Genetic and epigenetic differences associated with environmental gradients in replicate populations of two salt marsh perennials

Abstract

While traits and trait plasticity are partly genetically based, investigating epigenetic mechanisms may provide more nuanced understanding of the mechanisms underlying response to environment. Using AFLP and methylation-sensitive AFLP, we tested the hypothesis that differentiation to habitats along natural salt marsh environmental gradients occurs at epigenetic, but not genetic loci in two salt marsh perennials. We detected significant genetic and epigenetic structure among populations and among subpopulations, but we found multilocus patterns of differentiation to habitat type only in epigenetic variation for both species. In addition, more epigenetic than genetic loci were correlated with habitat in both species. When we analysed genetic and epigenetic variation simultaneously with partial Mantel, we found no correlation between genetic variation and habitat and a significant correlation between epigenetic variation and habitat in Spartina alterniflora. In Borrichia frutescens, we found significant correlations between epigenetic and/or genetic variation and habitat in four of five populations when populations were analysed individually, but there was no significant correlation between genetic or epigenetic variation and habitat when analysed jointly across the five populations. These analyses suggest that epigenetic mechanisms are involved in the response to salt marsh habitats, but also that the relationships among genetic and epigenetic variation and habitat vary by species. Site-specific conditions may also cloud our ability to detect response in replicate populations with similar environmental gradients. Future studies analysing sequence data and the correlation between genetic variation and DNA methylation will be powerful to identify the contributions of genetic and epigenetic response to environmental gradients.

Genetic and epigenetic variation in Spartina alterniflora following the Deepwater Horizon oil spill

“…Epigenotype diversity was high ( h‐ MSAFLP ranged from 0.089 to 0.222), and each individual displayed a unique epigenotype. Like the estimates for genetic patterns, there was no difference in epigenotype diversity between affected and unaffected sites ( p  =   .993), and as in our previous studies of S. alterniflora (Foust et al., 2016), h‐ MS‐AFLP tended to be lower than h‐ AFLP (Table 2). …”

“…However, we did not find evidence of decreased genetic diversity in contaminated populations, as nearly all individuals displayed a unique genotype in both contaminated and noncontaminated sites. These findings are consistent with other genetic surveys of S. alterniflora (Foust et al., 2016; Hughes & Lotterhos, 2014; Richards et al., 2004), which also show high levels of genetic variation. With our small sample size ( n  < 10 at most sites), it is possible that we were unable to capture a change in genetic diversity among populations if one occurred in response to the oil spill.…”

“…Our three contaminated sites fit the description of heavily oiled marshes, whereas the four uncontaminated sites had no visible oiling or impacted vegetation at the time samples were collected, and were not annotated as contaminated in the oil assessment databases. Samples were collected from the middle of the so‐called tall plant zone near the leading edge of the marsh (sensu “low‐salt habitat” in Foust et al., 2016). From each plant, we collected the 3rd fully expanded leaf to standardize age and minimize developmental bias in sampling.…”

“…These classic predictions are intuitive and often supported empirically (e.g., Clausen, Keck, & Hiesey, 1948). However, in some cases, data across a diversity of taxa show either no association of genetic differences with habitat (e.g., Richards, Hamrick, Donovan, & Mauricio, 2004; Foust et al., 2016; examples in Schmidt et al., 2008) or that low levels of molecular diversity are not associated with decreased phenotypic variation (Dlugosch & Parker, 2008; Richards et al., 2008). The disconnect between empirical findings and ecological theory suggests the possibility of additional, underexplored molecular mechanisms, such as epigenetic modifications, that mediate the relationship between phenotype and environment.…”

“…We measured genetic and epigenetic variation using amplified fragment length polymorphism (AFLP) and methylation sensitive fragment length polymorphism (MS‐AFLP) to test the hypothesis that oil exposure in S. alterniflora resulted in genetic and epigenetic signatures of population differentiation. As in previous studies of S. alterniflora (Edwards, Travis, & Proffitt, 2005; Foust et al., 2016; Hughes & Lotterhos, 2014; Richards et al., 2004; Travis, Proffitt, & Ritland, 2004), we expected to see high levels of genetic and epigenetic variation. However, we anticipated that moderate, nonrandom differential mortality in response to oil exposure would result in genetic differentiation of oil‐exposed populations from unexposed populations.…”