Genetic architecture and phenotypic plasticity are important considerations when studying trait variation within and among populations. Since environmental change can induce shifts in the genetic ...architecture and plasticity of traits, it is important to consider both genetic and environmental sources of phenotypic variation. While there is overwhelming evidence for environmental effects on phenotype, the underlying mechanisms are less clear. Variation in DNA methylation is a potential mechanism mediating environmental effects on phenotype due to its sensitivity to environmental stimuli, transgenerational inheritance, and influences on transcription. To characterize the effect of environment on methylation, we created two 6 × 6 (North Carolina II) Chinook salmon breeding crosses and reared the offspring in two environments: uniform hatchery tanks and seminatural stream channels. We sampled the fish twice during development, at the alevin (larval) and fry (juvenile) stages. We measured DNA methylation at 13 genes using a PCR-based bisulfite sequencing protocol. The genetic architecture of DNA methylation differed between rearing environments, with greater additive and nonadditive genetic variance in hatchery fish and greater maternal effects in seminatural channel fish, though gene-specific variation was evident. We observed plasticity in methylation across all assayed genes, as well as gene-specific effects at two genes in alevin and six genes in fry, indicating developmental stage-specific effects of rearing environment on methylation. Characterizing genetic and environmental influences on methylation is critical for future studies on DNA methylation as a potential mechanism for acclimation and adaptation.
Epigenetic inheritance can result in plastic responses to changing environments being faithfully transmitted to offspring. However, it remains unclear how epigenetic mechanisms such as DNA ...methylation can contribute to multigenerational acclimation and adaptation to environmental stressors. Brook charr (
), an economically important salmonid, is highly sensitive to thermal stress and is of conservation concern in the context of climate change. We studied the effects of temperature during parental sexual maturation and offspring rearing on whole-genome DNA methylation in brook charr juveniles (fry). Parents were split between warm and cold temperatures during sexual maturation, mated in controlled breeding designs, then offspring from each family were split between warm (8°C) and cold (5°C) rearing environments. Using whole-genome bisulfite sequencing, we found 188 differentially methylated regions (DMRs) due to parental maturation temperature after controlling for family structure. By contrast, offspring rearing temperature had a negligible effect on offspring methylation. Stable intergenerational inheritance of DNA methylation and minimal plasticity in progeny could result in the transmission of acclimatory epigenetic states to offspring, priming them for a warming environment. Our findings have implications pertaining to the role of intergenerational epigenetic inheritance in response to ongoing climate change.
Phenotypic plasticity buffers organisms from environmental change and is hypothesized to aid the initial establishment of nonindigenous species in novel environments and postestablishment range ...expansion. The genetic mechanisms that underpin phenotypically plastic traits are generally poorly characterized; however, there is strong evidence that modulation of gene transcription is an important component of these responses. Here, we use RNA sequencing to examine the transcriptional basis of temperature tolerance for round and tubenose goby, two nonindigenous fish species that differ dramatically in the extent of their Great Lakes invasions despite similar invasion dates. We used generalized linear models of read count data to compare gene transcription responses of organisms exposed to increased and decreased water temperature from those at ambient conditions. We identify greater response in the magnitude of transcriptional changes for the more successful round goby compared with the less successful tubenose goby. Round goby transcriptional responses reflect alteration of biological function consistent with adaptive responses to maintain or regain homeostatic function in other species. In contrast, tubenose goby transcription patterns indicate a response to stressful conditions, but the pattern of change in biological functions does not match those expected for a return to homeostatic status. Transcriptional plasticity plays an important role in the acute thermal tolerance for these species; however, the impaired response to stress we demonstrate in the tubenose goby may contribute to their limited invasion success relative to the round goby. Transcriptional profiling allows the simultaneous assessment of the magnitude of transcriptional response as well as the biological functions involved in the response to environmental stress and is thus a valuable approach for evaluating invasion potential.
