Epigenetic signatures of invasive status in populations of marine invertebrates

Abstract

Epigenetics, as a DNA signature that affects gene expression and enables rapid reaction of an organism to environmental changes, is likely involved in the process of biological invasions. DNA methylation is an epigenetic mechanism common to plants and animals for regulating gene expression. In this study we show, for the first time in any marine species, significant reduction of global methylation levels during the expansive phase of a pygmy mussel (Xenostrobus securis) recent invasion in Europe (two-year old), while in older introductions such epigenetic signature of invasion was progressively reduced. Decreased methylation was interpreted as a rapid way of increasing phenotypic plasticity that would help invasive populations to thrive. This epigenetic signature of early invasion was stronger than the expected environmental signature of environmental stress in younger populations sampled from ports, otherwise detected in a much older population (>90 year old) of the also invasive tubeworm Ficopomatus enigmaticus established in similar locations. Higher epigenetic than genetic diversity found in X. securis was confirmed from F. enigmaticus samples. As reported for introduced plants and vertebrates, epigenetic variation could compensate for relatively lower genetic variation caused by founder effects. These phenomena were compared with epigenetic mechanisms involved in metastasis, as parallel processes of community (biological invasion) and organism (cancer) invasions.

Link between epigenetic diversity and invasive status of south‐eastern European populations of phytopathogenic fungus Cryphonectria parasitica

“…As the population resides for a longer period in some area, the level of methylation increases due to accumulation of epigenetic changes. The same pattern has been observed in populations of marine invasive invertebrates (Ardura et al, ). In their study, Ardura et al .…”

“…In their study, Ardura et al . () demonstrated reduction in DNA methylation in a new population of Pygmy mussel during the expansion, while populations of older introductions showed higher levels of methylation. They obtained similar results analysing populations of the invasive Australian tubeworm.…”

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

“…For C. robusta and C. intestinalis , a great proportion of subepiloci was polymorphic, especially for m‐subepiloci (79.03%–92.40% in C. robusta , 81.39%–94.39% in C. intestinalis ). The ratios of polymorphic loci were higher than those in other species, such as the tubeworm F. enigmaticus where only 50% of the methylation‐susceptible loci were polymorphic (Ardura et al., ). A study on a rare floodplain herb Viola elatior showed that the polymorphism among populations ranged from 22.7% to 61.8% for u‐subepiloci and varied from 30.6% to 61.8% for methylated subepiloci (Schulz, Eckstein, & Durka, ).…”

“…Liebl, Schrey, Richards, and Martin () inferred that high methylation diversity could compensate for reduced genetic diversity during the invasion process of the house sparrow Passer domesticus . Interestingly, introduced populations of bluegrass Poa annua tended to have higher levels of methylation diversity than native populations (Chwedorzewska & Bednarek, ), and studies of the pygmy mussel ( Xenostrobus securis ) and tubeworm ( Ficopomatus enigmaticus ) found that recently introduced populations seemed to be less methylated in comparison with older introduced populations (Ardura, Zaiko, Morán, Planes, & Garcia‐Vazquez, ). Importantly, studies of invasive plants have also detected the association between DNA methylation variation and different habitats (Gao et al., ; Richards et al., ), and the authors further identified habitat‐related methylated loci (Richards et al., ).…”

Local parasite pressures and host genotype modulate epigenetic diversity in a mixed‐mating fish

“…To test the relationship between genome‐wide variation in DNA methylation and parasite loads, the proportion of methylated loci per individual was calculated as the proportion of loci scored as methylated over the total number of loci observed per individual (“0” for unmethylated and “1” for methylated, excluding the missing data cells per individual). The proportion (or percentage) of methylated loci has been previously used to analyze differences in epigenetic profiles among groups (Ardura, Zaiko, Morán, Planes, & Garcia‐Vazquez, ; Groot, Wagemaker, Ouborg, Verhoeven, & Vergeer, ; Veerger et al, ), and has shown both inter‐ and intraspecific variation (Alonso, Pérez, Bazaga, Medrano, & Herrera, ). We then employed a generalized linear model with a binomial link to model proportion of methylated loci as a function of scaled parasite load, selfing lineage, sampling site, and inbreeding status.…”