The Epigenetics Dilemma

International audienceThis special issue of Genes demonstrates clearly that research in epigenetics has proceeded at a very rapid pace in the last decade. A wide range of techniques is available to those who endeavor studies in epigenetics and as long as there is a research budget, there remains today very few technical constraints. It is, for instance, conceivable, as demonstrated by Liu et al. in this special issue [1], to practically start from scratch to sequence and assemble the genome of any species, establish the epigenome, and perform integrative comparative approaches on both within the framework of a single publication. This would have been inconceivable only a couple of years ago. As a consequence, results presented in this issue and elsewhere make clear that this is a time of opportunity for epigenetics as its contours and impact are traced more and more clearly: the epigenome is demonstrated to be very plastic, it changes during development [2], but also, and in a different way, when exposed to external environmental cues. These changes occur sometimes within generations [3] and, in other cases, epigenetic plasticity occurs through generations [4,5], conveying parental effects of very different type (e.g., parental diet or hatchery environment)

3D microscopic reconstruction of pearls using combined optical microscopy and photogrammetry

In this study, we introduce an affordable and accessible method that combines optical microscopy and photogrammetry to reconstruct 3D models of Tahitian pearls. We present a novel device designed for acquiring microscopic images around a sphere using translational displacement stages and outline our method for reconstructing these images. We successfully created 3D models of two individual pearl rings, each representing 6.3% of the pearl’s surface. Additionally, we generated a combined model representing 10.3% of the pearl’s surface. This showcases the potential for reconstructing entire pearls with appropriate instrumentation. We emphasize that our approach extends beyond pearls and spherical objects and can be adapted for various object types using appropriate acquisition devices. We provide a proof of concept demonstrating the feasibility of 3D photogrammetry using optical microscopy. Consequently, our method offers a practical and cost-effective alternative for generating 3D models at a microscopic scale, particularly when detailed internal structure information is unnecessary

The complete mitochondrial DNA of the Cuban gar ( Atractosteus tristoechus )

The Cuban gar (Atractosteus tristoechus) is an endemic lepisosteid living in Cuba. Among gars, this species is one of the most threatened and has the smallest natural distribution range. Lepisosteids are air-breathing fishes belonging to the Holostean, a basal non-teleost clade of actinopterygians. Recent studies have indicated that these fishes could be a ‘bridge between tetrapods and teleost biomedical models’. Herein, we sequenced and assembled the first complete mitochondrial genome of A. tristoechus. The total length of the mt genome is 16,290 bp, containing the typical 13 protein-coding genes, two ribosomal RNA (rRNA) genes, 22 transfer RNA (tRNA) genes, and a 537 bp length control region

Microplastics induce dose-specific transcriptomic disruptions in energy metabolism and immunity of the pearl oyster Pinctada margaritifera

A combined approach integrating bioenergetics and major biological activities is essential to properly understand the impact of microplastics (MP) on marine organisms. Following experimental exposure of polystyrene microbeads (micro-PS of 6 and 10 μm) at 0.25, 2.5, and 25 μg L−1, which demonstrated a dose-dependent decrease of energy balance in the pearl oyster Pinctada margaritifera, a transcriptomic study was conducted on mantle tissue. Transcriptomic data helped us to decipher the molecular mechanisms involved in P. margaritifera responses to micro-PS and search more broadly for effects on energetically expensive maintenance functions. Genes related to the detoxification process were impacted by long-term micro-PS exposure through a decrease in antioxidant response functioning, most likely leading to oxidative stress and damage, especially at higher micro-PS doses. The immune response was also found to be dose-specific, with a stress-related activity stimulated by the lowest dose present after a 2-month exposure period. This stress response was not observed following exposure to higher doses, reflecting an energy-limited capacity of pearl oysters to cope with prolonged stress and a dramatic shift to adjust to pessimum conditions, mostly limited and hampered by a lowered energetic budget. This preliminary experiment lays the foundation for exploring pathways and gene expression in P. margaritifera, and marine mollusks in general, under MP exposure. We also propose a conceptual framework to properly assess realistic MP effects on organisms and population resilience in future investigations

Predicting the genetic impact of stocking in Brook Charr ( Salvelinus fontinalis ) by combining RAD sequencing and modeling of explanatory variables

In fisheries management, intensive stocking programs are commonly used to enhance population abundance and maintain stock productivity. However, such practices are increasingly raising concerns as multiple studies documented adverse genetic and evolutionary impacts of stocking on wild populations. Improvement of stocking management relies on a better understanding of the dynamic of introgressive hybridization between wild and domestic population and on assessment of the genetic state of wild populations after stocking cessation. In Québec, Canada, over five million captive-reared Brook Charr (Salvelinus fontinalis) are stocked every year to support recreational fishing activities. Here, we investigated how variation in stocking history and environmental variables, including water temperature, pH, and dissolved oxygen, may influence the impact of stocking practices on the genetic integrity of wild Brook Charr populations. We collected DNA samples (n = 862, average of 30 individuals per lake) from 29 lakes that underwent different stocking intensity through time and also collected environmental parameters for each sampled lake. An average of 4,580 high-quality filtered SNPs was obtained for each population using genotyping by sequencing (GBS), which were then used to quantify the mean domestic membership of each sampled population. An exhaustive process of model selection was conducted to obtain a best-fitted model that explained 56% of the variance observed in mean domestic genetic membership. The number of years since the mean year of stocking was the best explanatory variable to predict variation in mean domestic genetic membership whereas environmental characteristics had little influence on observed patterns of admixture. Our model predictions also revealed that each sampled wild population could potentially return to a wild genetic state (absence of domestic genetic background) after stocking cessation. Overall, our study provides new insights on factors determining level of introgressive hybridization and suggests that stocking impacts could be reversible with time

