Adaptive Population Divergence Research Articles

Local adaptations and climate change: converging sensitivity of bud break in black spruce provenances.

Species with transcontinental distribution or spread over wide geographical regions develop populations with growth traits genetically adapted to the local climate. The aim of this study was to investigate the ecotypic sensitivity of bud break, a strong adaptive trait, to a changing environment. Six phenological phases of bud break were monitored daily on black spruce [Picea mariana (Mill.) BSP] seedlings submitted to different temperatures (12, 16 and 20 °C) and photoperiods (14, 18 and 22 h). Six provenances were tested in growth chambers, produced from seeds collected along the whole latitudinal range of the closed boreal forest in Quebec, Canada. Bud break lasted 13.3 days on average and occurred earlier in seedlings from colder sites. The annual temperature of the sites suitably tracked the clinal variation among ecotypes, providing a clear biological explanation for the environmental signal driving the adaptive divergence of populations to the local climate. Increasing temperature induced an earlier bud break according to a non-linear pattern with greater advancements observed between 12 and 16 °C. Photoperiod was significant, but sensitivity analysis indicated that its effect on bud break was marginal with respect to temperature. No interaction of provenance × treatment was observed, demonstrating an ecotypic convergence of the responses to both factors. Changes in the growing conditions could substantially modify the synchronization between bud phenology and climate, thus exposing the developing meristems of black spruce to frost damage. However, similar advancements of bud break could be expected in the different ecotypes subjected to warmer temperatures or longer day lengths.

Disentangling the role of phenotypic plasticity and genetic divergence in contemporary ecotype formation during a biological invasion.

The occurrence of contemporary ecotype formation through adaptive divergence of populations within the range of an invasive species typically requires standing genetic variation but can be facilitated by phenotypic plasticity. The relative contributions of both of these to adaptive trait differentiation have rarely been simultaneously quantified in recently diverging vertebrate populations. Here we study a case of intraspecific divergence into distinct lake and stream ecotypes of threespine stickleback that evolved in the past 140 years within the invasive range in Switzerland. Using a controlled laboratory experiment with full-sib crosses and treatments mimicking a key feature of ecotypic niche divergence, we test if the phenotypic divergence that we observe in the wild results from phenotypic plasticity or divergent genetic predisposition. Our experimental groups show qualitatively similar phenotypic divergence as those observed among wild adults. The relative contribution of plasticity and divergent genetic predisposition differs among the traits studied, with traits related to the biomechanics of feeding showing a stronger genetic predisposition, whereas traits related to locomotion are mainly plastic. These results implicate that phenotypic plasticity and standing genetic variation interacted during contemporary ecotype formation in this case.

GENETIC ARCHITECTURE OF SKELETAL EVOLUTION IN EUROPEAN LAKE AND STREAM STICKLEBACK

Advances in genomic techniques are greatly facilitating the study of molecular signatures of selection in diverging natural populations. Connecting these signatures to phenotypes under selection remains challenging, but benefits from dissections of the genetic architecture of adaptive divergence. We here perform quantitative trait locus (QTL) mapping using 488 F2 individuals and 2011 single nucleotide polymorphisms (SNPs) to explore the genetic architecture of skeletal divergence in a lake-stream stickleback system from Central Europe. We find QTLs for gill raker, snout, and head length, vertebral number, and the extent of lateral plating (plate number and height). Although two large-effect loci emerge, QTL effect sizes are generally small. Examining the neighborhood of the QTL-linked SNPs identifies several genes involved in bone formation, which emerge as strong candidate genes for skeletal evolution. Finally, we use SNP data from the natural source populations to demonstrate that some SNPs linked to QTLs in our cross also exhibit striking allele frequency differences in the wild, suggesting a causal role of these QTLs in adaptive population divergence. Our study paves the way for comparative analyses across other (lake-stream) stickleback populations, and for functional investigations of the candidate genes.

