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Abstract Parental exposure to environmental stress can influence phenotypic plasticity by offspring developing under that stressor. Transgenerational effects may also reshape natural selection on developmental plasticity by influencing its fitness consequences and expression of its genetic variation. We tested these hypotheses in the purple sea urchinStrongylocentrotus purpuratus, an invertebrate exposed to coastal upwelling (periods of low temperature and pH impacting biomineralization and performance). We conditioned parents and larvae to experimental upwelling and integrated RNA-seq, phenotyping of body size and biomineralization, and measured fitness-correlated traits in a quantitative genetic experiment. Larvae developing under upwelling induced widespread differential expression (DE), decreased biomineralization, and reduced body size. We detected fitness benefits for increased biomineralization and reduced size under upwelling indicative of adaptive plasticity, but only when larvae were spawned from parents exposed to upwelling. Larval DE was largely associated with adaptive phenotypic plasticity. Negative genetic correlation in DE was abundant between genes associated with adaptive plasticity. However, genetic correlations in DE associated with body size plasticity were significantly more positive in larvae from upwelling-exposed parents. These results show that transgenerational effects modify the fitness landscape and genetic architecture of phenotypic plasticity and its regulatory pathways. 

Abstract There is great interest in exploring epigenetic modifications as drivers of adaptive organismal responses to environmental change. Extending this hypothesis to populations, epigenetically driven plasticity could influence phenotypic changes across environments. The canonical model posits that epigenetic modifications alter gene regulation and subsequently impact phenotypes. We first discuss origins of epigenetic variation in nature, which may arise from genetic variation, spontaneous epimutations, epigenetic drift, or variation in epigenetic capacitors. We then review and synthesize literature addressing three facets of the aforementioned model: (i) causal effects of epigenetic modifications on phenotypic plasticity at the organismal level, (ii) divergence of epigenetic patterns in natural populations distributed across environmental gradients, and (iii) the relationship between environmentally induced epigenetic changes and gene expression at the molecular level. We focus on DNA methylation, the most extensively studied epigenetic modification. We find support for environmentally associated epigenetic structure in populations and selection on stable epigenetic variants, and that inhibition of epigenetic enzymes frequently bears causal effects on plasticity. However, there are pervasive confounding issues in the literature. Effects of chromatin-modifying enzymes on phenotype may be independent of epigenetic marks, alternatively resulting from functions and protein interactions extrinsic of epigenetics. Associations between environmentally induced changes in DNA methylation and expression are strong in plants and mammals but notably absent in invertebrates and nonmammalian vertebrates. Given these challenges, we describe emerging approaches to better investigate how epigenetic modifications affect gene regulation, phenotypic plasticity, and divergence among populations. 

Abstract BackgroundEpigenetic processes are proposed to be a mechanism regulating gene expression during phenotypic plasticity. However, environmentally induced changes in DNA methylation exhibit little-to-no association with differential gene expression in metazoans at a transcriptome-wide level. It remains unexplored whether associations between environmentally induced differential methylation and expression are contingent upon other epigenomic processes such as chromatin accessibility. We quantified methylation and gene expression in larvae of the purple sea urchinStrongylocentrotus purpuratusexposed to different ecologically relevant conditions during gametogenesis (maternal conditioning) and modeled changes in gene expression and splicing resulting from maternal conditioning as functions of differential methylation, incorporating covariates for genomic features and chromatin accessibility. We detected significant interactions between differential methylation, chromatin accessibility, and genic feature type associated with differential expression and splicing. ResultsDifferential gene body methylation had significantly stronger effects on expression among genes with poorly accessible transcriptional start sites while baseline transcript abundance influenced the direction of this effect. Transcriptional responses to maternal conditioning were 4–13 × more likely when accounting for interactions between methylation and chromatin accessibility, demonstrating that the relationship between differential methylation and gene regulation is partially explained by chromatin state. ConclusionsDNA methylation likely possesses multiple associations with gene regulation during transgenerational plasticity inS. purpuratusand potentially other metazoans,but its effects are dependent on chromatin accessibility and underlying genic features. 

Abstract BackgroundAntarctic fishes of the Notothenioidei suborder constitutively upregulate multiple inducible chaperones, a highly derived adaptation that preserves proteostasis in extreme cold, and represent a system for studying the evolution of gene frontloading. We screened forHsf1-binding sites, asHsf1is a master transcription factor of the heat shock response, and highly-conserved non-coding elements within proximal promoters of chaperone genes across 10 Antarctic notothens, 2 subpolar notothens, and 17 perciform fishes. We employed phylogenetic models of molecular evolution to determine whether (i) changes in motifs associated withHsf1-binding and/or (ii) relaxed purifying selection or exaptation at ancestralcis-regulatory elements coincided with the evolution of chaperone frontloading in Antarctic notothens. ResultsAntarctic notothens exhibited significantly fewerHsf1-binding sites per bp at chaperone promoters than subpolar notothens and Serranoidei, the most closely-related suborder to Notothenioidei included in this study. 90% of chaperone promoters exhibited accelerated substitution rates among Antarctic notothens relative to other perciformes. The proportion of bases undergoing accelerated evolution (i) was significantly greater in Antarctic notothens than in subpolar notothens and Perciformes in 70% of chaperone genes and (ii) increased among bases that were more conserved among perciformes. Lastly, we detected evidence of relaxed purifying selection and exaptation acting on ancestrally conservedcis-regulatory elements in the Antarctic notothen lineage and its major branches. ConclusionA large degree of turnover has occurred in Notothenioidei at chaperone promoter regions that are conserved among perciform fishes following adaptation to the cooling of the Southern Ocean. Additionally, derived reductions inHsf1-binding site frequency suggestcis-regulatory modifications to the classical heat shock response. Of note, turnover events within chaperone promoters were less frequent in the ancestral node of Antarctic notothens relative to younger Antarctic lineages. This suggests thatcis-regulatory divergence at chaperone promoters may be greater between Antarctic notothen lineages than between subpolar and Antarctic clades. These findings demonstrate that strong selective forces have acted uponcis-regulatory elements of chaperone genes among Antarctic notothens. 

Abstract Genomic methods are becoming increasingly valuable and established in ecological research, particularly in nonmodel species. Supporting their progress and adoption requires investment in resources that promote (i) reproducibility of genomic analyses, (ii) accessibility of learning tools and (iii) keeping pace with rapidly developing methods and principles.We introduce marineomics.io, an open‐source, living document to disseminate tutorials, reproducibility tools and best principles for ecological genomic research in marine and nonmodel systems.The website's existing content spans population and functional genomics, including current recommendations for whole‐genome sequencing, RAD‐seq, Pool‐seq and RNA‐seq. With the goal to facilitate the development of new, similar resources, we describe our process for aggregating and synthesizing methodological principles from the ecological genomics community to inform website content. We also detail steps for authorship and submission of new website content, as well as protocols for providing feedback and topic requests from the community.These web resources were constructed with guidance for doing rigorous, reproducible science. Collaboration and contributions to the website are encouraged from scientists of all skill sets and levels of expertise.