Regional epigenetic variation in asexual snail populations among urban and rural lakes

Abstract

Epigenetic variation has the potential to influence environmentally dependent development and contribute to phenotypic responses to local environments. Environmental epigenetic studies of sexual organisms confirm the capacity to respond through epigenetic variation. An epigenetic response could be even more important in a population when genetic variation is lacking. A previous study of an asexual snail, Potamopyrgus antipodarum, demonstrated that different populations derived from a single clonal lineage differed in both shell phenotype and methylation signature when comparing lake versus river populations. Here, we examine methylation variation among lakes that differ in environmental disturbance and pollution histories. Snails were collected from a more pristine rural Lake 1 (Lake Lytle), and two urban lakes, Lake 2 (Capitol Lake) and Lake 3 (Lake Washington) on the Northwest Pacific coast. DNA methylation was assessed for each sample population using methylated DNA immunoprecipitation, MeDIP, followed by next-generation sequencing. The differential DNA methylation regions (DMRs) identified among the different lake comparisons suggested a higher number of DMRs and variation between rural Lake 1 and one urban Lake 2, and between the two urban Lakes 2 and 3, but limited variation between the rural Lake 1 and urban Lake 3. DMR genomic characteristics and gene associations were investigated. The presence of site-specific differences between each of these lake populations suggest an epigenetic response to varied environmental factors. The results do not support an effect of geographic distance in these populations. The role of dispersal distance among lakes, population history, environmental pollution and stably inherited methylation versus environmentally triggered methylation in producing the observed epigenetic variation are discussed. Observations support the proposal that epigenetic alterations may associate with phenotypic variation and environmental factors and history of the different lakes.

Role of environmentally induced epigenetic transgenerational inheritance in evolutionary biology: Unified Evolution Theory

“…Alteration of environmental conditions (i.e. water flow) was found to associate with adaptive phenotypic variation that correlated with epigenetic alterations [ 117 , 118 ]. Chrosomus eos-neogaeus is a hybrid clonal fish that inhabits lakes and intermittent stream environments that has epigenetic variation in the divergent environments [ 119 , 120 ].…”

Urbanization is associated with modifications in DNA methylation in a small passerine bird

“…Modifications in DNA methylation have been shown to associate with anthropogenic‐linked factors including feeding on anthropogenic‐provided food in baboons (Lea et al., 2016), exposure to pollution in humans (Baccarelli et al., 2009), and stress resilience in response to handling in tree swallows (Taff et al., 2019). A few studies have specifically investigated epigenetic variation in wild animals in the context of urbanization, revealing varied patterns (Garcia et al., 2019; McNew et al., 2017; Riyahi et al., 2015; Thorson et al., 2019).…”

Paradigm shifts in animal epigenetics: Research on non‐model species leads to new insights into dependencies, functions and inheritance of DNA methylation

“…The resulting populations have evolved habitat-specific differences in shell shape that were correlated with water current speed. [35,36] Methylated DNA immunoprecipitation (MeDIP) and Illumina sequencing of foot pad tissue from single specimens revealed significant genome-wide DNA methylation differences between lakes and rivers despite virtual genetic identity. [35,36] Epigenetic variation most likely helped to establish adaptive phenotypic plasticity in the invasive snail in less than 100 generations.…”

“…[35,36] Methylated DNA immunoprecipitation (MeDIP) and Illumina sequencing of foot pad tissue from single specimens revealed significant genome-wide DNA methylation differences between lakes and rivers despite virtual genetic identity. [35,36] Epigenetic variation most likely helped to establish adaptive phenotypic plasticity in the invasive snail in less than 100 generations. This example suggests that in asexual reproducers epigenetic variation is largely independent from genetic variation.…”