The geographic range of an invasive species is a key determinant of relative impact in the invaded region. Comparison of invasive species that are widespread or rare in invaded ranges can highlight ...mechanistic traits that determine the risk of impact from invasion. Round Goby (Neogobius melanostomus) is more geographically widespread and abundant than Tubenose Goby (Proterorhinus semilunaris) across invaded ranges of the Laurentian Great Lakes. We used stable isotopes of carbon (δ¹³C) and nitrogen (δ¹⁵N) in liver and muscle to contrast the isotopic niche breadth and niche plasticity of Round Goby and Tubenose Goby near the inflow and outflow of Lake St. Clair and in western Lake Superior. At all sites, Round Goby and Tubenose Goby that matched in size (21–53 mm standard length) had distinct isotopic niches with no overlap, driven by higher δ¹⁵N in Round Goby. The variation in isotopic niche, and the mean difference in δ¹³C and δ¹⁵N between muscle and liver, was greater for Round Goby, suggesting both greater seasonal shifts in diet and niche plasticity in this more widely established invader. Round Goby that were significantly larger than Tubenose Goby had broader isotopic niches and greater niche plasticity in the majority of cases and this was associated with isotopic niche overlap with smaller Round Goby and Tubenose Goby. Our findings suggest that a broad and plastic isotopic niche provides scope for wider establishment range in invasive fish species.
Phenotypic differences among populations within a species have been reported for a variety of traits, ranging from life history to physiology to gene transcription. Population‐level phenotypic ...variation has been attributed to genetic differences resulting from genetic drift and/or local adaptation as well as environmental differences resulting from plasticity. We studied population‐ and family‐level variation in gene transcription for 22 fitness‐related genes, comprising immune, growth, metabolic, and stress processes in Chinook salmon (Oncorhynchus tshawytscha). We created hybrid Chinook salmon families from eight populations and treated them with an immune stimulus, a handling stress challenge, and held some as a no‐treatment control group. Population effects, sire effects, and narrow‐sense heritability (h2) were calculated for each candidate gene within each treatment group. We expected population to have a significant effect on gene transcription for many of our genes; however, we found a population effect for transcription at only one immune gene at rest. The limited number of significant population effects on gene transcription, combined with significant additive genetic variance within each population does not support the expectation of past strong selection pressures acting on heritable transcription profiles among populations. Instead, our results indicate that Chinook salmon likely adapt to their local environment through transcriptional plasticity rather than fixed differences. The expectation for fixed population‐level differences in gene transcription at fitness‐related genes, reflecting accepted models of local adaptation is high; however, comparisons among multiple populations using half‐sibling breeding designs are rare. Our work fills an important gap in our growing understanding of the process of among and within‐population divergence.
Animals are strongly connected to the environments they live in and may become adapted to local environments. Examining genetic–environment associations of key indicator species, like seabirds, ...provides greater insights into the forces that drive evolution in marine systems. Here we examined a RADseq dataset of 19,213 SNPs for 99 rhinoceros auklets (Cerorhinca monocerata) from five western Pacific and 10 eastern Pacific breeding colonies. We used partial redundancy analyses to identify candidate adaptive loci and to quantify the effects of environmental variation on population genetic structure. We identified 262 candidate adaptive loci, which accounted for 3.0% of the observed genetic variation among western Pacific and eastern Pacific breeding colonies. Genetic variation was more strongly associated with pH and maximum current velocity, than maximum sea surface temperature. Genetic–environment associations explain genetic differences between western and eastern Pacific populations; however, genetic variation within the western and eastern Pacific Ocean populations appears to follow a pattern of isolation‐by‐distance. This study represents a first to quantify the relationship between environmental and genetic variation for this widely distributed marine species and provides greater insights into the evolutionary forces that act on marine species.
Examining adaptive genetic variation of key indicator species, like seabirds, provides greater insights into the forces that drive evolution in marine systems. Here we examined a ddRAD dataset of 19,213 SNPs for 99 rhinoceros auklets (Cerorhinca monocerata) from five west Pacific and 10 east Pacific breeding colonies. Our analyses provide evidence for local adaption between western and eastern Pacific populations; however, we did not find evidence for local adaptation within populations from either the west Pacific or the east Pacific.
