Landscape‐scale variation in an anthropogenic factor shapes immune gene variation within a wild population

Understanding the spatial scale at which selection acts upon adaptive genetic variation in natural populations is fundamental to our understanding of evolutionary ecology, and has important ramifications for conservation. The environmental factors to which individuals of a population are exposed can vary at fine spatial scales, potentially generating localized patterns of adaptation. Here, we compared patterns of neutral and major histocompatibility complex (MHC) variation within an island population of Berthelot's pipit (Anthus berthelotii) to assess whether landscape‐level differences in pathogen‐mediated selection generate fine‐scale spatial structuring in these immune genes. Specifically, we tested for spatial associations between the distribution of avian malaria, and the factors previously shown to influence that distribution, and MHC variation within resident individuals. Although we found no overall genetic structure across the population for either neutral or MHC loci, we did find localized associations between environmental factors and MHC variation. One MHC class I allele (ANBE48) was directly associated with malaria infection risk, while the presence of the ANBE48 and ANBE38 alleles within individuals correlated (positively and negatively, respectively) with distance to the nearest poultry farm, an anthropogenic factor previously shown to be an important determinant of disease distribution in the study population. Our findings highlight the importance of considering small spatial scales when studying the patterns and processes involved in evolution at adaptive loci.     

Phenotypic plasticity in gene expression contributes to divergence of locally adapted populations of Fundulus heteroclitus

We examine the interaction between phenotypic plasticity and evolutionary adaptation using muscle gene expression levels among populations of the fish Fundulus heteroclitus acclimated to three temperatures. Our analysis reveals shared patterns of phenotypic plasticity due to thermal acclimation as well as non‐neutral patterns of variation among populations adapted to different thermal environments. For the majority of significant differences in gene expression levels, phenotypic plasticity and adaptation operate on different suites of genes. The subset of genes that demonstrate both adaptive differences and phenotypic plasticity, however, exhibit countergradient variation of expression. Thus, expression differences among populations counteract environmental effects, reducing the phenotypic differentiation between populations. Finally, gene‐by‐environment interactions among genes with non‐neutral patterns of expression suggest that the penetrance of adaptive variation depends on the environmental conditions experienced by the individual.     

The biology hidden inside residual within‐individual phenotypic variation

Phenotypes vary hierarchically among taxa and populations, among genotypes within populations, among individuals within genotypes, and also within individuals for repeatedly expressed, labile phenotypic traits. This hierarchy produces some fundamental challenges to clearly defining biological phenomena and constructing a consistent explanatory framework. We use a heuristic statistical model to explore two consequences of this hierarchy. First, although the variation existing among individuals within populations has long been of interest to evolutionary biologists, within‐individual variation has been much less emphasized. Within‐individual variance occurs when labile phenotypes (behaviour, physiology, and sometimes morphology) exhibit phenotypic plasticity or deviate from a norm‐of‐reaction within the same individual. A statistical partitioning of phenotypic variance leads us to explore an array of ideas about residual within‐individual variation. We use this approach to draw attention to additional processes that may influence within‐individual phenotypic variance, including interactions among environmental factors, ecological effects on the fitness consequences of plasticity, and various types of adaptive variance. Second, our framework for investigating variation in phenotypic variance reveals that interactions between levels of the hierarchy form the preconditions for the evolution of all types of plasticity, and we extend this idea to the residual level within individuals, where both adaptive plasticity in residuals and canalization‐like processes (stability) can evolve. With the statistical tools now available to examine heterogeneous residual variance, an array of novel questions linking phenotype to environment can be usefully addressed.     

Genetic diversity and differentiation at MHC genes in island populations of tuatara (Sphenodon spp.)

