Genome-Wide DNA Methylation Profiling Reveals Epigenetic Adaptation of Stickleback to Marine and Freshwater Conditions

Abstract

The three-spined stickleback (Gasterosteus aculeatus) represents a convenient model to study microevolution-adaptation to a freshwater environment. Although genetic adaptations to freshwater environments are well-studied, epigenetic adaptations have attracted little attention. In this work, we investigated the role of DNA methylation in the adaptation of the marine stickleback population to freshwater conditions. DNA methylation profiling was performed in marine and freshwater populations of sticklebacks, as well as in marine sticklebacks placed into a freshwater environment and freshwater sticklebacks placed into seawater. We showed that the DNA methylation profile after placing a marine stickleback into fresh water partially converged to that of a freshwater stickleback. For six genes including ATP4A ion pump and NELL1, believed to be involved in skeletal ossification, we demonstrated similar changes in DNA methylation in both evolutionary and short-term adaptation. This suggested that an immediate epigenetic response to freshwater conditions can be maintained in freshwater population. Interestingly, we observed enhanced epigenetic plasticity in freshwater sticklebacks that may serve as a compensatory regulatory mechanism for the lack of genetic variation in the freshwater population. For the first time, we demonstrated that genes encoding ion channels KCND3, CACNA1FB, and ATP4A were differentially methylated between the marine and the freshwater populations. Other genes encoding ion channels were previously reported to be under selection in freshwater populations. Nevertheless, the genes that harbor genetic and epigenetic changes were not the same, suggesting that epigenetic adaptation is a complementary mechanism to selection of genetic variants favorable for freshwater environment.

Environmental influences on life history strategies in partially anadromous brown trout (Salmo trutta, Salmonidae)

“…Furthermore, it has been shown that salt-induced alterations in DNA methylation patterns play a role in sea water adaptation in fishes (Artemov et al, 2017;Moran, Marco-Rius, Megías, Covelo-Soto, & Pérez-Figueroa, 2013). One may hypothesize that early environmental factors may also influence life-history decisions and phenotypic plasticity in brown trout, although this has not yet been investigated.…”

Synthesizing the role of epigenetics in the response and adaptation of species to climate change in freshwater ecosystems

“…An exception is the study of Artemov et al. (), who investigated the role of DNA methylation in the adaptation of populations of the marine stickleback ( Gasterosteus aculeatus ) to freshwater conditions. Notably, the DNA methylation profile of marine sticklebacks transferred into freshwater partially converged to that of a freshwater stickleback, with the genes encoding ion channels (KCND3, CACNA1FB and ATP4A) being differentially methylated between the marine and the freshwater populations.…”

“…For example, Kumar and Wigge (2010) showed that the short- Varriale (2014) The levels of methylation of warm-blooded species were consistently lower than those of the cold-blooded vertebrates Garg, Chevala, Shankar, and Jain (2015) Reported that the role of DNA methylation patterns are typically associated with genes important for abiotic stress responses in three rice (Oryza sativa) cultivars (IR64, stresssensitive; Nagina 22, drought-tolerant; Pokkali, salinity-tolerant) Artemov et al (2017) Genes encoding ion channels (KCND3, CACNA1FB and ATP4A) were differentially methylated between a marine and the freshwater populations of the winter skate (Leucoraja ocellata) Sun et al (2016) Both females and males from the Nile tilapia (Oreochromis niloticus) showed an increase in methylation levels on various chromosomes after high-temperature exposure Lighten et al (2016) Epigenetic mechanisms determined the different profiles of gene expression and life-history traits of two recently diverged populations of the winter skate (Leucoraja ocellata)…”

“…While the previous findings helped to unveil the circumstances and mechanisms leading to the rise of epigenetically determined phenotypes in vertebrates, their maintenance and stable transmission over evolutionary times remains largely unexplored among freshwater ecosystems. An exception is the study ofArtemov et al (2017), who investigated the role of DNA methylation in the adaptation of populations of the marine stickleback (Gas-…”

Genome‐scale sampling suggests cryptic epigenetic structuring and insular divergence in Canada lynx

“…DNA methylation has been implicated in mediating ecologically relevant traits in response to varied environmental conditions (Artemov et al, ; Baerwald et al, ; Lea, Altmann, Alberts, & Tung, ), primarily due to its regulatory relationship with gene expression, particularly around CpG islands that are dense clusters of cytosine‐guanine dinucleotides (Fujita et al, ; Lorincz, Dickerson, Schmitt, & Groudine, ; Maunakea et al, ). If heritable epigenetic modifications are imparted by specific environments, and these modifications increase fitness regardless of underlying genetic sequence (Herman & Sultan, ), then these epigenetic loci have important long‐term evolutionary consequences (Hu & Barrett, ).…”