Rapid response to changing environments during biological invasions: DNA methylation perspectives

Abstract

Dissecting complex interactions between species and their environments has long been a research hot spot in the fields of ecology and evolutionary biology. The well-recognized Darwinian evolution has well-explained long-term adaptation scenarios; however, "rapid" processes of biological responses to environmental changes remain largely unexplored, particularly molecular mechanisms such as DNA methylation that have recently been proposed to play crucial roles in rapid environmental adaptation. Invasive species, which have capacities to successfully survive rapidly changing environments during biological invasions, provide great opportunities to study molecular mechanisms of rapid environmental adaptation. Here, we used the methylation-sensitive amplified polymorphism (MSAP) technique in an invasive model ascidian, Ciona savignyi, to investigate how species interact with rapidly changing environments at the whole-genome level. We detected quite rapid DNA methylation response: significant changes of DNA methylation frequency and epigenetic differentiation between treatment and control groups occurred only after 1 hr of high-temperature exposure or after 3 hr of low-salinity challenge. In addition, we detected time-dependent hemimethylation changes and increased intragroup epigenetic divergence induced by environmental stresses. Interestingly, we found evidence of DNA methylation resilience, as most stress-induced DNA methylation variation maintained shortly (~48 hr) and quickly returned back to the control levels. Our findings clearly showed that invasive species could rapidly respond to acute environmental changes through DNA methylation modifications, and rapid environmental changes left significant epigenetic signatures at the whole-genome level. All these results provide fundamental background to deeply investigate the contribution of DNA methylation mechanisms to rapid contemporary environmental adaptation.

Methylation divergence of invasive Ciona ascidians: Significant population structure and local environmental influence

“…The high level of intrapopulation methylation diversity can also be seen from the high values of Shannon index. Recent studies showed that environmental stresses could increase random methylation changes, leading to the high methylation divergence among individuals in the same populations (Huang et al., ; Morán et al., ; Richards et al., ). In a salt‐enriched experiment of brown trout ( Salmo trutta L.), genomewide methylation changes were triggered after feeding on salt‐enriched diets for 2 days, and the largest methylation differentiation was observed at the fourth day after treatment (Morán et al., ).…”

“…In a salt‐enriched experiment of brown trout ( Salmo trutta L.), genomewide methylation changes were triggered after feeding on salt‐enriched diets for 2 days, and the largest methylation differentiation was observed at the fourth day after treatment (Morán et al., ). Interestingly, our recent study showed that Ciona ascidians could respond to rapid changing environments in the methylation profile, such as after 1 hr of high temperature exposure or after 3 hr of low salinity challenge, and environmental changes increased intrapopulation methylation variation (Huang et al., ). Many studies clearly showed that environment‐induced DNA methylation variation was heritable, thus such a type of DNA methylation variation can be relatively steadily maintained in populations (see the review by Verhoeven et al., ).…”

“…Stress‐related methylation differentiation has been documented in experimental populations (Gao et al., ; Huang et al., ; Morán et al., ; Verhoeven et al., ). The stability of stress‐related DNA methylation variation varied from several hours to several generations (Herman, Spencer, Donohue, & Sultan, ; Huang et al., ). If the same advantageous phenotype arose every generation repeatedly by transient methylated modifications, such changes are expected to contribute to the interpopulation methylation differentiation in different environments (Schulz et al., ).…”

“…Studies based on both common garden experiments and populations collected from the wild have detected correlations between DNA methylation variation and environmental stresses, indicating the environmental influence on DNA methylation divergence. For example, greenhouse experiments have shown that various stresses, such as low nutrients, salt stress, dietary components, and pathogen attack, can induce methylation variation throughout the whole genome (Dowen et al., ; Huang et al., ; Morán, Marco‐Rius, Megías, Covelo‐Soto, & Pérez‐Figueroa, ; Platt, Gugger, Pellegrini, & Sork, ; Verhoeven, Jansen, van Dijk, & Biere, ). In the wild, DNA methylation differentiation among populations has been frequently observed in different environments (Gugger, Fitz‐Gibbon, Pellegrini, & Sork, ; Paun et al., ; Wenzel & Piertney, ).…”

“Winners” and “losers” in the Anthropocene: Understanding adaptation through phenotypic plasticity

“…The 9 months of being in aquarium conditions did not remove transcriptomic differences between the subtidal and intertidal groups. The epigenetic differences seen at the start of the transplant experiments did not persist, although the authors do acknowledge that they may have missed some methylation as it can be extensive across the genome (Huang et al., ).…”