Signatures of selection in the Iberian honey bee (Apis mellifera iberiensis) revealed by a genome scan analysis of single nucleotide polymorphisms

Understanding the genetic mechanisms of adaptive population divergence is one of the most fundamental endeavours in evolutionary biology and is becoming increasingly important as it will allow predictions about how organisms will respond to global environmental crisis. This is particularly important for the honey bee, a species of unquestionable ecological and economical importance that has been exposed to increasing human-mediated selection pressures. Here, we conducted a single nucleotide polymorphism (SNP)-based genome scan in honey bees collected across an environmental gradient in Iberia and used four FST -based outlier tests to identify genomic regions exhibiting signatures of selection. Additionally, we analysed associations between genetic and environmental data for the identification of factors that might be correlated or act as selective pressures. With these approaches, 4.4% (17 of 383) of outlier loci were cross-validated by four FST -based methods, and 8.9% (34 of 383) were cross-validated by at least three methods. Of the 34 outliers, 15 were found to be strongly associated with one or more environmental variables. Further support for selection, provided by functional genomic information, was particularly compelling for SNP outliers mapped to different genes putatively involved in the same function such as vision, xenobiotic detoxification and innate immune response. This study enabled a more rigorous consideration of selection as the underlying cause of diversity patterns in Iberian honey bees, representing an important first step towards the identification of polymorphisms implicated in local adaptation and possibly in response to recent human-mediated environmental changes.

Are habitat fragmentation, local adaptation and isolation‐by‐distance driving population divergence in wild rice Oryza rufipogon?

Habitat fragmentation weakens the connection between populations and is accompanied with isolation by distance (IBD) and local adaptation (isolation by adaptation, IBA), both leading to genetic divergence between populations. To understand the evolutionary potential of a population and to formulate proper conservation strategies, information on the roles of IBD and IBA in driving population divergence is critical. The putative ancestor of Asian cultivated rice (Oryza sativa) is endangered in China due to habitat loss and fragmentation. We investigated the genetic variation in 11 Chinese Oryza rufipogon populations using 79 microsatellite loci to infer the effects of habitat fragmentation, IBD and IBA on genetic structure. Historical and current gene flows were found to be rare (mh =0.0002-0.0013, mc =0.007-0.029), indicating IBD and resulting in a high level of population divergence (FST =0.343). High within-population genetic variation (HE =0.377-0.515), relatively large effective population sizes (Ne = 96-158), absence of bottlenecks and limited gene flow were found, demonstrating little impact of recent habitat fragmentation on these populations. Eleven gene-linked microsatellite loci were identified as outliers, indicating local adaptation. Hierarchical AMOVA and partial Mantel tests indicated that population divergence of Chinese O.rufipogon was significantly correlated with environmental factors, especially habitat temperature. Common garden trials detected a significant adaptive population divergence associated with latitude. Collectively, these findings imply that IBD due to historical rather than recent fragmentation, followed by local adaptation, has driven population divergence in O.rufipogon.

Lack of parallel genetic patterns underlying the repeated ecological divergence of beach and stream‐spawning kokanee salmon

Recent progress in methods for detecting adaptive population divergence in situ shows promise for elucidating the conditions under which selection acts to generate intraspecific diversity. Rapid ecological diversification is common in fishes; however, the role of phenotypic plasticity and adaptation to local environments is poorly understood. It is now possible to investigate genetic patterns to make inferences regarding phenotypic traits under selection and possible mechanisms underlying ecotype divergence, particularly where similar novel phenotypes have arisen in multiple independent populations. Here, we employed a bottom-up approach to test for signatures of directional selection associated with divergence of beach- and stream-spawning kokanee, the obligate freshwater form of sockeye salmon (Oncorhynchus nerka). Beach- and stream-spawners co-exist in many post-glacial lakes and exhibit distinct reproductive behaviours, life-history traits and spawning habitat preferences. Replicate ecotype pairs across five lakes in British Columbia, Canada were genotyped at 57 expressed sequence tag-linked and anonymous microsatellite loci identified in a previous genome scan. Fifteen loci exhibited signatures of directional selection (high FST outliers), four of which were identified in multiple lakes. However, the lack of parallel genetic patterns across all lakes may be a result of: 1) an inability to detect loci truly under selection; 2) alternative genetic pathways underlying ecotype divergence in this system; and/or 3) phenotypic plasticity playing a formative role in driving kokanee spawning habitat differences. Gene annotations for detected outliers suggest pathogen resistance and energy metabolism as potential mechanisms contributing to the divergence of beach- and stream-spawning kokanee, but further study is required.

