Aaron W. Schrey

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

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.

Ten years of transcriptomics in wild populations: what have we learned about their ecology and evolution?

Molecular ecology has moved beyond the use of a relatively small number of markers, often noncoding, and it is now possible to use whole‐genome measures of gene expression with microarrays and RNAseq (i.e. transcriptomics) to capture molecular response to environmental challenges. While transcriptome studies are shedding light on the mechanistic basis of traits as complex as personality or physiological response to catastrophic events, these approaches are still challenging because of the required technical expertise, difficulties with analysis and cost. Still, we found that in the last 10 years, 575 studies used microarrays or RNAseq in ecology. These studies broadly address three questions that reflect the progression of the field: (i) How much variation in gene expression is there and how is it structured? (ii) How do environmental stimuli affect gene expression? (iii) How does gene expression affect phenotype? We discuss technical aspects of RNAseq and microarray technology, and a framework that leverages the advantages of both. Further, we highlight future directions of research, particularly related to moving beyond correlation and the development of additional annotation resources. Measuring gene expression across an array of taxa in ecological settings promises to enrich our understanding of ecology and genome function.

Ecological Epigenetics: Beyond MS-AFLP

Ecological Epigenetics studies the relationship between epigenetic variation and ecologically relevant phenotypic variation. As molecular epigenetic mechanisms often control gene expression, even across generations, they may impact many evolutionary processes. Multiple molecular epigenetic mechanisms exist, but methylation of DNA so far has dominated the Ecological Epigenetic literature. There are several molecular techniques used to screen methylation of DNA; here, we focus on the most common technique, methylation-sensitive-AFLP (MS-AFLP), which is used to identify genome-wide methylation patterns. We review studies that used MS-AFLP to address ecological questions, that describe which taxa have been investigated, and that identify general trends in the field. We then discuss, noting the general themes, four studies across taxa that demonstrate characteristics that increase the inferences that can be made from MS-AFLP data; we suggest that future MS-AFLP studies should incorporate these methods and techniques. We then review the short-comings of MS-AFLP and suggest alternative techniques that might address some of these limitations. Finally, we make specific suggestions for future research on MS-AFLP and identify questions that are most compelling and tractable in the short term.

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

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.

Broad‐scale latitudinal patterns of genetic diversity among native European and introduced house sparrow (Passer domesticus) populations

Introduced species offer unique opportunities to study evolution in new environments, and some provide opportunities for understanding the mechanisms underlying macroecological patterns. We sought to determine how introduction history impacted genetic diversity and differentiation of the house sparrow (Passer domesticus), one of the most broadly distributed bird species. We screened eight microsatellite loci in 316 individuals from 16 locations in the native and introduced ranges. Significant population structure occurred between native than introduced house sparrows. Introduced house sparrows were distinguished into one North American group and a highly differentiated Kenyan group. Genetic differentiation estimates identified a high magnitude of differentiation between Kenya and all other populations, but demonstrated that European and North American samples were differentiated too. Our results support previous claims that introduced North American populations likely had few source populations, and indicate house sparrows established populations after introduction. Genetic diversity also differed among native, introduced North American, and Kenyan populations with Kenyan birds being least diverse. In some cases, house sparrow populations appeared to maintain or recover genetic diversity relatively rapidly after range expansion (<50 years; Mexico and Panama), but in others (Kenya) the effect of introduction persisted over the same period. In both native and introduced populations, genetic diversity exhibited large‐scale geographic patterns, increasing towards the equator. Such patterns of genetic diversity are concordant with two previously described models of genetic diversity, the latitudinal model and the species diversity model.

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

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.

Adaptive plasticity and epigenetic variation in response to warming in an Alpine plant

Environmentally induced phenotypic plasticity may be a critical component of response to changing environments. We examined local differentiation and adaptive phenotypic plasticity in response to elevated temperature in half-sib lines collected across an elevation gradient for the alpine herb, Wahlenbergia ceracea. Using Amplified Fragment Length Polymorphism (AFLP), we found low but significant genetic differentiation between low- and high-elevation seedlings, and seedlings originating from low elevations grew faster and showed stronger temperature responses (more plasticity) than those from medium and high elevations. Furthermore, plasticity was more often adaptive for plants of low-elevation origin and maladaptive for plants of high elevation. With methylation sensitive-AFLP (MS-AFLP), we revealed an increase in epigenetic variation in response to temperature in low-elevation seedlings. Although we did not find significant direct correlations between MS-AFLP loci and phenotypes, our results demonstrate that adaptive plasticity in temperature response to warming varies over fine spatial scales and suggest the involvement of epigenetic mechanisms in this response.

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

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.

Fire increases variance in genetic characteristics of Florida Sand Skink (Plestiodon reynoldsi) local populations

Fire is a complex event that maintains many ecological systems. The Florida Sand Skink (Plestiodon reynoldsi) is precinctive to Florida Scrub, a habitat that is maintained by infrequent fire. We characterize the effect of fire on genetic diversity and genetic differentiation at eight microsatellite loci in the Florida Sand Skink (n = 470) collected from 30 replicate sites over three ‘time since last fire’ categories at the Archbold Biological Station. Long unburned sites had greater allelic richness and expected heterozygosity than either recently or intermediately burned sites. More recently, burned sites had greater standard deviations of allelic richness and private allelic richness. Expected heterozygosity positively correlated with ‘time since fire’ (r = 0.36, P = 0.05) and abundance (r = 0.53, P = 0.002). There was a significant spatial component to genetic differentiation, and results indicate individuals rarely disperse >1 km. Genetic differentiation was positively correlated with geographic distance in long unburned units (r = 0.59, P = 0.04), yet this relationship was disrupted by fire in recently (r = 0.00, 1) and intermediately (r = −0.81, 0.05) burned areas. Simulations indicate that demographic changes to a local population could have generated the observed differences among ‘time since fire’ categories. Our findings indicate that infrequent fire may be beneficial to the Florida Sand Skink and that local populations begin to recover from changes attributable to the fire after 10 years. Too frequent fires may reduce genetic diversity because it may take multiple generations for local populations to recover.

Surveillance for microbes and range expansion in house sparrows

Interactions between hosts and parasites influence the success of host introductions and range expansions post-introduction. However, the physiological mechanisms mediating these outcomes are little known. In some vertebrates, variation in the regulation of inflammation has been implicated, perhaps because inflammation imparts excessive costs, including high resource demands and collateral damage upon encounter with novel parasites. Here, we tested the hypothesis that variation in the regulation of inflammation contributed to the spread of house sparrows (Passer domesticus) across Kenya, one of the worlds most recent invasions of this species. Specifically, we asked whether inflammatory gene expression declines with population age (i.e. distance from Mombasa (dfM), the site of introduction around 1950). We compared expression of two microbe surveillance molecules (Toll-like receptors, TLRs-2 and 4) and a proinflammatory cytokine (interleukin-6, IL-6) before and after an injection of an immunogenic component of Gram-negative bacteria (lipopolysaccharide, LPS) among six sparrow populations. We then used a best-subset model selection approach to determine whether population age (dfM) or other factors (e.g. malaria or coccidian infection, sparrow density or genetic group membership) best-explained gene expression. For baseline expression of TLR-2 and TLR-4, population age tended to be the best predictor with expression decreasing with population age, although other factors were also important. Induced expression of TLRs was affected by LPS treatment alone. For induced IL-6, only LPS treatment reliably predicted expression; baseline expression was not explained by any factor. These data suggest that changes in microbe surveillance, more so than downstream control of inflammation via cytokines, might have been important to the house sparrow invasion of Kenya.