Gene expression response under thermal stress in two Hawaiian corals is dominated by ploidy and genotype.

Transcriptome data are frequently used to investigate coral bleaching; however, the factors controlling gene expression in natural populations of these species are poorly understood. We studied two corals, Montipora capitata and Pocillopora acuta, that inhabit the sheltered Kane'ohe Bay, Hawai'i. M. capitata colonies in the bay are outbreeding diploids, whereas P. acuta is a mixture of clonal diploids and triploids. Populations were sampled from six reefs and subjected to either control (no stress), thermal stress, pH stress, or combined pH and thermal stress treatments. RNA-seq data were generated to test two competing hypotheses: (1) gene expression is largely independent of genotype, reflecting a shared treatment-driven response (TDE) or, (2) genotype dominates gene expression, regardless of treatment (GDE). Our results strongly support the GDE model, even under severe stress. We suggest that post-transcriptional processes (e.g., control of translation, protein turnover) modify the signal from the transcriptome, and may underlie the observed differences in coral bleaching sensitivity via the downstream proteome and metabolome.

Coral species-specific loss and physiological legacy effects are elicited by an extended marine heatwave.

Marine heatwaves are increasing in frequency and intensity, with potentially catastrophic consequences for marine ecosystems such as coral reefs. An extended heatwave and recovery time-series that incorporates multiple stressors and is environmentally realistic can provide enhanced predictive capacity for performance under climate change conditions. We exposed common reef-building corals in Hawai'i, Montipora capitata and Pocillopora acuta, to a 2-month period of high temperature and high PCO2 conditions or ambient conditions in a factorial design, followed by 2 months of ambient conditions. High temperature, rather than high PCO2, drove multivariate physiology shifts through time in both species, including decreases in respiration rates and endosymbiont densities. Pocillopora acuta exhibited more significantly negatively altered physiology, and substantially higher bleaching and mortality than M. capitata. The sensitivity of P. acuta appears to be driven by higher baseline rates of photosynthesis paired with lower host antioxidant capacity, creating an increased sensitivity to oxidative stress. Thermal tolerance of M. capitata may be partly due to harboring a mixture of Cladocopium and Durusdinium spp., whereas P. acuta was dominated by other distinct Cladocopium spp. Only M. capitata survived the experiment, but physiological state in heatwave-exposed M. capitata remained significantly diverged at the end of recovery relative to individuals that experienced ambient conditions. In future climate scenarios, particularly marine heatwaves, our results indicate a species-specific loss of corals that is driven by baseline host and symbiont physiological differences as well as Symbiodiniaceae community compositions, with the surviving species experiencing physiological legacies that are likely to influence future stress responses.

Ploidy Variation and Its Implications for Reproduction and Population Dynamics in Two Sympatric Hawaiian Coral Species.

Standing genetic variation is a major driver of fitness and resilience and therefore of fundamental importance for threatened species such as stony corals. We analyzed RNA-seq data generated from 132 Montipora capitata and 119 Pocillopora acuta coral colonies collected from Kane'ohe Bay, O'ahu, Hawai'i. Our goals were to determine the extent of colony genetic variation and to study reproductive strategies in these two sympatric species. Surprisingly, we found that 63% of the P. acuta colonies were triploid, with putative independent origins of the different triploid clades. These corals have spread primarily via asexual reproduction and are descended from a small number of genotypes, whose diploid ancestor invaded the bay. In contrast, all M. capitata colonies are diploid and outbreeding, with almost all colonies genetically distinct. Only two cases of asexual reproduction, likely via fragmentation, were identified in this species. We report two distinct strategies in sympatric coral species that inhabit the largest sheltered body of water in the main Hawaiian Islands. These data highlight divergence in reproductive behavior and genome biology, both of which contribute to coral resilience and persistence.

Developmental series of gene expression clarifies maternal mRNA provisioning and maternal-to-zygotic transition in a reef-building coral.

