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Understanding connectivity between populations is key to identifying hotspots of diversity, dispersal sinks and sources, and effective management units for natural resources. Multi-species connectivity seeks to overcome species-specific idiosyncrasies to identify shared patterns that are most critical to spatial management. The linear Hawaiian archipelago provides an excellent platform to assess multi-species connectivity patterns, with shared boundaries to gene flow identified across a majority of the 41 coral reef species surveyed to date. Here, we evaluate genome-scale data by comparing consistency and resolution to previous connectivity studies using far fewer loci. We used pool-seq to genotype 22,503–232,730 single nucleotide polymorphisms per species (625,215 SNPs total) from the same individuals published in previous studies of two fishes, two corals, and two lobsters. Additionally, one coral species (Pocillopora meandrina) without previous archipelago-wide population genetic data was included. With greater statistical power, most genetic differences between pairwise comparisons of islands were significant (250 of 308), consistent with the most recent larval dispersal models for the Hawaiian Archipelago. These data reveal significant differentiation at a finer scale than previously reported using single-marker studies, yet did not overturn any of the conclusions or management implications drawn from previous studies. We confirm that population genomic datasets are consistent with previously reported patterns of multispecies connectivity but add a finer layer of population resolution that is pertinent to management. 

Reef-building coral populations are at serious risk of collapse due to the combined effects of ocean warming and acidification. Nonetheless, many corals show potential to adapt to the changing ocean conditions. Here we examine the broad sense heritability (H²) of coral calcification rates across an ecologically and phylogenetically diverse sampling of eight of the primary reef-building corals across the Indo-Pacific. We show that all eight species exhibit relatively high heritability of calcification rates under combined warming and acidification (0.23–0.56). Furthermore, tolerance to each factor is positively correlated and the two factors do not interact in most of the species, contrary to the idea of trade-offs between temperature and pH sensitivity, and all eight species can co-evolve tolerance to elevated temperature and reduced pH. Using these values together with historical data, we estimate potential increases in thermal tolerance of 1.0–1.7°C over the next 50 years, depending on species. None of these species are probably capable of keeping up with a high global change scenario and climate change mitigation is essential if reefs are to persist. Such estimates are critical for our understanding of how corals may respond to global change, accurately parametrizing modelled responses, and predicting rapid evolution. 

Abstract Signals of natural selection can be quickly eroded in high gene flow systems, curtailing efforts to understand how and when genetic adaptation occurs in the ocean. This long‐standing, unresolved topic in ecology and evolution has renewed importance because changing environmental conditions are driving range expansions that may necessitate rapid evolutionary responses. One example occurs in Kellet's whelk (Kelletia kelletii), a common subtidal gastropod with an ~40‐ to 60‐day pelagic larval duration that expanded their biogeographic range northwards in the 1970s by over 300 km. To test for genetic adaptation, we performed a series of experimental crosses with Kellet's whelk adults collected from their historical (HxH) and recently expanded range (ExE), and conducted RNA‐Seq on offspring that we reared in a common garden environment. We identified 2770 differentially expressed genes (DEGs) between 54 offspring samples with either only historical range (HxH offspring) or expanded range (ExE offspring) ancestry. Using SNPs called directly from the DEGs, we assigned samples of known origin back to their range of origin with unprecedented accuracy for a marine species (92.6% and 94.5% for HxH and ExE offspring, respectively). The SNP with the highest predictive importance occurred on triosephosphate isomerase (TPI), an essential metabolic enzyme involved in cold stress response.TPIwas significantly upregulated and contained a non‐synonymous mutation in the expanded range. Our findings pave the way for accurately identifying patterns of dispersal, gene flow and population connectivity in the ocean by demonstrating that experimental transcriptomics can reveal mechanisms for how marine organisms respond to changing environmental conditions. 

ABSTRACT How reproductive barriers arise in early stages of divergence among broadcast spawning organisms that exist in sympatry remains poorly understood. Reproductively isolated lineages (Clade A and B) ofStichopuscf.horrenswere previously reported across the western Pacific, with an additional putative cryptic species detected within the Clade B lineage warranting further examination. The present study further examines the hypothesis that the two mitochondrial lineages (Clade A and Clade B) ofStichopuscf. horrensrepresent putative cryptic species and whether another cryptic species within the Clade B lineage exists using a reduced representation genomic approach. Using double‐digest RAD (ddRAD) sequencing, a total of 9788 single nucleotide polymorphism (SNP) markers were used to examine divergence amongStichopuscf. horrenslineages (n = 82). Individuals grouped into three SNP genotype clusters, broadly concordant with their mitochondrial lineages and microsatellite genotype clusters, with limited gene flow inferred among clusters. Outlier analysis recovered highly divergent SNP loci with significant homology to proteins related to rhodopsin and tachykinin receptor signaling, sperm motility, transmembrane transport, and hormone response. This study confirms the existence of three reproductively isolated genotype clusters withinStichopuscf.horrensand highlights gene regions related to reproduction that may contribute to establishing reproductive barriers between broadcast spawning species at an early stage of divergence. 