Strong selection genome-wide enhances fitness trade-offs across environments and episodes of selection.

Fitness trade-offs across episodes of selection and environments influence life-history evolution and adaptive population divergence. Documenting these trade-offs remains challenging as selection can vary in magnitude and direction through time and space. Here, we evaluate fitness trade-offs at the levels of the whole organism and the quantitative trait locus (QTL) in a multiyear field study of Boechera stricta (Brassicaceae), a genetically tractable mustard native to the Rocky Mountains. Reciprocal local adaptation was pronounced for viability, but not for reproductive components of fitness. Instead, local genomes had a fecundity advantage only in the high latitude garden. By estimating realized selection coefficients from individual-level data on viability and reproductive success and permuting the data to infer significance, we examined the genetic basis of fitness trade-offs. This analytical approach (Conditional Neutrality-Antagonistic Pleiotropy, CNAP) identified genetic trade-offs at a flowering phenology QTL (costs of adaptation) and revealed genetic trade-offs across fitness components (costs of reproduction). These patterns would not have emerged from traditional ANOVA-based QTL mapping. Our analytical framework can be applied to other systems to investigate fitness trade-offs. This task is becoming increasingly important as climate change may alter fitness landscapes, potentially disrupting fitness trade-offs that took many generations to evolve.

The spatial patterns of directional phenotypic selection

Local adaptation, adaptive population divergence and speciation are often expected to result from populations evolving in response to spatial variation in selection. Yet, we lack a comprehensive understanding of the major features that characterise the spatial patterns of selection, namely the extent of variation among populations in the strength and direction of selection. Here, we analyse a data set of spatially replicated studies of directional phenotypic selection from natural populations. The data set includes 60 studies, consisting of 3937 estimates of selection across an average of five populations. We performed meta-analyses to explore features characterising spatial variation in directional selection. We found that selection tends to vary mainly in strength and less in direction among populations. Although differences in the direction of selection occur among populations they do so where selection is often weakest, which may limit the potential for ongoing adaptive population divergence. Overall, we also found that spatial variation in selection appears comparable to temporal (annual) variation in selection within populations; however, several deficiencies in available data currently complicate this comparison. We discuss future research needs to further advance our understanding of spatial variation in selection.

High degree of genetic differentiation in marine three‐spined sticklebacks (Gasterosteus aculeatus)

Populations of widespread marine organisms are typically characterized by a low degree of genetic differentiation in neutral genetic markers, but much less is known about differentiation in genes whose functional roles are associated with specific selection regimes. To uncover possible adaptive population divergence and heterogeneous genomic differentiation in marine three-spined sticklebacks (Gasterosteus aculeatus), we used a candidate gene-based genome-scan approach to analyse variability in 138 microsatellite loci located within/close to (<6 kb) functionally important genes in samples collected from ten geographic locations. The degree of genetic differentiation in markers classified as neutral or under balancing selection-as determined with several outlier detection methods-was low (F(ST) = 0.033 or 0.011, respectively), whereas average FST for directionally selected markers was significantly higher (F(ST) = 0.097). Clustering analyses provided support for genomic and geographic heterogeneity in selection: six genetic clusters were identified based on allele frequency differences in the directionally selected loci, whereas four were identified with the neutral loci. Allelic variation in several loci exhibited significant associations with environmental variables, supporting the conjecture that temperature and salinity, but not optic conditions, are important drivers of adaptive divergence among populations. In general, these results suggest that in spite of the high degree of physical connectivity and gene flow as inferred from neutral marker genes, marine stickleback populations are strongly genetically structured in loci associated with functionally relevant genes.