BACKGROUND: Maternal mRNA provisioning of oocytes regulates early embryogenesis. Maternal transcripts are degraded as zygotic genome activation (ZGA) intensifies, a phenomenon known as the maternal-to-zygotic transition (MZT). Here, we examine gene expression over nine developmental stages in the Pacific rice coral, Montipora capitata, from eggs and embryos at 1, 4, 9, 14, 22, and 36 h-post-fertilization (hpf), as well as swimming larvae (9d), and adult colonies. RESULTS: Weighted Gene Coexpression Network Analysis revealed four expression peaks, identifying the maternal complement, two waves of the MZT, and adult expression. Gene ontology enrichment revealed maternal mRNAs are dominated by cell division, methylation, biosynthesis, metabolism, and protein/RNA processing and transport functions. The first MZT wave occurs from ~4-14 hpf and is enriched in terms related to biosynthesis, methylation, cell division, and transcription. In contrast, functional enrichment in the second MZT wave, or ZGA, from 22 hpf-9dpf, includes ion/peptide transport and cell signaling. Finally, adult expression is enriched for functions related to signaling, metabolism, and ion/peptide transport. Our proposed MZT timing is further supported by expression of enzymes involved in zygotic transcriptional repression (Kaiso) and activation (Sox2), which peak at 14 hpf and 22 hpf, respectively. Further, DNA methylation writing (DNMT3a) and removing (TET1) enzymes peak and remain stable past ~4 hpf, suggesting that methylome programming occurs before 4 hpf. CONCLUSIONS: Our high-resolution insight into the coral maternal mRNA and MZT provides essential baseline information to understand parental carryover effects and the sensitivity of developmental success under increasing environmental stress.

Molecular characterization of nearshore baitfish populations in Bermuda to inform management.

Small-bodied marine fishes play an important role in the food web, feeding both larger fishes and seabirds. Often referred to as baitfishes, they concentrate seasonally in coastal areas in large, often heterospecific assemblages that are targeted by both commercial and recreational fishers. Given apparent declines in at least some of Bermuda's baitfish species over the past 40 years, it is useful to determine the species composition of baitfish assemblages, and how it varies among sites, in order to inform management. Using genetic barcoding of the Cytochrome c oxidase 1 gene (COI), we confirm species identity, assess intraspecific genetic diversity locally, and determine rates of broader genetic connectivity for baitfish assemblages in Bermuda. Species analyzed included Hypoatherina harringtonensis, Anchoa choerostoma, Jenkinsia lamprotaenia, Harengula humeralis, Opisthonema oglinum and Sardinella aurita. Species identification based on molecular barcoding revealed some misidentification of individuals based solely on gross morphological characteristics, with an error rate of 11%, validating the usefulness of this approach. Interestingly, sequence results for the endemic Bermuda anchovy, A. choerostoma, were within 1% similarity to the more broadly distributed big-eye anchovy, A. lamprotaenia, and thus additional analyses are warranted to evaluate the genetic basis for endemism. Estimates of genetic diversity within and among baitfish assemblages in Bermuda were high, indicating high rates of local connectivity among sites for all species. As such, management should consider Bermuda's baitfish species as single, highly mixed populations. However, with the exception of H. humeralis and the endemic A. choerostoma, significant genetic differentiation and population structure were found when comparing Bermuda's baitfish populations with those from other regions, suggesting limited gene flow between other regions and Bermuda for these species. Limited regional connectivity has implications for management, as strong genetic divergence suggests that populations in Bermuda are predominantly self-seeding and thus not likely to be replenished from distant populations. These results therefore support precautionary management of baitfish species in Bermuda.

Plasticity of thermal tolerance and its relationship with growth rate in juvenile mussels (Mytilus californianus).

Complex life cycles characterized by uncertainty at transitions between larval/juvenile and adult environments could favour irreversible physiological plasticity at such transitions. To assess whether thermal tolerance of intertidal mussels (Mytilus californianus) adjusts to post-settlement environmental conditions, we collected juveniles from their thermally buffered microhabitat from high- and low-shore locations at cool (wave-exposed) and warm (wave-protected) sites. Juveniles were transplanted to unsheltered cages at the two low sites or placed in a common garden. Juveniles transplanted to the warm site for one month in summer had higher thermal tolerance, regardless of origin site. By contrast, common-garden juveniles from all sites had lower tolerance indistinguishable from exposed site transplants. After six months in the field plus a common garden period, there was a trend for higher thermal tolerance at the protected site, while reduced thermal tolerance at both sites indicated seasonal acclimatization. Thermal tolerance and growth rate were inversely related after one but not six months; protected-site transplants were more tolerant but grew more slowly. In contrast to juveniles, adults from low-shore exposed and protected sites retained differences in thermal tolerance after common garden treatment in summer. Both irreversible and reversible forms of plasticity must be considered in organismal responses to changing environments.