Neutral genetic markers are commonly used to understand the effects of fragmentation and population bottlenecks on genetic variation in threatened species. Although neutral markers are useful for inferring population history, the analysis of functional genes is required to determine the significance of any observed geographical differences in variation. The genes of the major histocompatibility complex (MHC) are well‐known examples of genes of adaptive significance and are particularly relevant to conservation because of their role in pathogen resistance. In this study, we survey diversity at MHC class I loci across a range of tuatara populations. We compare the levels of MHC variation with that observed at neutral microsatellite markers to determine the relative roles of balancing selection, diversifying selection and genetic drift in shaping patterns of MHC variation in isolated populations. In general, levels of MHC variation within tuatara populations are concordant with microsatellite variation. Tuatara populations are highly differentiated at MHC genes, particularly between the northern and Cook Strait regions, and a trend towards diversifying selection across populations was observed. However, overall our results indicate that population bottlenecks and isolation have a larger influence on patterns of MHC variation in tuatara populations than selection.     

Differences in prey personality mediate trophic cascades

Functional trait approaches in ecology chiefly assume the mean trait value of a population adequately predicts the outcome of species interactions. Yet this assumption ignores substantial trait variation among individuals within a population, which can have a profound effect on community structure and function. We explored individual trait variation through the lens of animal personality to test whether among‐individual variation in prey behavior mediates trophic interactions. We quantified the structure of personalities within a population of generalist grasshoppers and examined, through a number of field and laboratory‐based experiments, how personality types could impact tri‐trophic interactions in a food chain. Unlike other studies of this nature, we used spatial habitat domains to evaluate how personality types mechanistically map to behaviors relevant in predator–prey dynamics and found shy and bold individuals differed in both their habitat use and foraging strategy under predation risk by a sit‐and‐wait spider predator. In the field‐based mesocosm portion of our study, we found experimental populations of personality types differed in their trophic impact, demonstrating that prey personality can mediate trophic cascades. We found no differences in respiration rates or body size between personality types used in the mesocosm experiment, indicating relative differences in trophic impact were not due to variation in prey physiology but rather variation in behavioral strategies. Our work demonstrates how embracing the complexity of individual trait variation can offer mechanistically richer understanding of the processes underlying trophic interactions.     

An integrated framework to identify wildlife populations under threat from climate change

Climate change is a major threat to global biodiversity that will produce a range of new selection pressures. Understanding species responses to climate change requires an interdisciplinary perspective, combining ecological, molecular and environmental approaches. We propose an applied integrated framework to identify populations under threat from climate change based on their extent of exposure, inherent sensitivity due to adaptive and neutral genetic variation and range shift potential. We consider intraspecific vulnerability and population‐level responses, an important but often neglected conservation research priority. We demonstrate how this framework can be applied to vertebrates with limited dispersal abilities using empirical data for the bat Plecotus austriacus. We use ecological niche modelling and environmental dissimilarity analysis to locate areas at high risk of exposure to future changes. Combining outlier tests with genotype–environment association analysis, we identify potential climate‐adaptive SNPs in our genomic data set and differences in the frequency of adaptive and neutral variation between populations. We assess landscape connectivity and show that changing environmental suitability may limit the future movement of individuals, thus affecting both the ability of populations to shift their distribution to climatically suitable areas and the probability of evolutionary rescue through the spread of adaptive genetic variation among populations. Therefore, a better understanding of movement ecology and landscape connectivity is needed for predicting population persistence under climate change. Our study highlights the importance of incorporating genomic data to determine sensitivity, adaptive potential and range shift potential, instead of relying solely on exposure to guide species vulnerability assessments and conservation planning.     

Adaptation in temporally variable environments: stickleback armor in periodically breaching bar‐built estuaries

The evolutionary consequences of temporal variation in selection remain hotly debated. We explored these consequences by studying threespine stickleback in a set of bar‐built estuaries along the central California coast. In most years, heavy rains induce water flow strong enough to break through isolating sand bars, connecting streams to the ocean. New sand bars typically re‐form within a few weeks or months, thereby re‐isolating populations within the estuaries. These breaching events cause severe and often extremely rapid changes in abiotic and biotic conditions, including shifts in predator abundance. We investigated whether this strong temporal environmental variation can maintain within‐population variation while eroding adaptive divergence among populations that would be caused by spatial variation in selection. We used neutral genetic markers to explore population structure and then analysed how stickleback armor traits, the associated genes Eda and Pitx1 and elemental composition (%P) varies within and among populations. Despite strong gene flow, we detected evidence for divergence in stickleback defensive traits and Eda genotypes associated with predation regime. However, this among‐population variation was lower than that observed among other stickleback populations exposed to divergent predator regimes. In addition, within‐population variation was very high as compared to populations from environmentally stable locations. Elemental composition was strongly associated with armor traits, Eda genotype and the presence of predators, thus suggesting that spatiotemporal variation in armor traits generates corresponding variation in elemental phenotypes. We conclude that gene flow, and especially temporal environmental variation, can maintain high levels of within‐population variation while reducing, but not eliminating, among‐population variation driven by spatial environmental variation.     

