genetic relatedness among samples. This allowed us to estimate narrow‐sense heritability of variation in bleaching responses, revealing that variation in these responses was highly heritable (h2 = 0.58). This suggests substantial potential for adaptive responses to warming by natural populations of O. faveolata in this region. We further investigated the functional basis for this variation using genomic and transcriptomic approaches. We used a publicly available genetic linkage map and genome assembly to map markers associated with bleaching responses, identifying twelve markers associated with variation in bleaching responses. We also profiled gene expression in corals with contrasting bleaching phenotypes, uncovering substantial differences in transcriptional stress responses between heat‐tolerant and heat‐susceptible corals. Together, our findings contribute to the growing body of evidence that natural populations of corals possess genetic variation in thermal stress responses that may potentially support adaptive responses to rising ocean temperatures.

Reef-building corals are highly sensitive to rising ocean temperatures, and substantial adaptation will be required for corals and the ecosystems they support to persist in changing ocean conditions. Genetic variation that might support adaptive responses has been measured in larval stages of some corals, but these estimates remain unavailable for adult corals and the functional basis of this variation remains unclear. In this study, we focused on the potential for adaptation in Orbicella faveolata, a dominant reef-builder in the Caribbean. We conducted thermal stress experiments using corals collected from natural populations in Bocas del Toro, Panama, and used multilocus SNP genotypes to estimate genetic relatedness among samples. This allowed us to estimate narrow-sense heritability of variation in bleaching responses, revealing that variation in these responses was highly heritable (h2=0.58). This suggests substantial potential for adaptive responses to warming by natural populations of O. faveolata in this region. We further investigated the functional basis for this variation using genomic and transcriptomic approaches. We used a publicly available genetic linkage map and genome assembly to map markers associated with bleaching responses, identifying twelve markers associated with variation in bleaching responses. We also profiled gene expression in corals with contrasting bleaching phenotypes, uncovering substantial differences in transcriptional stress responses between heat-tolerant and heat-susceptible corals. Together, our findings contribute to the growing body of evidence that natural populations of corals possess genetic variation in thermal stress responses that may potentially support adaptive responses to rising ocean temperatures.

No abstract

Genomic methods are powerful tools for studying evolutionary responses to selection, but the application of these tools in non-model systems threatened by climate change has been limited by the availability of genomic resources in those systems. High-throughput DNA sequencing has enabled development of genome and transcriptome assemblies in non-model systems including reef-building corals, but the fragmented nature of early draft assemblies often obscures the relative positions of genes and genetic markers, and limits the functional interpretation of genomic studies in these systems. To address this limitation and improve genomic resources for the study of adaptation to ocean warming in corals, we've developed a genetic linkage map for the mountainous star coral, Orbicella faveolata. We analyzed genetic linkage among multilocus SNP genotypes to infer the relative positions of markers, transcripts, and genomic scaffolds in an integrated genomic map. To illustrate the utility of this resource, we tested for genetic associations with bleaching responses and fluorescence phenotypes, and estimated genomewide patterns of population differentiation. Mapping the significant markers identified from these analyses in the integrated genomic resource identified hundreds of genes linked to significant markers, highlighting the utility of this resource for genomic studies of corals. The functional interpretations drawn from genomic studies are often limited by the availability of genomic resources linking genes to genetic markers. The resource developed in this study provides a framework for comparing genetic studies of O. faveolata across genotyping methods or references, and illustrates an approach for integrating genomic resources that may be broadly useful in other non-model systems.

Humans have exaggerated natural habitat fragmentation, negatively impacting species dispersal and reducing population connectivity. Habitat fragmentation can be especially detrimental in freshwater populations, whose dispersal is already constrained by the river network structure. Aquatic insects, for instance, are generally limited to two primary modes of dispersal: downstream drift in the aquatic juvenile life stages and flight during the terrestrial winged adult stage. Yet the impacts of large hydropower dams can make rivers uninhabitable for incoming (drifting) juvenile insects, with remaining refugia found only in tributaries. The ability of adult aquatic insects to traverse such river stretches in search of suitable tributary habitat likely depends on factors such as species-specific dispersal ability and distance between tributaries. To explore the intersection of natural and human-induced habitat fragmentation on aquatic insect dispersal ability, we quantified population genetics of three taxa with varying dispersal abilities, a caddisfly (Hydropsychidae, Hydropsyche oslari), a mayfly (Baetidae: Fallceon quilleri), and a water strider (Veliidae: Rhagovelia distincta), throughout tributaries of the Colorado River in the Grand Canyon, Arizona, USA. Using 2bRAD reduced genome sequencing and landscape genetics analyses, we revealed a strong pattern of isolation by distance among mayfly populations. This contrasts with caddisfly and water strider populations, which were largely panmictic.Analysis of thousands of informative single nucleotide polymorphisms showed that realized dispersal ability may not be accurately predicted by species traits for these widespread species. Principal components analysis revealed a strong division between caddisfly populations upstream and downstream of Havasu Creek (279 km through the 390 km study reach), suggesting that the geography of the Grand Canyon imposes a dispersal barrier for this species. Our use of genetic tools in the Grand Canyon to understand population structure has enabled us to elucidate dispersal barriers for aquatic insects. Ultimately, these data may be useful in informing effective conservation management plans for understudied organisms of conservation interest.