Strong parallel differential gene expression induced by hatchery rearing weakly associated with methylation signals in adult Coho Salmon ( O. kisutch )

Human activities and resource exploitation led to a massive decline of wild salmonid populations, consequently numerous conservation programs have been developed to supplement wild populations. However, many studies documented reduced fitness of hatchery-born relative to wild fish. Here, by using both RNA sequencing and Whole Genome Bisulfite Sequencing (WGBS), we show that of hatchery and wild born adult Coho Salmon (Oncorhynchus kisutch) originating from two previously studied river systems, early-life hatchery rearing environment induced significant and parallel gene expression differentiation is maintained until Coho come back to their natal river for reproduction. A total of 3,643 genes differentially expressed and 859 co-expressed genes were down-regulated in parallel in hatchery born fish from both rivers relative to their wild congeners. Among those genes, 26 displayed a significant relationship between gene expression and the median gene body methylation and 669 single CpG displayed a significant correlation between methylation level and the associated gene expression. The link between methylation and gene expression was weak suggesting that DNA methylation is not the only player in mediating hatchery-related expression differences. Yet, significant gene expression differentiation was observed despite 18 month spent in a common environment (i.e. the sea). Finally, the differentiation is observed in parallel in two different river system, highlighting the fact that early life environment may account for at least some of the reduced fitness of the hatchery salmon in the wild. These results illustrate the relevance and importance of considering both epigenome and transcriptome to evaluate the costs and benefits of large-scale supplementation programs

Substantial gene expression shifts during larval transitions in the pearl oyster Pinctada margaritifera

Early development stages in marine bivalve are critical periods where larvae transition from pelagic free‐life to sessile mature individuals. The successive metamorphosis requires the expression of key genes, the functions of which might be under high selective pressure, hence understanding larval development represents key knowledge for both fundamental and applied research. Phenotypic larvae development is well known, but the underlying molecular mechanisms such as associated gene expression dynamic and molecular cross‐talks remains poorly described for several nonmodel species, such as P. margaritifera. We designed a whole transcriptome RNA‐sequencing analysis to describe such gene expression dynamics following four larval developmental stages:  d‐shape, Veliger, Umbo and Eye‐spot. Larval gene expression and annotated functions drastically diverge. Metabolic function (gene expression related to lipid, amino acid and carbohydrate use) is highly upregulated in the first development stages, with increasing demand from  d‐shape to umbo. Morphogenesis and larval transition are partly ordered by Thyroid hormones and Wnt signaling. While larvae shells show some similar characteristic to adult shells, the cause of initialization of biomineralization differ from the one found in adults. The present study provides a global overview of Pinctada margaritifera larval stages transitioning through gene expression dynamics, molecular mechanisms and ontogeny of biomineralization, immune system, and sensory perception processes

Molecular mechanisms of acclimation to long‐term elevated temperature exposure in marine symbioses

Seawater temperature rise in French Polynesia has repeatedly resulted in the bleaching of corals and giant clams. Because giant clams possess distinctive ectosymbiotic features, they represent a unique and powerful model for comparing molecular pathways involved in 1) maintenance of symbiosis and 2) acquisition of thermo‐tolerance among coral reef organisms. Herein, we explored the physiological and transcriptomic responses of the clam hosts and their photosynthetically active symbionts over a 65‐day experiment in which clams were exposed to either normal or environmentally relevant elevated seawater temperatures. Additionally, we used metabarcoding data coupled with in situ sampling/survey data to explore the relative importance of holobiont adaptation (i.e., a symbiont community shift) versus acclimation (i.e., physiological changes at the molecular level) in the clams’ responses to environmental change. We finally compared transcriptomic data to publicly available genomic datasets for Symbiodiniaceae dinoflagellates (both cultured and in hospite with the coral Pocillopora damicornis) to better tease apart the responses of both hosts and specific symbiont genotypes in this mutualistic association. Gene module preservation analysis revealed that the function of the symbionts’ photosystem II was impaired at high temperature, and this response was also found across all holobionts and Symbiodiniaceae lineages examined. Similarly, epigenetic modulation appeared to be a key response mechanism for symbionts in hospite with giant clams exposed to high temperatures, and such modulation was able to distinguish thermo‐tolerant from thermo‐sensitive Cladocopium goreaui ecotypes; epigenetic processes may, then, represent a promising research avenue for those interested in coral reef conservation in this era of changing global climate

DNA methylation reprogramming, TE derepression, and postzygotic isolation of nascent animal species

The genomic shock hypothesis stipulates that the stress associated with divergent genome admixture can cause transposable element (TE) derepression, which could act as a postzygotic isolation mechanism. TEs affect gene structure, expression patterns, and chromosome organization and may have deleterious consequences when released. For these reasons, they are silenced by heterochromatin formation, which includes DNA methylation. Here, we show that a significant proportion of TEs are differentially methylated between the “dwarf” (limnetic) and the “normal” (benthic) whitefish, two nascent species that diverged some 15,000 generations ago within the Coregonus clupeaformis species complex. Moreover, TEs are overrepresented among loci that were demethylated in hybrids, indicative of their transcriptional derepression. These results are consistent with earlier studies in this system that revealed TE transcriptional derepression causes abnormal embryonic development and death of hybrids. Hence, this supports a role of DNA methylation reprogramming and TE derepression in postzygotic isolation of nascent animal species