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.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
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.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
During range expansions, organisms can use epigenetic mechanisms to adjust to conditions in novel areas by altering gene expression and enabling phenotypic plasticity. Here, we predicted that the ...number of CpG sites within the genome, one form of epigenetic potential, would be important for successful range expansions because DNA methylation can modulate gene expression and, consequently, plasticity. We asked how the number of CpG sites and DNA methylation varied across five locations in the ∼70-year-old Kenyan house sparrow (Passer domesticus) range expansion. We found that the number of CpG sites was highest toward the vanguard of the invasion and decreased toward the range core. Analysis suggests that this pattern may have been driven by selection, favoring birds with more CpG sites at the range edge. However, we cannot rule out other processes, including nonrandom gene flow. Additionally, DNA methylation did not change across the range expansion, nor was it more variable. We hypothesize that as new areas are colonized, epigenetic potential may be selectively advantageous early but eventually be replaced by less plastic and perhaps genetically canalized traits as populations adapt to local conditions. Although further work is needed on epigenetic potential, this form (CpG number) appears to be a promising mechanism to investigate as a driver of expansions via capacitated phenotypic plasticity in other natural and anthropogenic range expansions.
Epigenetic changes associated with early life conditions are known to play a significant role in shaping the adult phenotype. Studies of DNA methylation in wild animals are lacking, yet are important ...for understanding the fitness consequences of environmentally induced epigenetic change. In our study, we quantified variation in DNA methylation in wild, post‐hatch zebra finches Taeniopygia guttata developing at seasonally variable temperatures in the Australian desert. We also compared variation in DNA methylation among captive zebra finch siblings raised in temperature controlled ‘hot’ or ‘cool’ rooms. We detected an increase in genome‐wide levels of DNA methylation between day 3 and day 11 of post hatch development in wild zebra finches. In the wild, ambient temperatures were also found to affect genome‐wide levels of DNA methylation and plasticity in the methylation state of individual loci. Family effects had a significant influence on DNA methylation throughout our study, and while we did not detect an effect of temperature on DNA methylation levels in non‐related captive birds, our sibling pair analyses revealed that within families, elevated temperatures were associated with higher levels of DNA methylation. Our findings suggest a wide window in early development during which climatically induced variation in DNA methylation could occur. Further work is necessary to understand the potential for such variation to promote ecologically relevant variation in wild birds.
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DOBA, FZAB, GIS, IJS, IZUM, KILJ, NLZOH, NUK, OILJ, PILJ, PNG, SAZU, SBCE, SBMB, UILJ, UKNU, UL, UM, UPUK
Telomere length and DNA methylation (DNAm) are two promising biomarkers of biological age. Environmental factors and life history traits are known to affect variation in both these biomarkers, ...especially during early life, yet surprisingly little is known about their reciprocal association, especially in natural populations. Here, we explore how variation in DNAm, growth rate, and early‐life conditions are associated with telomere length changes during development. We tested these associations by collecting data from wild, nestling zebra finches in the Australian desert. We found that increases in the level of DNAm were negatively correlated with telomere length changes across early life. We also confirm previously documented effects of post hatch growth rate and clutch size on telomere length in a natural ecological context for a species that has been extensively studied in the laboratory. However, we did not detect any effect of ambient temperature during developmental on telomere length dynamics. We also found that the absolute telomere length of wild zebra finches, measured using the in‐gel TRF method, was similar to that of captive birds. Our findings highlight exciting new opportunities to link and disentangle potential relationships between DNA based biomarkers of ageing, and of physiological reactions to environmental change.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Individuals may delay dispersing from their natal habitat, even after maturation to adulthood. Such delays can have broad consequences from determining population structure to allowing an individual ...to gain indirect fitness by helping parents rear future offspring. Dispersal in species that use delayed dispersal is largely thought to be opportunistic; however, how individuals, particularly inexperienced juveniles, assess their environments to determine the appropriate time to disperse is unknown. One relatively unexplored possibility is that dispersal decisions are the result of epigenetic mechanisms interacting between a genome and environment during development to generate variable dispersive phenotypes. Here, we tested this using epiRADseq to compare genome-wide levels of DNA methylation of blood in cooperatively breeding chestnut-crowned babblers (Pomatostomus ruficeps). We measured dispersive and philopatric individuals at hatching, before fledging, and at 1 year (following when first year dispersal decisions would be made). We found that individuals that dispersed in their first year had a reduced proportion of methylated loci than philopatric individuals before fledging, but not at hatching or as adults. Further, individuals that dispersed in the first year had a greater number of loci change methylation state (i.e. gain or lose) between hatching and fledging. The existence and timing of these changes indicate some influence of development on epigenetic changes that may influence dispersal behavior. However, further work needs to be done to address exactly how developmental environments may be associated with dispersal decisions and which loci in particular are manipulated to generate such changes.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
