bioRxiv Science⌕ Search

Biology subjects

Bogan, S. N.

Publications and source records attributed to Bogan, S. N..

5 recordsLinked to original sources

Tissue-specific plasticity of DNA methylation across intertidal microhabitats in juvenile mussels (Mytilus californianus)

Epigenetic modifications to DNA are proposed to underpin plastic responses to environmental change, and the manner in which DNA methylation contributes to plasticity likely differs among tissues. However, few studies have investigated tissue-specific DNA methylation responses to ecologically relevant environmental stressors in natural settings. Here, we used reduced representation bisulfite sequencing on foot and gill to examine the influence of in situ microhabitats on DNA methylation in juvenile California mussels (Mytilus californianus), a foundation species with widespread dispersal and little evidence of genetic population structure. We examined mussels from a one-month reciprocal transplant experiment between a cool, wave-exposed and a warm, wave-protected microhabitat. These manipulations, which were previously shown to alter juvenile mussels heat tolerance, led to significant and highly tissue-specific changes in CpG methylation, including within a number of genes with roles in stress response pathways. Differentially methylated genes were involved in processes including heat shock response, proteolysis, DNA repair, and temperature sensing. In gill, differentially methylated CpGs were more likely to occur in introns relative to other inter- and intragenic features. This study expands on previous research that examined environmentally driven shifts in DNA methylation by documenting plastic and tissue-specific changes in DNA methylation between microhabitats in a natural setting.

genomics↗

Mitigating assembly and switch errors in phased genomes of polar fishes reveals haplotype diversity in copy number of antifreeze protein genes

Phased genomes and pangenomes are enhancing our understanding of genetic variation. Accurate phasing and assembly in repetitive regions of the genome remain challenging, however. Addressing this obstacle is crucial for studying structural genomic variation such as copy number variations (CNVs) common to repetitive regions. Polar fishes, for example, evolved repetitive tandem arrays of antifreeze protein (AFP) genes that facilitated adaptation to freezing and expanded in copy number in colder environments. AFP CNVs remain poorly characterized in polar fishes and may be illuminated by haplotype-aware approaches. We performed long-read sequencing of two polar fishes in the suborder Zoarcoidei and leveraged published long-read data to assemble phased genomes. We developed a workflow to measure haplotype diversity in CNV while controlling for misassembly and switch errors--a change from one parental haplotype to another in a contiguous assembly. We present gfa_parser, which computes and extracts all possible contiguous sequences for phased or primary assemblies from graphical fragment assembly files, and switch_error_screen, which flags potential switch errors. gfa_parser revealed that assembly uncertainty was ubiquitous across AFP array haplotypes and that standard processing of graphical fragment assemblies can bias measurement of haplotype CNVs. We detected no switch errors in AFP arrays. After controlling for misassembly and switch error, we detected haplotype diversity of AFP CNVs in all studied polar Zoarcoidei species and in 60% of AFP arrays. Intraindividual haplotype diversity spanned differences of 3-16 copies. Our workflow revealed intraspecific genomic diversity in zoarcoids that likely fueled evolution of AFP copy number across temperature.

genomics↗

Transgenerational effects alter the fitness consequences and genetic architecture of phenotypic plasticity and its regulatory pathways

Transgenerational effects, where parental environments influence offspring phenotype, facilitate acclimation over ecological timescales. Transgenerational effects may also influence evolution by altering the fitness costs of offspring traits and the expression of genetic variation. We tested the evolutionary role of transgenerational effects in the sea urchin Strongylocentrotus purpuratus, whose populations are exposed to coastal upwelling (periods of low temperature and pH) and exhibit local adaptation, parental effects, and phenotypic plasticity in response to upwelling. Using a quantitative genetic breeding design, we conditioned parents and larvae to upwelling or control conditions and combined RNA-seq with larval phenotyping (body size, biomineralization, survival). Larval upwelling exposure caused widespread differential expression (DE), reduced biomineralization, and reduced size. Survival was linked to biomineralization, body size, and their plasticity under upwelling, but only in offspring of upwelling-conditioned parents -evidence that parental environment affected selection on offspring traits. DE under upwelling was associated with adaptive plasticity in biomineralization and size, but adaptive gene expression changes shared negative genetic correlations. However, genetic correlations in gene expression associated with body size plasticity were significantly more positive in larvae from upwelling parents. Parental conditioning strengthened selection on offspring performance and reduced genetic tradeoffs between performance-associated expression pathways, potentially accelerating adaptation.

evolutionary biology↗

Temperature and Pressure Shaped the Evolution of Antifreeze Proteins in Polar and Deep Sea Zoarcoid Fishes

Antifreeze proteins (AFPs) have enabled teleost fishes to repeatedly colonize polar seas. Four AFP types have convergently evolved in several fish lineages. AFPs inhibit ice crystal growth and lower cellular freezing point. In lineages with AFPs, species inhabiting colder environments may possess more AFP copies. Elucidating how differences in AFP copy number evolve is challenging due to the genes tandem array structure and consequently poor resolution of these repetitive regions. Here we explore the evolution of type III AFPs (AFP III) in the globally distributed suborder Zoarcoidei, leveraging six new long-read genome assemblies. Zoarcoidei has fewer genomic resources relative to other polar fish clades while it is one of the few groups of fishes adapted to both the Arctic and Southern Oceans. Combining these new assemblies with additional long-read genomes available for Zoarcoidei, we conducted a comprehensive phylogenetic test of AFP III evolution and modeled the effects of thermal habitat and depth on AFP III gene family evolution. We confirm a single origin of AFP III via neofunctionalization of the enzyme sialic acid synthase B and show that AFP copies expanded under low temperature, but also decreased with depth, which reduces freezing point via pressure. Associations between the environment and AFP III copy number were driven by duplications of paralogs that were translocated out of the ancestral locus at which Zoarcoidei AFP arose. Our results reveal novel environmental effects on AFP evolution and demonstrate the value of high-quality genomic resources for studying how structural genomic variation shapes convergent adaptation.

evolutionary biology↗

Gene regulation by DNA methylation is contingent on chromatin accessibility during transgenerational plasticity in the purple sea urchin

Epigenetic processes are proposed to contribute to phenotypic plasticity. In invertebrates, DNA methylation commonly varies across environments and can correlate or causally associate with phenotype, but its role in transcriptional responses to the environment remains unclear. Maternal environments experienced by the sea urchin Strongylocentrotus purpuratus induce 3 - 6x greater differential CpG methylation in offspring larvae relative to larval developmental environments, suggesting a role for DNA methylation in transgenerational plasticity (TGP). However, a negligible association has been observed between differentially methylated and differentially expressed genes. What gene regulatory roles does invertebrate DNA methylation possess under environmental change, if any? We quantified DNA methylation and gene expression in S. purpuratus larvae exposed to different ecologically relevant conditions during gametogenesis (maternal conditioning) or embryogenesis (developmental conditioning). We modeled differential gene expression and differential splicing under maternal conditioning as functions of DNA methylation, incorporating variables for genomic feature and chromatin accessibility. We detected significant interactions between differential methylation, chromatin accessibility, and genic architecture associated with differential expression and splicing. Observed transcriptional responses to maternal conditioning were also 4 - 13x more likely when accounting for interactions between methylation and chromatin accessibility. Our results provide evidence that DNA methylation possesses multiple functional roles during TGP in S. purpuratus, but its effects are contingent upon other genomic and epigenomic states. Singularly unpredictive of transcription, DNA methylation is likely one cog in the epigenomic machinery contributing to environmental responses and phenotypic plasticity in S. purpuratus and other invertebrates.

genomics↗