A practical guide to measuring local adaptation

Patterns of local adaptation are expected to emerge when selection is spatially heterogeneous and sufficiently strong relative to the action of other evolutionary forces. The observation of local adaptation thus provides important insight into evolutionary processes and the adaptive divergence of populations. The detection of local adaptation, however, suffers from several conceptual, statistical and methodological issues. Here, we provide practical recommendations regarding (1) the definition of local adaptation, (2) the analysis of transplant experiments and (3) the optimisation of the experimental design of local adaptation studies. Together, these recommendations provide a unified approach for measuring local adaptation and understanding the adaptive divergence of populations in a wide range of biological systems.

Adaptive divergence in seed color camouflage in contrasting soil environments

Although adaptive plant population divergence across contrasting soil conditions is often driven by abiotic soil factors, natural enemies may also contribute. Cryptic matching to the native soil color is a form of defensive camouflage that seeds can use to avoid detection by seed predators. The legume Acmispon wrangelianus occurs across a variety of gray-green serpentine soils and brown nonserpentine soils. Quantitative digital image analysis of seed and soil colors was used to test whether genetically based seed color is a closer match to the color of the native soil than to the color of other nearby soils. Lineages bear seeds that more closely match the color of their native serpentine or nonserpentine soil type than the opposing soil type. Further, even within a soil type, lineages bear seeds with a closer color match to the soil at their native site than to other sites. The striking concordance between seed and native soil color suggests that natural selection for locally camouflaged seed color morphs, probably driven by seed predators, may maintain adaptive divergence in pigmentation, despite the opportunity for migration between soil environments.

The role of genetic structure in the adaptive divergence of populations experiencing saltwater intrusion due to relative sea‐level rise

Saltwater intrusion into estuaries creates stressful conditions for nektonic species. Previous studies have shown that Gambusia affinis populations with exposure to saline environments develop genetic adaptations for increased survival during salinity stress. Here, we evaluate the genetic structure of G.affinis populations, previously shown to have adaptations for increased salinity tolerance, and determine the impact of selection and gene flow on structure of these populations. We found that gene flow was higher between populations experiencing different salinity regimes within an estuary than between similar marsh types in different estuaries, suggesting the development of saline-tolerant phenotypes due to local adaptation. There was limited evidence of genetic structure along a salinity gradient, and only some of the genetic variation among sites was correlated with salinity. Our results suggest limited structure, combined with selection to saltwater intrusion, results in phenotypic divergence in spite of a lack of physical barriers to gene flow.

An outlier locus relevant in habitat-mediated selection in an alpine plant across independent regional replicates

Habitat types can induce genetic responses in species and may drive adaptive differentiation and evolutionary divergence of populations. In this study, we aimed at detecting loci indicative of adaptation for different habitat types in the alpine plant Arabis alpina. We used a dataset consisting of A. alpina plants collected in scree, nutrient-rich and moist habitat types in two independent regional replicates of the European Alps (the Swiss and French Alps). Genome scans resulting in 825 amplified fragment length polymorphisms (AFLPs) followed by outlier analysis, i.e. looking for excessive differentiation between habitat types, after accounting for heterozygosity and population structure, was used to detect loci under divergent selection for habitat type within and across the alpine regions. The outlier analyses resulted in the detection of a consistent single outlier locus, which showed a higher fragment frequency in moist compared to the other habitat types in both alpine regions. In addition, a posteriori tests for hierarchical population structuring in the dataset did not detect signals confounding selection at this locus (i.e. signals of regional population structure). Thus, we consider this locus indicative of habitat-mediated selection, and we subsequently sequence-characterized and compared it to the Arabidopsis genome. The sequence was found to be a putative homologue to the SIT4 phosphatase-associated family protein. The detection of this locus in two alpine regions and the availability of its genome sequence make this locus a strong candidate worth further exploration in the habitat-mediated selection and genetic adaptation of natural populations in the alpine plant A. alpina.

