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ABSTRACT Triploid oysters are commonly used as the basis for production in the aquaculture of eastern oysters along the USA East and Gulf of Mexico coasts. While they are valued for their rapid growth, incidents of triploid mortality during summer months have been well documented in eastern oysters, especially at low salinity sites. We compared global transcriptomic responses of diploid and triploid oysters bred from the same three maternal source populations at two different hatcheries and outplanted to a high (annual mean salinity = 19.4 ± 6.7) and low (annual mean salinity = 9.3 ± 5.0) salinity site. Oysters were sampled for gene expression at the onset of a mortality event in the summer of 2021 to identify triploid‐specific gene expression patterns associated with low salinity sites, which ultimately experienced greater triploid mortality. We also examined chromosome‐specific gene expression to test for instances of aneuploidy in experimental triploid oyster lines, another possible contributor to elevated mortality in triploids. We observed a strong effect of hatchery conditions (cohort) on triploid‐specific mortality (field data) and a strong interactive effect of hatchery, ploidy, and outplant site on gene expression. At the low salinity site where triploid oysters experienced high mortality, we observed downregulation of transcripts related to calcium signaling, ciliary activity, and cell cycle checkpoints in triploids relative to diploids. These transcripts suggest dampening of the salinity stress response and problems during cell division as key cellular processes associated with elevated mortality risk in triploid oysters. No instances of aneuploidy were detected in our triploid oyster lines. Our results suggest that triploid oysters may be fundamentally less tolerant of rapid decreases in salinity, indicating that oyster farmers may need to limit the use of triploid oysters to sites with more stable salinity conditions.

The eastern oyster, Crassostrea virginica, is a keystone species native to the Gulf of Mexico and Atlantic coasts of the United States and Canada. It provides habitat for other marine organisms and makes up the majority of oyster production in the United States. Despite its tolerance to hypoxic conditions, C. virginica is threatened by anthropogenic climate change, which is increasing both average temperature and the frequency and severity of hypoxic events. In this study, we explore the differences in hypoxia-transcriptional response between two populations of eastern oysters with known differences in hypoxia tolerance at three time points over the course of a 5-day hypoxia treatment. We identified sets of genes involved in the hypoxia response and found differences in both the timing and baseline expression of hypoxia-responsive genes between tolerant and sensitive populations, consistent with a scenario of local adaptation. Analysis of differential gene expression between the two populations and conditions revealed two gene modules with higher baseline expression of hypoxia-sensitive genes in the more hypoxia tolerant population. Key GO terms for genes corresponding to differences between populations include DNA repair, ribosome biogenesis, and ribonucleotide binding. Our results imply that differences in hypoxia tolerance between populations could be due to genetic frontloading of hypoxia response pathways in the more tolerant population.

Abstract Populations may respond to environmental heterogeneity via evolutionary divergence or phenotypic plasticity. While evolutionary divergence occurs through DNA sequence differences among populations, plastic divergence among populations may be generated by changes in the epigenome. Here, we present the results of a genome‐wide comparison of DNA methylation patterns and genetic structure among four populations of Eastern oyster (Crassostrea virginica) in the northern Gulf of Mexico. We used a combination of restriction site‐associated DNA sequencing (RADseq) and reduced representation bisulfite sequencing (RRBS) to explore population structure, gene‐wide averages of FST, and DNA methylation differences between oysters inhabiting four estuaries with unique salinity profiles. This approach identified significant population structure despite a moderately low FST (0.02) across the freshwater boundary of the Mississippi river, a finding that may reflect recent efforts to restore oyster stock populations. Divergence between populations in CpG methylation was greater than for divergence in FST, likely reflecting environmental effects on DNA methylation patterns. Assessment of CpG methylation patterns across all populations identified that only 26% of methylated DNA was intergenic; and, only 17% of all differentially methylated regions (DMRs) were within these same regions. DMRs within gene bodies between sites were associated with genes known to be involved in DNA damage repair, ion transport, and reproductive timing. Finally, when assessing the correlation between genomic variation and DNA methylation between these populations, we observed population‐specific DNA methylation profiles that were not directly associated with single nucleotide polymorphisms or broader gene‐body mean FST trends. Our results suggest that C. virginica may use DNA methylation to generate environmentally responsive plastic phenotypes and that there is more divergence in methylation than divergence in allele frequencies.

