DNA methylation differences during development distinguish sympatric morphs of Arctic charr (Salvelinus alpinus)

Abstract

Changes in DNA methylation in specific coding or non‐coding regions can influence development and potentially divergence in traits within species and groups. While the impact of epigenetic variation on developmental pathways associated with evolutionary divergence is the focus of intense investigation, few studies have looked at recently diverged systems. Phenotypic diversity between closely related populations of Arctic charr (Salvelinus alpinus), which diverged within the last 10,000 years, offers an interesting ecological model to address such effects. Using bisulphite sequencing, we studied general DNA methylation patterns during development in the four sympatric morphs of Arctic charr from Lake Thingvallavatn. The data revealed strong differences between developmental timepoints and between morphs (mainly along the benthic–limnetic axis), both at single CpG sites and in 1000 bp‐regions. Genes located close to differentially methylated CpG sites were involved in nucleosome assembly, regulation of osteoclast differentiation, and cell‐matrix adhesion. Differentially methylated regions were enriched in tRNA and rRNA sequences, and half of them were located close to transcription start sites. The expression of 14 genes showing methylation differences over time or between morphs was further investigated by qPCR and nine of these were found to be differentially expressed between morphs. Four genes (ARHGEF37‐like, H3‐like, MPP3 and MEGF9) showed a correlation between methylation and expression. Lastly, histone gene clusters displayed interesting methylation differences between timepoints and morphs, as well as intragenic methylation variation. The results presented here provide a motivation for further studies on the contribution of epigenetic traits, such as DNA methylation, to phenotypic diversity and developmental mechanisms.

Diversity in the internal functional feeding elements of sympatric morphs of Arctic charr (Salvelinus alpinus)

“…Indeed, RNA-sequencing of embryos (PL-, LB- and SB-charr) reared in a common garden revealed ~2000 genes to be differentially expressed by morphs during development (from formation of the gill-arches to establishment of the viscerocranium primordia) (Guðbrandsson et al, 2018). Similarly, the developmental methylome differs (for the same developmental window), mainly between benthic and pelagic morphs in the lake (Matlosz et al, 2022). Finally, the developmental miRNA transcriptome differs by genotype in one study comparing SB-charr to aquaculture charr (Kapralova et al, 2014).…”

Epigenetic and genetic differentiation betweenCoregonusspecies pairs

“…Previous studies have shown that methylation is affected by temperature (Anastasiadi et al 2017; Metzger and Schulte 2017; Ryu et al 2018; McCaw et al 2020; Venney et al 2022), salinity (Artemov et al 2017; Heckwolf et al 2020), rearing environment (Le Luyer et al 2017; Gavery et al 2018; Leitwein et al 2021; Wellband et al 2021), and other factors. Differences in habitat use can influence DNA methylation, as observed between capelin ( Mallotus villosus ) utilizing beach- and demersal-spawning life history tactics (Venney et al in press ), among sympatric Arctic charr morphs occupying different habitats and dietary niches (Matlosz et al 2022), between phenotypically divergent cichlid species (Vernaz et al 2022), and in freshwater snails ( Potamopyrgus antipodarum ) which exhibit differences in shell shape associated with water current speed (Thorson et al 2017). DNA methylation can also be influenced by genetic variation (Richards 2006; Lallias et al 2021), therefore epigenetic differences may in part be driven by genetic divergence between species.…”

“…Previous studies have shown that methylation is affected by temperature (Ryu et al 2018;Venney et al 2022;Metzger & Schulte 2017;McCaw et al 2020;Anastasiadi et al 2017), salinity (Heckwolf et al 2020;Artemov et al 2017), rearing environment (Leitwein et al 2021;Le Luyer et al 2017;Wellband et al 2021;Gavery et al 2018), and other factors in various systems. Differences in habitat use can influence DNA methylation, as observed between capelin (Mallotus villosus) utilizing beach-and demersal-spawning life history tactics (Venney et al 2023), among sympatric Arctic charr morphs occupying different habitats and dietary niches (Matlosz et al 2022), between phenotypically divergent cichlid species (Vernaz et al 2022), and in freshwater snails (Potamopyrgus antipodarum) which exhibit differences in shell shape associated with water current speed (Thorson et al 2017).…”

“…DNA methylation is highly sensitive to the environment, with differences in temperature (McCaw et al 2020; Ryu et al 2020; Beemelmanns et al 2021; Venney et al 2022), salinity (Artemov et al 2017; Heckwolf et al 2020; Hu et al 2021), rearing environment (Le Luyer et al 2017; Berbel-Filho et al 2020; Venney et al 2020; Leitwein et al 2021; Wellband et al 2021), and other factors leading to epigenetic changes. DNA methylation can often alter phenotype (Anastasiadi et al 2021; Vogt 2021), with evidence for phenotypically-linked epigenetic divergence associated with spawning life history tactics in capelin ( Mallotus villosus ; Venney et al in press ) and between four sympatric Arctic charr morphs (Matlosz et al 2022). Due to the role of DNA methylation in plasticity and phenotypic diversification, it may contribute to speciation (Vogt 2017; Laporte et al 2019; Ashe et al 2021; Stajic and Jansen 2021).…”

“…DNA methylation is sensitive to the environment and epigenetic marks are known to be affected by several factors such as temperature (Ryu et al 2020; Beemelmanns et al 2021; McCaw et al 2020; Venney et al 2022), salinity (Hu et al 2021; Artemov et al 2017; Heckwolf et al 2020), and rearing environment (Leitwein et al 2021; Le Luyer et al 2017; Wellband et al 2021; Berbel-Filho et al 2020; Venney et al 2020). DNA methylation can alter phenotype (Anastasiadi et al 2021; Vogt 2021), with evidence for phenotypically-linked epigenetic divergence associated with spawning tactics in capelin ( Mallotus villosus ; (Venney et al 2023) and between four sympatric Arctic charr morphs (Matlosz et al 2022). Due to the potential role of DNA methylation in plasticity and phenotypic diversification, it may contribute to speciation (Vogt 2017; Ashe et al 2021; Stajic & Jansen 2021; Laporte et al 2019).…”