Quantitative genetics of feeding behavior in two ecological races of the pea aphid, Acyrthosiphon pisum

Much of the diversity of herbivorous insects stems from the adaptive divergence of populations onto different host plants. This often involves the evolution of specialized patterns of host acceptance that in turn lead to assortative mating for insects that mate exclusively on their hosts. Here, we explore the genetic architecture of feeding behavior in a herbivorous insect that has become a model for the study of incipient speciation, the pea aphid (Acyrthosiphon pisum). We use crosses between individuals specialized to either alfalfa or red clover in order to perform both a biometrical analysis and a quantitative trait locus (QTL) analysis of key feeding behaviors. For each character in each environment, Castle-Wright's estimator for the number of effective factors segregating ranged from 0.11 to 2.54. Similarly, between 0 and 3 QTLs were detected. In one case, a single QTL explained over 50% of the variance in the F2, suggesting that at least one gene (or a complex of tightly linked genes) has a major effect on feeding behavior in the pea aphid. However, the identified QTL explain only 23-73% of the genetic variance for these characters thus additional genes of minor effect are also involved. We found a variety of modes of gene action, including several cases of non-additive gene action. Our results suggest that feeding behavior in pea aphids is neither simple nor highly polygenic. The oligogenetic basis of variation in feeding behavior may facilitate host shifts, providing one explanation for the frequent divergence and speciation of herbivorous insects.

Range limits, large-scale biogeographic variation, and localized evolutionary dynamics in a polymorphic damselfly

Studies of heritable colour polymorphisms allow investigators to track the genetic dynamics of natural populations. By comparing polymorphic populations over large geographic areas and across generations, issues about both morph stability and evolutionary dynamics can be addressed, increasing our understanding of the potential mechanisms maintaining genetic polymorphisms. In the present study, we investigated population morph frequencies in a sex-limited heritable colour polymorphic damselfly (Ischnura elegans, Vander Linden), with three discrete female morphs. We compared the frequencies of these three female morphs in 120 different populations from ten European countries at differing latitudes and longitudes. There were pronounced differences in morph frequencies both across the entire European biogeographic range, as well as at a smaller scale within regions. We also found considerable between-population variation at the local scale within regions, particularly at the edges of the range of this species. We discuss these findings in the context of recent models of adaptive population divergence along the range of a species. This polymorphism is thus highly dynamic, with stable morph frequencies at the core of the species range but fluctuating morph dynamics at the range limits. We finish with a discussion of how local interactions and climatic factors can be expected to have a strong influence on the biogeographic patterns in this species and other sexually selected polymorphisms.

Adaptive divergence for a fitness‐related trait among invasiveAmbrosia artemisiifoliapopulations in France

The impact of natural selection on the adaptive divergence of invasive populations can be assessed by testing the null hypothesis that the extent of quantitative genetic differentiation (Q(ST) ) would be similar to that of neutral molecular differentiation (F(ST) ). Using eight microsatellite loci and a common garden approach, we compared Q(ST) and F(ST) among ten populations of an invasive species Ambrosia artemisiifolia (common ragweed) in France. In a common garden study with varying water and nutrient levels, we measured Q(ST) for five traits (height, total biomass, reproductive allocation, above- to belowground biomass ratio, and days to flowering). Although low F(ST) indicated weak genetic structure and strong gene flow among populations, we found significant diversifying selection (Q(ST) > F(ST) ) for reproductive allocation that may be closely related to fitness. It suggests that abiotic conditions may have exerted selection pressure on A. artemisiifolia populations to differentiate adaptively, such that populations at higher altitude or latitude evolved greater reproductive allocation. As previous studies indicate multiple introductions from various source populations of A. artemisiifolia in North America, our results suggest that the admixture of introduced populations may have increased genetic diversity and additive genetic variance, and in turn, promoted the rapid evolution and adaptation of this invasive species.

Population transcriptomics of Drosophila melanogaster females

BackgroundVariation at the level of gene expression is abundant in natural populations and is thought to contribute to the adaptive divergence of populations and species. Gene expression also differs considerably between males and females. Here we report a microarray analysis of gene expression variation among females of 16 Drosophila melanogaster strains derived from natural populations, including eight strains from the putative ancestral range in sub-Saharan Africa and eight strains from Europe. Gene expression variation among males of the same strains was reported previously.ResultsWe detected relatively low levels of expression polymorphism within populations, but much higher expression divergence between populations. A total of 569 genes showed a significant expression difference between the African and European populations at a false discovery rate of 5%. Genes with significant over-expression in Europe included the insecticide resistance gene Cyp6g1, as well as genes involved in proteolysis and olfaction. Genes with functions in carbohydrate metabolism and vision were significantly over-expressed in the African population. There was little overlap between genes expressed differently between populations in females and males.ConclusionsOur results suggest that adaptive changes in gene expression have accompanied the out-of-Africa migration of D. melanogaster. Comparison of female and male expression data indicates that the vast majority of genes differing in expression between populations do so in only one sex and suggests that most regulatory adaptation has been sex-specific.

