Epigenetic inheritance and intergenerational effects in mollusks

Abstract

List of abbreviations 5mC5-methylcytosine, a cytosine that has been modified by the addition of a methyl group on its 5th carbon ADP Adenosine diphosphate AFLP Amplified fragment length polymorphism BLAST Basic Local Alignment Search Tool BS-Seq Bisulfite sequencing BS-PCR-Seq PCr amplification after bisulfite sequencing followed by sequencing Cd Cadium meDIP-seq Methylated DNA Immunoprecipitation sequencing MiRNAs Micro RNAs MSAP Methylation-sensitive amplified polymorphism MS-PCR Methylation-specific PCR pCO2 partial pressure of C02 PCR Polymerase chain reaction PTMs Post-Translational Modifications pH potential of Hydrogen qPCR quantitative Polymerase chain reaction RT-qPCR quantitative reverse transcription PCR RNA Ribonucleic acid RRBS Reduced representation bisulfite sequencing SAM S-adenosyl methionine SDS-PAGE Sodium Dodecil Sulfate PolyAcrylamide Gel Electrophoresis UV-HPLC Ultraviolet High performance liquid chromatography Abstract Recent insights in evolutionary biology have shed light on epigenetic variation that interacts with genetic variation to convey heritable information. An important characteristic of epigenetic changes is that they can be produced in response to environmental cues and passed on to later generations, potentially facilitating later genetic adaptation. While our understanding of epigenetic mechanisms in vertebrates is rapidly growing, our knowledge about invertebrates remains lower, or is restricted to model organisms. Mollusks in particular, are a large group of invertebrates, with several species important for ecosystem function, human economy and health. In this review, we attempt to summarize the literature on epigenetic and 4 intergenerational studies in mollusk species, with potential importance for adaptive evolution. Our review highlights that two molecular bearers of epigenetic information, DNA methylation and histone modifications, are key features for development in mollusk species, and both are sensitive to environmental conditions to which developing individuals are exposed. Further, although studies are still scarce, various environmental factors (e.g. predator cues, chemicals, parasites) can induce intergenerational effects on the phenotype (life-history traits, morphology, behaviour) of several mollusk taxa. More work is needed to better understand whether environmentally-induced changes in DNA methylation and histone modifications have phenotypic impacts, whether they can be inherited through generations and their role in intergenerational effects on phenotype. Such work may bring insight into the potential role of epigenetic in adaptation and evolution in mollusks.

Transgenerational Plasticity in the Context of Predator-Prey Interactions

“…A similar result was observed in mice, where only the gene expression patterns of female offspring were impacted by maternal exposure to predator-cues (St-Cyr and McGowan, 2015). Interestingly, Hales et al (2017) observed a decrease in the number of differentially expressed genes between the F1 and F2 generations-a trend consistent with the observed decrease in transgenerational responses ( §4.2; Walsh et al, 2015) and the lability of inherited epigenetic marks (Fallet et al, 2020). In a companion methodological paper, Schield et al (2016) found shifts in the methylation state of sampled loci between F0 (with predator-cues) and F1 (without predatorcues) in D. ambigua, suggesting that DNA methylation patterns can vary between generations experiencing different predation environments.…”

“…Although this is not evidence of transgenerational epigenetic inheritance, it suggests that predation-risk driven behavior of fathers may influence the epigenetic programming of their offspring, which might in turn be transmitted to the next generation. To our knowledge, how and to what extent the epigenome is related to phenotype across generations is still an open question both in predator-prey systems and in general (see Fallet et al, 2020 for a detailed discussion). Taken together, the above results highlight the need for future work examining predator-induced TGP and WGP simultaneously, at both the (epi)genomic and phenotypic levels.…”

Genome-wide epigenomic stress response in the European sea bass (Dicentrarchus labrax, L.)

“…These proposals are not mutually exclusive. Transgenerational inheritance has gained interest over the last years [171], notably in marine species [50,172,173], and including sea bass [83]. Parents and/or the germline were unfortunately not sampled in this study for further analysis.…”

Deciphering mollusc shell production: the roles of genetic mechanisms through to ecology, aquaculture and biomimetics

“…An early epigenetic study in molluscs using methylation‐sensitive polymerase chain reaction (PCR) and bisulphite sequencing revealed extensive CpG methylation in Crassostrea gigas (Gavery & Roberts, 2010). To date, epigenetic studies in molluscs have predominantly involved methylation analyses, often studying developmental effects (Fallet et al ., 2020), although other mechanisms include remodelling of chromatin structure through chemical changes to histone proteins and regulation by small RNA molecules. Thus, epigenetic effects may result from a mix of mechanisms in natural environments (Suarez‐Ulloa et al ., 2015).…”