LANDSCAPE GENOMICS IN ATLANTIC SALMON (SALMO SALAR): SEARCHING FOR GENE–ENVIRONMENT INTERACTIONS DRIVING LOCAL ADAPTATION

A growing number of studies are examining the factors driving historical and contemporary evolution in wild populations. By combining surveys of genomic variation with a comprehensive assessment of environmental parameters, such studies can increase our understanding of the genomic and geographical extent of local adaptation in wild populations. We used a large‐scale landscape genomics approach to examine adaptive and neutral differentiation across 54 North American populations of Atlantic salmon representing seven previously defined genetically distinct regional groups. Over 5500 genome‐wide single nucleotide polymorphisms were genotyped in 641 individuals and 28 bulk assays of 25 pooled individuals each. Genome scans, linkage map, and 49 environmental variables were combined to conduct an innovative landscape genomic analysis. Our results provide valuable insight into the links between environmental variation and both neutral and potentially adaptive genetic divergence. In particular, we identified markers potentially under divergent selection, as well as associated selective environmental factors and biological functions with the observed adaptive divergence. Multivariate landscape genetic analysis revealed strong associations of both genetic and environmental structures. We found an enrichment of growth‐related functions among outlier markers. Climate (temperature–precipitation) and geological characteristics were significantly associated with both potentially adaptive and neutral genetic divergence and should be considered as candidate loci involved in adaptation at the regional scale in Atlantic salmon. Hence, this study significantly contributes to the improvement of tools used in modern conservation and management schemes of Atlantic salmon wild populations.     

Haplotype structure,adaptive history and associations with exploratory behaviour of the DRD4 gene region in four great tit (Parus major) populations

The assessment of genetic architecture and selection history in genes for behavioural traits is fundamental to our understanding of how these traits evolve. The dopamine receptor D4 (DRD4) gene is a prime candidate for explaining genetic variation in novelty seeking behaviour, a commonly assayed personality trait in animals. Previously, we showed that a single nucleotide polymorphism in exon 3 of this gene is associated with exploratory behaviour in at least one of four Western European great tit (Parus major) populations. These heterogeneous association results were explained by potential variable linkage disequilibrium (LD) patterns between this marker and the causal variant or by other genetic or environmental differences among the populations. Different adaptive histories are further hypothesized to have contributed to these population differences. Here, we genotyped 98 polymorphisms of the complete DRD4 gene including the flanking regions for 595 individuals of the four populations. We show that the LD structure, specifically around the original exon 3 SNP is conserved across the four populations and does not explain the heterogeneous association results. Study‐wide significant associations with exploratory behaviour were detected in more than one haplotype block around exon 2, 3 and 4 in two of the four tested populations with different allele effect models. This indicates genetic heterogeneity in the association between multiple DRD4 polymorphisms and exploratory behaviour across populations. The association signals were in or close to regions with signatures of positive selection. We therefore hypothesize that variation in exploratory and other dopamine‐related behaviour evolves locally by occasional adaptive shifts in the frequency of underlying genetic variants.     

