The expansion of invasive species challenges our understanding of the process of adaptation. Given that the invasion process often entails population bottlenecks, it is surprising that many invasives appear to thrive even with low levels of sequence-based genetic variation. Using Amplified Fragment Length Polymorphism (AFLP) and methylation sensitive-AFLP (MS-AFLP) markers, we tested the hypothesis that differentiation of invasive Japanese knotweed in response to new habitats is more correlated with epigenetic variation than DNA sequence variation. We found that the relatively little genetic variation present was differentiated among species, with less differentiation among sites within species. In contrast, we found a great deal of epigenetic differentiation among sites within each species and evidence that some epigenetic loci may respond to local microhabitat conditions. Our findings indicate that epigenetic effects could contribute to phenotypic variation in genetically depauperate invasive populations. Deciphering whether differences in methylation patterns are the cause or effect of habitat differentiation will require manipulative studies.

Invasion of diverse habitats by few Japanese knotweed genotypes is correlated with epigenetic differentiation

Rapid adaptation of invasive species to novel habitats has puzzled evolutionary biologists for decades, especially as this often occurs in the face of limited genetic variability. Although some ecological traits common to invasive species have been identified, little is known about the possible genomic/genetic mechanisms that may underlie their success. A common scenario in many introductions is that small founder population sizes will often lead to reduced genetic diversity, but that invading populations experience large environmental perturbations, such as changes in habitat and environmental stress. Although sudden and intense stress is usually considered in a negative context, these perturbations may actually facilitate rapid adaptation by affecting genome structure, organization and function via interactions with transposable elements (TEs), especially in populations with low genetic diversity. Stress-induced changes in TE activity can alter gene action and can promote structural variation that may facilitate the rapid adaptation observed in new environments. We focus here on the adaptive potential of TEs in relation to invasive species and highlight their role as powerful mutational forces that can rapidly create genetic diversity. We hypothesize that activity of transposable elements can explain rapid adaptation despite low genetic variation (the genetic paradox of invasive species), and provide a framework under which this hypothesis can be tested using recently developed and emerging genomic technologies.

Transposable elements as agents of rapid adaptation may explain the genetic paradox of invasive species

Although there is keen interest in the potential adaptive value of epigenetic variation, it is unclear what conditions favor the stability of these variants either within or across generations. Because epigenetic modifications can be environmentally sensitive, existing theory on adaptive phenotypic plasticity provides relevant insights. Our consideration of this theory suggests that stable maintenance of environmentally induced epigenetic states over an organism's lifetime is most likely to be favored when the organism accurately responds to a single environmental change that subsequently remains constant, or when the environmental change cues an irreversible developmental transition. Stable transmission of adaptive epigenetic states from parents to offspring may be selectively favored when environments vary across generations and the parental environment predicts the offspring environment. The adaptive value of stability beyond a single generation of parent-offspring transmission likely depends on the costs of epigenetic resetting. Epigenetic stability both within and across generations will also depend on the degree and predictability of environmental variation, dispersal patterns, and the (epi)genetic architecture underlying phenotypic responses to environment. We also discuss conditions that favor stability of random epigenetic variants within the context of bet hedging. We conclude by proposing research directions to clarify the adaptive significance of epigenetic stability.

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How stable 'should' epigenetic modifications be? insights from adaptive plasticity and bet hedging

The spread of invasive species presents a genetic paradox: how do individuals overcome the genetic barriers associated with introductions (e.g., bottlenecks and founder effects) to become adapted to the new environment? In addition to genetic diversity, epigenetic variation also contributes to phenotypic variation and could influence the spread of an introduced species in novel environments. This may occur through two different (non-mutually exclusive) mechanisms. Individuals may benefit from existing (and heritable) epigenetic diversity or de novo epigenetic marks may increase in response to the new environment; both mechanisms might increase flexibility in new environments. Although epigenetic changes in invasive plants have been described, no data yet exist on the epigenetic changes throughout a range expansion of a vertebrate. Here, we used methylation sensitive-amplified fragment length polymorphism to explore genome-wide patterns of methylation in an expanding population of house sparrows (Passer domesticus). House sparrows were introduced to Kenya in the 1950s and have significant phenotypic variation dependent on the time since colonization. We found that Kenyan house sparrows had high levels of variation in methylation across the genome. Interestingly, there was a significant, potentially compensatory relationship between epigenetic and genetic diversity: epigenetic diversity was negatively correlated with genetic diversity and positively correlated with inbreeding across the range expansion. Thus, methylation may increase phenotypic variation and/or plasticity in response to new environments and therefore be an important source of inter-individual variation for adaptation in these environments, particularly over the short timescales over which invasions occur.

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Patterns of DNA Methylation Throughout a Range Expansion of an Introduced Songbird

DNA methylation is an important, heritable epigenetic modification in most eukaryotic organisms that is connected with numerous biological processes. To study the impact of natural epigenetic variation in an ecological or evolutionary context, epigenetic studies are increasingly using methylation-sensitive amplification polymorphism (MSAP) for surveys at the population or species level. However, no consensus exists on how to interpret and score the multistate information obtained from the MSAP banding patterns. Here, we review the previously used scoring approaches for population epigenetic studies and develop new alternatives. To assess effects of the different approaches on parameters of epigenetic diversity and differentiation, we applied eight scoring schemes to a case study of three populations of the plant species Viola elatior. For a total number of 168 detected polymorphic MSAP fragments, the number of ultimately scored polymorphic epiloci ranged between 78 and 286 depending on the particular scoring scheme. Both, estimates of epigenetic diversity and differentiation varied strongly between scoring approaches. However, linear regression and PCoA revealed qualitatively similar patterns, suggesting that the scoring approaches are largely consistent. For single-locus analyses of MSAP data, for example the search for loci under selection, we advocate a new scoring approach that separately takes into account different methylation types and thus seems appropriate for drawing more detailed conclusions in ecological or evolutionary contexts. An R script (MSAP_score.r) for scoring and basic data analysis is provided.

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Scoring and analysis of methylation‐sensitive amplification polymorphisms for epigenetic population studies

Epigenetic mechanisms impact several phenotypic traits and may be important for ecology and evolution. The introduced house sparrow (Passer domesticus) exhibits extensive phenotypic variation among and within populations. We screened methylation in populations from Kenya and Florida to determine if methylation varied among populations, varied with introduction history (Kenyan invasion <50 years old, Florida invasion ~150 years old), and could potentially compensate for decrease genetic variation with introductions. While recent literature has speculated on the importance of epigenetic effects for biological invasions, this is the first such study among wild vertebrates. Methylation was more frequent in Nairobi, and outlier loci suggest that populations may be differentiated. Methylation diversity was similar between populations, in spite of known lower genetic diversity in Nairobi, which suggests that epigenetic variation may compensate for decreased genetic diversity as a source of phenotypic variation during introduction. Our results suggest that methylation differences may be common among house sparrows, but research is needed to discern whether methylation impacts phenotypic variation.

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Epigenetic Variation May Compensate for Decreased Genetic Variation with Introductions: A Case Study Using House Sparrows ( Passer domesticus ) on Two Continents

Michael T. Grispo

Papers

Epigenetic Variation May Compensate for Decreased Genetic Variation with Introductions: A Case Study Using House Sparrows ( Passer domesticus ) on Two Continents