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.

Figure 1. DNA methylation in methylation-sensitive loci detected from all analyzed specimens of Xenostrobus securis, per population.

Type I to IV are respectively: no methylated, methylation of internal C, methylation of external C or hemimethylation, and hypermethylation or mutation in restriction site. Methylated: Global methylation level estimated following Nicotra et al. (Nicotra et al.41), as proportion of (Type II+Type III loci)/(scorable loci). The letters yo mean “year old”.

Figure 2. Two-dimensional visualization of the Principal Component Analysis (PCoA) of the detected methylation patterns in Xenostrobus securis, with the epigenetic variation (methylation-sensitive loci) on the left and the genetic variation (no methylated loci, NML) on the right.

The individuals of each population are represented by the acronyms XAtl, XCant and XMed for the Atlantic international port, Cantabric international port and Mediterranean lagoon populations respectively.

Figure 3. DNA methylation in methylation-sensitive loci detected from the analyzed specimens of Ficopomatus enigmaticus.

Type I to IV are respectively: no methylated, methylation of internal C, methylation of external C or hemimethylation, and hypermethylation or mutation in restriction site. Methylated: Global methylation level estimated following Nicotra et al., as proportion of (Type II+Type III loci)/(scorable loci). The letters yo mean “year old”.

Figure 4. Two-dimensional visualization of the Principal Component Analysis (PCoA) of the detected methylation patterns in Ficopomatus enigmaticus, with the epigenetic variation (methylation-sensitive loci) on the left and the genetic variation (no methylated loci, NML) on the right.

Each population is represented by the acronyms FNZ, FCant and FMed for samples, respectively, from the international Napier port in New Zealand, Cantabric fishing port and Mediterranean lagoon locations.