Adaptive divergence of the moor frog (Rana arvalis) along an acidification gradient

BackgroundEnvironmental stress can result in strong ecological and evolutionary effects on natural populations, but to what extent it drives adaptive divergence of natural populations is little explored. We used common garden experiments to study adaptive divergence in embryonic and larval fitness traits (embryonic survival, larval growth, and age and size at metamorphosis) in eight moor frog, Rana arvalis, populations inhabiting an acidification gradient (breeding pond pH 4.0 to 7.5) in southwestern Sweden. Embryos were raised until hatching at three (pH 4.0, 4.3 and 7.5) and larvae until metamorphosis at two (pH 4.3 and 7.5) pH treatments. To get insight into the putative selective agents along this environmental gradient, we measured relevant abiotic and biotic environmental variables from each breeding pond, and used linear models to test for phenotype-environment correlations.ResultsWe found that acid origin populations had higher embryonic and larval acid tolerance (survival and larval period were less negatively affected by low pH), higher larval growth but slower larval development rates, and metamorphosed at a larger size. The phenotype-environment correlations revealed that divergence in embryonic acid tolerance and metamorphic size correlated most strongly with breeding pond pH, whereas divergence in larval period and larval growth correlated most strongly with latitude and predator density, respectively.ConclusionOur results suggest that R. arvalis has diverged in response to pH mediated selection along this acidification gradient. However, as latitude and pH were closely spatially correlated in this study, further studies are needed to disentangle the specific agents of natural selection along acidification gradients. Our study highlights the need to consider the multiple interacting selective forces that drive adaptive divergence of natural populations along environmental stress gradients.

Variation in anonymous and EST-microsatellites suggests adaptive population divergence in turbot

We studied the variation at 30 anonymous and 30 expressed sequence tag (EST)-associ- ated microsatellites in 4 natural populations of turbot Scophthalmus maximus living in habitats with different salinity and temperature conditions. We identified putative divergent selection effects on 3 genes: the fibroblast growth factor receptor, the β microglobuline, and the trap alpha gene for translocon associate protein. The markers closely linked to these genes showed significant deviations from the neutral expectations using 2 different statistical methods in several pairwise population comparisons involving samples from salty and brackish environments. Our results confirmed the weak genetic structure among populations from the northeast Atlantic and the low but significant genetic differentiation of turbot from the Baltic Sea. These results suggest that populations from the Baltic-Atlantic transition area could be accumulating adaptive polymorphisms in the face of high gene flow.

Divergent resistance to a monogenean flatworm among three‐spined stickleback populations

Summary1. Given their ubiquity, we might expect parasites to play an important role in the adaptive divergence of host populations. Specifically, adaptation to local parasite communities is predicted to influence the evolution of a number of host traits such as parasite resistance.2. To investigate the possibility that divergent parasite‐mediated selection drives population‐level variation in parasite resistance, we artificially infected lab‐reared three‐spined sticklebacks with the monogenean flatwormGyrodactylus gasterostei. The fish were derived from five populations from North Uist, Scotland, that were chosen because they differed in natural infection levels ofGyrodactylus arcuatus.3. We found substantial differences in resistance toG. gasterosteiamong populations. Resistance was defined largely by the ability to limit the size of the worm population rather than by the timing of the host response.4. Experimental resistance was not significantly correlated with natural infection levels ofG. arcuatus. However, in general, populations with greater exposure toG. arcuatuswere shown to be more resistant toG. gasterostei. Fish from the only naturally unexposed population showed the highest susceptibility, which may be the result of less selection to maintain resistance.5. Taken together, these results suggest that the divergent selection mediated byGyrodactylusmay play a role in driving population‐level variation in resistance to this parasite.