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

Abstract

The geographical expansion of invasive species usually leads to temporary and/or permanent changes at multiple levels (genetics, epigenetics, gene expression, etc.) to acclimatize to abiotic and/or biotic stresses in novel environments. Epigenetic variation such as DNA methylation is often involved in response to diverse local environments, thus representing one crucial mechanism to promote invasion success. However, evidence is scant on the potential role of DNA methylation variation in rapid environmental response and invasion success during biological invasions. In particular, DNA methylation patterns and possible contributions of varied environmental factors to methylation differentiation have been largely unknown in many invaders, especially for invasive species in marine systems where extremely complex interactions exist between species and surrounding environments. Using the methylation‐sensitive amplification polymorphism (MSAP) technique, here we investigated population methylation structure at the genome level in two highly invasive model ascidians, Ciona robusta and C. intestinalis, collected from habitats with varied environmental factors such as temperature and salinity. We found high intrapopulation methylation diversity and significant population methylation differentiation in both species. Multiple analyses, such as variation partitioning analysis, showed that both genetic variation and environmental factors contributed to the observed DNA methylation variation. Further analyses found that 24 and 20 subepiloci were associated with temperature and/or salinity in C. robusta and C. intestinalis, respectively. All these results clearly showed significant methylation divergence among populations of both invasive ascidians, and varied local environmental factors, as well as genetic variation, were responsible for the observed DNA methylation patterns. The consistent findings in both species here suggest that DNA methylation, coupled with genetic variation, may facilitate local environmental adaptation during biological invasions, and DNA methylation variation molded by local environments may contribute to invasion success.

Stress Memory of Recurrent Environmental Challenges in Marine Invasive Species: Ciona robusta as a Case Study

“…Biological invasions provide an excellent "natural experiment" to study how species cope with environmental stresses, as invasive species encounter sudden, and often repeated, extensive environmental challenges during the invasion process (Zhan et al, 2015;Ni et al, 2018). Particularly for human activity-mediated introductions, invasive species often encounter environmental changes much greater and/or faster than what species can experience under natural conditions such as seasonal fluctuations (Zhan et al, 2015;Chen et al, 2018a).…”

Epigenetic patterns associated with an ascidian invasion: a comparison of closely related clades in their native and introduced ranges

“…vexillum (New Zealand), but not in the native range (Japan). Recent studies of invasive populations have found DNA methylation differences between environments that may play a role in adaptation to different habitats 49,76,77 . In the present study, comparisons of DNA methylation patterns between sites with similar or different environmental stress (temperature and salinity) scores indicate that DNA methylation patterns are not driven by environmental variations alone.…”

Effect of a locally adapted genome on environmentally induced epigenetic variation

“…Only the sites hosting lineage C are not completely isolated from each other, but M04 and M05 are still 3.6 km apart and separated by a road and grasslands, which are typically avoided by Ambystoma salamanders [39]. Salamanders from the genus Ambystoma display strong fidelity to their breeding sites [40], and the dispersing individuals move on average only 150 m from their breeding ponds during breeding season, and rarely over 300 m [32, 39–42].…”