Abstract Coral reefs are iconic examples of climate change impacts because climate-induced heat stress causes the breakdown of the coral-algal symbiosis leading to a spectacular loss of color, termed ‘coral bleaching’. To examine the fine-scale dynamics of this process, we re-sampled 600 individually marked Montipora capitata colonies from across Kāne’ohe Bay, Hawai’i and compared the algal symbiont composition before and after the 2019 bleaching event. The relative proportion of the heat-tolerant symbiont Durusdinium in corals increased in most parts of the bay following the bleaching event. Despite this widespread increase in abundance of Durusdinium , the overall algal symbiont community composition was largely unchanged, and hydrodynamically defined regions of the bay retained their distinct pre-bleaching compositions. We explain ~ 21% of the total variation, of which depth and temperature variability were the most significant environmental drivers of Symbiodiniaceae community composition by site regardless of bleaching intensity or change in relative proportion of Durusdinium . We hypothesize that the plasticity of symbiont composition in corals may be constrained to adaptively match the long-term environmental conditions surrounding the holobiont, despite an individual coral’s stress and bleaching response. 

The plasticity of some coral-associated microbial communities under stressors like warming and ocean acidification suggests the microbiome has a role in the acclimatization of corals to future ocean conditions. Here, we evaluated the acclimatization potential of coral-associated microbial communities of four Hawaiian coral species (Porites compressa,Porites lobata,Montipora capitata, andPocillopora acuta) over 22-month mesocosm experiment. The corals were exposed to one of four treatments: control, ocean acidification, ocean warming, or combined future ocean conditions. Over the 22-month study, 33–67% of corals died or experienced a loss of most live tissue coverage in the ocean warming and future ocean treatments while only 0–10% died in the ocean acidification and control. Among the survivors, coral-associated microbial communities responded to the chronic future ocean treatment in one of two ways: (1) microbial communities differed between the control and future ocean treatment, suggesting the potential capacity for acclimatization, or (2) microbial communities did not significantly differ between the control and future ocean treatment. The first strategy was observed in bothPoritesspecies and was associated with higher survivorship compared toM.capitataandP.acutawhich exhibited the second strategy. Interestingly, the microbial community responses to chronic stressors were independent of coral physiology. These findings indicate acclimatization of microbial communities may confer resilience in some species of corals to chronic warming associated with climate change. However,M.capitatagenets that survived the future ocean treatment hosted significantly different microbial communities from those that died, suggesting the microbial communities of the survivors conferred some resilience. Thus, even among coral species with inflexible microbial communities, some individuals may already be tolerant to future ocean conditions. These findings suggest that coral-associated microbial communities could play an important role in the persistence of some corals and underlie climate change-driven shifts in coral community composition. 

Understanding the genomic characteristics of non-model organisms can bridge research gaps between ecology and evolution. However, the lack of a reference genome and transcriptome for these species makes their study challenging. Here, we complete the first full genome and transcriptome sequence assembly of the non-model organism Kellet’s whelk,Kelletia kelletii, a marine gastropod exhibiting a poleward range expansion coincident with climate change. We used a combination of Oxford Nanopore Technologies, PacBio, and Illumina sequencing platforms and integrated a set of bioinformatic pipelines to create the most complete and contiguous genome documented among the Buccinoidea superfamily to date. Genome validation revealed relatively high completeness with low missing metazoan Benchmarking Universal Single-Copy Orthologs (BUSCO) and an average coverage of ∼70x for all contigs. Genome annotation identified a large number of protein-coding genes similar to some other closely related species, suggesting the presence of a complex genome structure. Transcriptome assembly and analysis of individuals during their period of peak embryonic development revealed highly expressed genes associated with specific Gene Ontology (GO) terms and metabolic pathways, most notably lipid, carbohydrate, glycan, and phospholipid metabolism. We also identified numerous heat shock proteins (HSPs) in the transcriptome and genome that may be related to coping with thermal stress during the sessile life history stage. A robust reference genome and transcriptome for the non-model organismK. kelletiiprovide resources to enhance our understanding of its ecology and evolution and potential mechanisms of range expansion for marine species facing environmental changes.