During range expansions, organisms are often exposed to multiple pressures, including novel enemies (i.e., predators, competitors and/or parasites) and unfamiliar or limited resources. Additionally, ...small propagule sizes at range edges can result in genetic founder effects and bottlenecks, which can affect phenotypic diversity and thus selection. Despite these obstacles, individuals in expanding populations often thrive at the periphery of a range, and this success may be mediated by phenotypic plasticity. Increasing evidence suggests that epigenetic mechanisms may underlie such plasticity because they allow for more rapid phenotypic responses to novel environments than are possible via the accumulation of genetic variation. Here, we review how molecular epigenetic mechanisms could facilitate plasticity in range-expanding organisms, emphasizing the roles of DNA methylation and other epigenetic marks in the physiological regulatory networks that drive whole-organism performance. We focus on the hypothalamic-pituitary-adrenal (HPA) axis, arguing that epigenetically-mediated plasticity in the regulation of glucocorticoids in particular might strongly impact range expansions. We hypothesize that novel environments release and/or select for epigenetic potential in HPA variation and hence organismal performance and ultimately fitness.
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BFBNIB, NMLJ, NUK, PNG, SAZU, UL, UM, UPUK
Epigenetic mechanisms may play a central role in mediating phenotypic plasticity, especially during range expansions, when populations face a suite of novel environmental conditions. Individuals may ...differ in their epigenetic potential (EP; their capacity for epigenetic modifications of gene expression), which may affect their ability to colonize new areas. One form of EP, the number of CpG sites, is higher in introduced house sparrows (
) than in native birds in the promoter region of a microbial surveillance gene, Toll-like Receptor 4 (
), which may allow invading birds to fine-tune their immune responses to unfamiliar parasites. Here, we compared
gene expression from whole blood, liver and spleen in house sparrows with different EP, first challenging some birds with lipopolysaccharide (LPS), to increase gene expression by simulating a natural infection. We expected that high EP would predict high inducibility and reversibility of
expression in the blood of birds treated with LPS, but we did not make directional predictions regarding organs, as we could not repeatedly sample these tissues. We found that EP was predictive of
expression in all tissues. Birds with high EP expressed more
in the blood than individuals with low EP, regardless of treatment with LPS. Only females with high EP exhibited reversibility in gene expression. Further, the effect of EP varied between sexes and among tissues. Together, these data support EP as one regulator of
expression.
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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BFBNIB, NMLJ, NUK, PNG, SAZU, UL, UM, UPUK
The marine aquarium trade in the United States operates primarily in Florida, and though the trade’s effects on many marine taxa are largely unknown, local declines have been observed for some ...harvested species. To reverse local declines in the abundance of the giant Caribbean sea anemone
Condylactis gigantea
, state managers prohibited harvest of this popular aquarium organism in late 2012. To assess the recovery of
C. gigantea
following the moratorium, we monitored relative abundance at 45 fixed locations in South Florida from 2013 to 2016. Seventeen of the sites were locations provided to us by commercial aquarium-trade collectors. The remaining sites were locations at which
C. gigantea
was presumably not being exploited. We found increased densities at only 4 of those 17 sites, while densities at the remaining sites remained unchanged. We also examined genome-wide single nucleotide polymorphism data to assess genetic diversity and population structure of 82 individuals from seven locations (three collection and four non-collection locations) across South Florida. Observed genetic diversity was comparable in all locations. But the location in the eastern Gulf of Mexico showed a significant F
IS
value, suggesting inbreeding that might be attributed to a small number of occupants.
Condylactis gigantea
is generally well mixed across South Florida, though a relatively weak pattern of genetic differentiation was detected. These results suggest limited reproductive success and dispersal that is restricted by hydrological and geographical barriers. We highlight the importance of periodic population and genetic monitoring to assess changes in relative abundance and genetic diversity.
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EMUNI, FIS, FZAB, GEOZS, GIS, IJS, IMTLJ, KILJ, KISLJ, MFDPS, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, SBMB, SBNM, UKNU, UL, UM, UPUK, VKSCE, ZAGLJ
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