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The phenomenon of chaotic genetic patchiness is a pattern commonly seen in marine organisms, particularly those with demersal adults and pelagic larvae. This pattern is usually associated with sweepstakes recruitment and variable reproductive success. Here we investigate the biological underpinnings of this pattern in a species of marine goby Coryphopterus personatus. We find that populations of this species show tell-tale signs of chaotic genetic patchiness including: small, but significant, differences in genetic structure over short distances; a non-equilibrium or “chaotic” pattern of differentiation among locations in space; and within locus, within population deviations from the expectations of Hardy-Weinberg equilibrium (HWE). We show that despite having a pelagic larval stage, and a wide distribution across Caribbean coral reefs, this species forms groups of highly related individuals at small spatial scales (<10 metres). These spatially clustered family groups cause the observed deviations from HWE and local population differentiation, a finding that is rarely demonstrated, but could be more common than previously thought.

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AbstractEpigenetic modification, specifically DNA methylation, is one possible mechanism for intergenerational plasticity. Before inheritance of methylation patterns can be characterized, we need a better understanding of how environmental change modifies the parental epigenome. To examine the influence of experimental ocean acidification on eastern oyster (Crassostrea virginica) gonad tissue, oysters were cultured in the laboratory under control (491 ± 49 μatm) or high (2550 ± 211 μatm) pCO2 conditions for four weeks. DNA from reproductive tissue was isolated from five oysters per treatment, then subjected to bisulfite treatment and DNA sequencing. Irrespective of treatment, DNA methylation was primarily found in gene bodies with approximately 22% of CpGs (2.7% of total cytosines) in the C. virginica genome predicted to be methylated. In response to elevated pCO2, we found 598 differentially methylated loci primarily overlapping with gene bodies. A majority of differentially methylated loci were in exons (61.5%) with less intron overlap (31.9%). While there was no evidence of a significant tendency for the genes with differentially methylated loci to be associated with distinct biological processes, the concentration of these loci in gene bodies, including genes involved in protein ubiquitination and biomineralization suggests DNA methylation may be important for transcriptional control in response to ocean acidification. Changes in gonad methylation also indicate potential for these methylation patterns to be inherited by offspring. Understanding how experimental ocean acidification conditions modify the oyster epigenome, and if these modifications are inherited, allows for a better understanding of how ecosystems will respond to environmental change.

Word Count: 350 Manuscript Word Count: 15658 1 Abstract Early evidence suggests that DNA methylation can mediate phenotypic responses of marine calcifying species to ocean acidification (OA). Few studies, however, have explicitly studied DNA methylation in calcifying tissues through time. Here, we examined the phenotypic and molecular responses in the extrapallial fluid and mantle (fluid and tissue at the calcification site) in the Eastern oyster ( Crassostrea virginica ) exposed to experimental OA over 80 days. Oysters were reared under three experimental pCO 2 treatments ('control', 580 μatm; 'moderate OA', 1000 uatm; 'high OA', 2800 μatm) and sampled at 6 time points (24 hours -80 days). We found that high OA initially induced changes in the pH of the extrapallial fluid (pH EPF ) relative to the external seawater, but the magnitude of this difference was highest at 9 days and diminished over time. Calcification rates were significantly lower in the high OA treatment compared to the other treatments. To explore how oysters regulate their extrapallial fluid, gene expression and DNA methylation were examined in the mantle-edge tissue of oysters from day 9 and 80 in the control and high OA treatments. Mantle tissue mounted a significant global molecular response (both in the transcriptome and methylome) to OA that shifted through time. Although we did not find individual genes that were significantly differentially expressed to OA, the pH EPF was correlated with the eigengene expression of several co-expressed gene clusters. A small number of OA-induced differentially methylated loci were discovered, which corresponded with a weak association between OA-induced changes in genome-wide gene body DNA methylation and gene expression. Gene body methylation, however, was not significantly correlated with the eigengene expression of pH EPF correlated gene clusters. These results suggest that in C. virginica , OA induces a subtle response in a large number of genes, but also indicates that plasticity at the molecular level may be limited. Our study highlights the need to re-assess the plasticity of tissue-specific molecular responses in marine calcifiers , as well as the role of DNA methylation and gene expression in mediating physiological and biomineralization responses to OA.