Abstract
An epigenetic basis for transgenerational plasticity in animals is widely theorized, but convincing empirical support is limited by taxa-specific differences in the presence and role of ...epigenetic mechanisms. In teleost fishes, DNA methylation generally does not undergo extensive reprogramming and has been linked with environmentally induced intergenerational effects, but solely in the context of early life environmental differences. Using whole-genome bisulfite sequencing, we demonstrate that differential methylation of sperm occurs in response to captivity during the maturation of Atlantic Salmon (Salmo salar), a species of major economic and conservation significance. We show that adult captive exposure further induces differential methylation in an F1 generation that is associated with fitness-related phenotypic differences. Some genes targeted with differential methylation were consistent with genes differential methylated in other salmonid fishes experiencing early-life hatchery rearing, as well as genes under selection in domesticated species. Our results support a mechanism of transgenerational plasticity mediated by intergenerational inheritance of DNA methylation acquired late in life for salmon. To our knowledge, this is the first-time environmental variation experienced later in life has been directly demonstrated to influence gamete DNA methylation in fish.
Invasive species are expected to experience a unique combination of high genetic drift due to demographic factors while also experiencing strong selective pressures. The paradigm that reduced genetic ...diversity should limit the evolutionary potential of invasive species, and thus, their potential for range expansion has received little empirical support, possibly due to the choice of genetic markers. Our goal was to test for effects of genetic drift and selection at functional genetic markers as they relate to the invasion success of two paired invasive goby species, one widespread (successful) and one with limited range expansion (less successful). We genotyped fish using two marker types: single nucleotide polymorphisms (SNPs) in known‐function, protein‐coding genes and microsatellites to contrast the effects of neutral genetic processes. We identified reduced allelic variation in the invaded range for the less successful tubenose goby. SNPs putatively under selection were responsible for the observed differences in population structure between marker types for round goby (successful) but not tubenose goby (less successful). A higher proportion of functional loci experienced divergent selection for round goby, suggesting increased evolutionary potential in invaded ranges may be associated with round goby's greater invasion success. Genes involved in thermal tolerance were divergent for round goby populations but not tubenose goby, consistent with the hypothesis that invasion success for fish in temperate regions is influenced by capacity for thermal tolerance. Our results highlight the need to incorporate functional genetic markers in studies to better assess evolutionary potential for the improved conservation and management of species.
Variation in gene transcription is widely believed to be the mechanistic basis of phenotypically plastic traits; however, comparatively little is known about the inheritance patterns of ...transcriptional variation that would allow us to predict its response to selection. In addition, acclimation to different environmental conditions influences acute transcriptional responses to stress and it is unclear if these effects are heritable. To address these gaps in knowledge, we assayed levels of messenger RNA for 14 candidate genes at rest and in response to a 24-h confinement stress for 72 half-sib families of Chinook salmon reared in two different environments (hatchery and semi-natural stream channel). We observed extensive plasticity for mRNA levels of metabolic and stress response genes and demonstrated that mRNA level plasticity due to rearing environment affects mRNA level plasticity in response to stress. These effects have important implications for natural populations experiencing multiple stressors. We identified genotype-by-environment interactions for mRNA levels that were dominated by maternal effects; however, mRNA level response to challenge also exhibited a non-additive genetic basis. Our results indicate that while plasticity for mRNA levels can evolve, predicting the outcome of selection will be difficult. The inconsistency in genetic architecture among treatment groups suggests there is considerable cryptic genetic variation for gene expression.
Captive‐breeding programs are among the most adopted conservation practices to mitigate the loss of biodiversity, including genetic diversity. However, both genetic and nongenetic changes occurring ...in captivity can reduce the fitness of supplemented individuals, which complicate rehabilitation efforts. In the case of Atlantic salmon, the intensity of changes that occur in captivity and their impact on fitness will vary with the stocking practice adopted. In this study, we test whether salmon stocked at the parr stage have reduced reproductive success compared with their wild conspecifics and whether they contribute to increase genetic diversity in the targeted population. To do so, we use high‐throughput microsatellite sequencing of 38 loci to accurately assign 2381 offspring to a comprehensive set of possible parents from a supplemented Atlantic salmon population in Québec, Canada. Captive‐bred salmon stocked at the parr stage had fewer mates than their wild conspecifics, as well as a reduced relative reproductive success (RSS) compared with their wild counterparts. Nonetheless, in comparison with previous studies, stocking at the parr stage significantly improved RSS compared with salmon stocked as smolts and they displayed a reduction in reproductive success similar to salmon stocked as fry, which spend less time in captivity than parr. Moreover, supplementation of captive‐bred salmon significantly contributed to increasing genetic diversity. These results should contribute to informing resource managers in determining the best stocking practice to enhance Atlantic salmon populations.
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