Neophobia (aversion to new objects, food, and environments) is a personality trait that affects the ability of wildlife to adapt to new challenges and opportunities. Despite the ubiquity and importance of this trait, the molecular mechanisms underlying repeatable individual differences in neophobia in wild animals are poorly understood. We evaluated wild-caught house sparrows (Passer domesticus) for neophobia in the lab using novel object tests. We then selected a subset of neophobic and non-neophobic individuals (n = 3 of each, all females) and extracted RNA from four brain regions involved in learning, memory, threat perception, and executive function: striatum, caudal dorsomedial hippocampus, medial ventral arcopallium, and caudolateral nidopallium (NCL). Our analysis of differentially expressed genes (DEGs) used 11,889 gene regions annotated in the house sparrow reference genome for which we had an average of 25.7 million mapped reads/sample. PERMANOVA identified significant effects of brain region, phenotype (neophobic vs. non-neophobic), and a brain region by phenotype interaction. Comparing neophobic and non-neophobic birds revealed constitutive differences in DEGs in three of the four brain regions examined: hippocampus (12% of the transcriptome significantly differentially expressed), striatum (4%) and NCL (3%). DEGs included important known neuroendocrine mediators of learning, memory, executive function, and anxiety behavior, including serotonin receptor 5A, dopamine receptors 1, 2 and 5 (downregulated in neophobic birds), and estrogen receptor beta (upregulated in neophobic birds). These results suggest that some of the behavioral differences between phenotypes may be due to underlying gene expression differences in the brain. The large number of DEGs in neophobic and non-neophobic birds also implies that there are major differences in neural function between the two phenotypes that could affect a wide variety of behavioral traits beyond neophobia.

Eastern oysters in the northern Gulf of Mexico are routinely infected with the protistan parasite Perkinsus marinus, the cause of the disease commonly known as dermo. Recent experimental challenges among Atlantic coast populations have identified both resistant and susceptible genotypes using comparative transcriptomics. While controlled experimental challenges are essential first assessments, expanding this analysis to field reared individuals provides an opportunity to identify key genomic signatures of infection that appear both in the laboratory and in the field. In this study we combined reduced representation bisulfite sequencing with 3′ RNA sequencing (Tag-seq) to describe two molecular phenotypes associated with infection in oysters outplanted at a common garden field site. These combined approaches allowed us to examine changes in DNA methylation and gene expression for a large number of individuals (n = 40) that developed infections during the course of a common garden outplant experiment. Our epigenetic analysis of DNA methylation identified significant changes in gene body methylation associated with increasing infection intensity, across genes associated with immune responses. There was a smaller transcriptomic response to increasing infection intensities with 32 genes showing differential expression; however, only 40% of these genes were found to also be differentially methylated. While there was no clear pattern between direction of differential methylation and gene expression, there was a significant effect of percent methylation on gene-by-gene expression levels and the coefficient of variation in gene body methylation between treatments. These results show that in C. virginica, heavily methylated genes have high levels of gene expression with low levels of variation. Comparing our differential expression results with previously published experimental P. marinus challenges identified overlapping expression patterns for genes associated with C1q-domain-containing and V-type proton ATPase proteins. Through our comparative transcriptomic approach using field reared individuals and co-expression network analysis we have also been able to identify a network of genes that change in expression in response to infection. These combined analyses provide evidence for a conserved response to P. marinus infections across infection intensities and suggest that DNA methylation may not be a reliable predictor of differential gene expression in long-term infections.

As global ocean change progresses, reef-building corals and their early life history stages will rely on physiological plasticity to tolerate new environmental conditions. Larvae from brooding coral species contain algal symbionts upon release, which assist with the energy requirements of dispersal and metamorphosis. Global ocean change threatens the success of larval dispersal and settlement by challenging the performance of the larvae and of the symbiosis. In this study, larvae of the reef-building coral Pocillopora damicornis were exposed to elevated pCO2 and temperature to examine the performance of the coral and its symbionts in situ and better understand the mechanisms of physiological plasticity and stress tolerance in response to multiple stressors. We generated a de novo holobiont transcriptome containing coral host and algal symbiont transcripts and bioinformatically filtered the assembly into host and symbiont components for downstream analyses. Seventeen coral genes were differentially expressed in response to the combined effects of pCO2 and temperature. In the symbiont, 89 genes were differentially expressed in response to pCO2. Our results indicate that many of the whole-organism (holobiont) responses previously observed for P. damicornis larvae in scenarios of ocean acidification and warming may reflect the physiological capacity of larvae to cope with the environmental changes without expressing additional protective mechanisms. At the holobiont level, the results suggest that the responses of symbionts to future ocean conditions could play a large role in shaping success of coral larval stages.

The extent to which acclimation and genetic adaptation might buffer natural populations against climate change is largely unknown. Most models predicting biological responses to environmental change assume that species' climatic envelopes are homogeneous both in space and time. Although recent discussions have questioned this assumption, few empirical studies have characterized intraspecific patterns of genetic variation in traits directly related to environmental tolerance limits. We test the extent of such variation in the broadly distributed tidepool copepod Tigriopus californicus using laboratory rearing and selection experiments to quantify thermal tolerance and scope for adaptation in eight populations spanning more than 17° of latitude. Tigriopus californicus exhibit striking local adaptation to temperature, with less than 1 per cent of the total quantitative variance for thermal tolerance partitioned within populations. Moreover, heat-tolerant phenotypes observed in low-latitude populations cannot be achieved in high-latitude populations, either through acclimation or 10 generations of strong selection. Finally, in four populations there was no increase in thermal tolerance between generations 5 and 10 of selection, suggesting that standing variation had already been depleted. Thus, plasticity and adaptation appear to have limited capacity to buffer these isolated populations against further increases in temperature. Our results suggest that models assuming a uniform climatic envelope may greatly underestimate extinction risk in species with strong local adaptation. [ABSTRACT FROM AUTHOR]