Genetic by environmental variation but no local adaptation in oysters (Crassostrea virginica)

Functional trait variation within and across populations can strongly influence population, community, and ecosystem processes, but the relative contributions of genetic vs. environmental factors to this variation are often not clear, potentially complicating conservation and restoration efforts. For example, local adaptation, a particular type of genetic by environmental (G*E) interaction in which the fitness of a population in its own habitat is greater than in other habitats, is often invoked in management practices, even in the absence of supporting evidence. Despite increasing attention to the potential for G*E interactions, few studies have tested multiple populations and environments simultaneously, limiting our understanding of the spatial consistency in patterns of adaptive genetic variation. In addition, few studies explicitly differentiate adaptation in response to predation from other biological and environmental factors. We conducted a reciprocal transplant experiment of first‐generation eastern oyster (Crassostrea virginica) juveniles from six populations across three field sites spanning 1000 km in the southeastern Atlantic Bight in both the presence and absence of predation to test for G*E variation in this economically valuable and ecologically important species. We documented significant G*E variation in survival and growth, yet there was no evidence for local adaptation. Condition varied across oyster cohorts: Offspring of northern populations had better condition than offspring from the center of our region. Oyster populations in the southeastern Atlantic Bight differ in juvenile survival, growth, and condition, yet offspring from local broodstock do not have higher survival or growth than those from farther away. In the absence of population‐specific performance information, oyster restoration and aquaculture may benefit from incorporating multiple populations into their practices.     

REACTION NORMS OF MORPHOLOGICAL AND LIFE-HISTORY TRAITS TO LIGHT AVAILABILITY IN IMPATIENS CAPENSIS

For plants, light availability is an important environmental factor that varies both within and between populations. Although the existence of sun and shade “ecotypes” is controversial, it is often assumed that trade-offs may exist between performance in sun and in shade. This study therefore investigated variation in reaction norms to light availability within and between two neighboring natural populations of the annual Impatiens capensis, one in full sun and the other in a forest understory. Seedlings were collected randomly from both populations and grown to maturity in a greenhouse under two light conditions: full light and 18% of full light. Selfed full-sib seed families were collected from plants from both populations grown in both parental light environments. To characterize family reaction norms, seedlings from each family were divided into the same two light treatments and individuals were scored for a variety of morphological and life-history traits. The maternal light environment had little impact on progeny reaction norms. However, the two study populations differed both qualitatively and quantitatively in plastic response to light availability (indicated by significant population x environment interactions in mixed-model ANCOVA). Much of this difference was attributable to population differences in light sensitivity of axillary meristem allocation patterns, which produced concurrent differences in reaction norms for a suite of developmentally linked traits. Within each population, different sets of traits displayed significant variation in plasticity (indicated by significant family x environment interactions). Thus, the genetic potential for evolutionary response to selection in heterogeneous light environments may differ dramatically between neighboring plant populations. Between-environment genetic correlations were largely positive in the woods population and positive or nonsignificant in the sun population; there was no evidence for performance trade-offs across environments or sun or shade “specialist” genotypes within either population. There was little evidence that population differences represented adaptive differentiation for sun or shade; rather, the results suggested the hypothesis of differential selection on patterns of meristem allocation caused by population differences in timing of mortality and intensity of competition.     

The influence of population structure on gene expression and flowering time variation in the ubiquitous weed Capsella bursa‐pastoris (Brassicaceae)

Population structure is a potential problem when testing for adaptive phenotypic differences among populations. The observed phenotypic differences among populations can simply be due to genetic drift, and if the genetic distance between them is not considered, the differentiation may be falsely interpreted as adaptive. Conversely, adaptive and demographic processes might have been tightly associated and correcting for the population structure may lead to false negatives. Here, we evaluated this problem in the cosmopolitan weed Capsella bursa‐pastoris. We used RNA‐Seq to analyse gene expression differences among 24 accessions, which belonged to a much larger group that had been previously characterized for flowering time and circadian rhythm and were genotyped using genotyping‐by‐sequencing (GBS) technique. We found that clustering of accessions for gene expression retrieved the same three clusters that were obtained with GBS data previously, namely Europe, the Middle East and Asia. Moreover, the three groups were also differentiated for both flowering time and circadian rhythm variation. Correction for population genetic structure when analysing differential gene expression analysis removed all differences among the three groups. This may suggest that most differences are neutral and simply reflect population history. However, geographical variation in flowering time and circadian rhythm indicated that the distribution of adaptive traits might be confounded by population structure. To bypass this confounding effect, we compared gene expression differentiation between flowering ecotypes within the genetic groups. Among the differentially expressed genes, FLOWERING LOCUS C was the strongest candidate for local adaptation in regulation of flowering time.