Evolution of fitnesses and allele frequencies in a population with spatially heterogeneous selection pressures

The level of gene flow considerably influences the outcome of evolutionary processes in structured populations with spatial heterogeneity in selection pressures; low levels of gene flow may allow local adaptation whereas high levels of gene flow may oppose this process thus preventing the stable maintenance of polymorphism. Indeed, proportions of fitness space that successfully maintain polymorphism are substantially larger in spatially heterogenous populations with lower to moderate levels of gene flow when compared to single-deme models. Nevertheless, the effect of spatial heterogeneity on the evolutionary construction of polymorphism is less clear. We have investigated the levels of polymorphism resulting from a simple two-deme construction model, which incorporates recurrent mutation as well as selection. We further compared fitness properties, stability of equilibria, and frequency distribution patterns emerging from the construction approach and compared these to the static fitness-space approach. The construction model either promotes or constrains the level of polymorphisms, depending on the levels of gene flow. Comparison of the fitness properties resulting from both approaches shows that they maintain variation in different parts of fitness space. The part of fitness space resulting from construction is more stable than that implied by the ahistoric fitness-space approach. Finally, the equilibrium allele-frequency distribution patterns vary substantially with different levels of gene flow, underlining the importance of correctly sampling spatial structure if these patterns are to be used to estimate population-genetic processes.     

Environmental heterogeneity enhances clonal interference

Clonal interference (CI) is a phenomenon that may be important in several asexual microbes. It occurs when population sizes are large and mutation rates to new beneficial alleles are of significant magnitude. Here we explore the role of gene flow and spatial heterogeneity in selection strength in the adaptation of asexuals. We consider a subdivided population of individuals that are adapting, through new beneficial mutations, and that migrate between different patches. The fitness effect of each mutation depends on the patch and all mutations considered are assumed to be unconditionally beneficial. We find that spatial variation in selection pressure affects the rate of adaptive evolution and its qualitative effects depend on the level of gene flow. In particular, we find that both low migration and high levels of heterogeneity lead to enhanced CI. In contrast, for high levels of migration the rate of fixation of adaptive mutations is higher when environmental heterogeneity is present. In addition, we observe that the level of fitness variation is higher and simultaneous fixation of multiple mutations tends to occur in the regime of low migration rates and high heterogeneity.     

Genetic Analysis of Invasive Plant Populations at Different Spatial Scales

Measuring genetic diversity requires selection of a spatial scale of analysis. Different levels of genetic structuring are revealed at different spatial scales, however, and the relative importance of factors driving genetic structuring varies along the spatial scale continuum. Unequal gene flow is a major factor determining genetic structure in plant populations at the local level, while the effect of selection imposed by environmental heterogeneity increases with the spatial scale of analysis. At a continental and global scale genetic structure of invasive plant populations is significantly affected by founder effect and propagule transport via human vectors. Although genetic analysis at one spatial scale provides only partial information about the invasion process, little published research reports such data for the same species at multiple scales. A multi-faceted approach to investigating the genetic structure of invasive plant species that incorporates sampling at different spatial and temporal scales would provide a more complete picture of the role of genetic forces in invasion.     

STRONG SELECTION BARRIERS EXPLAIN MICROGEOGRAPHIC ADAPTATION IN WILD SALAMANDER POPULATIONS

Microgeographic adaptation occurs when populations evolve divergent fitness advantages across the spatial scales at which focal organisms regularly disperse. Although an increasing number of studies find evidence for microgeographic adaptation, the underlying causes often remain unknown. Adaptive divergence requires some combination of limited gene flow and strong divergent natural selection among populations. In this study, we estimated the relative influence of selection, gene flow, and the spatial arrangement of populations in shaping patterns of adaptive divergence in natural populations of the spotted salamander (Ambystoma maculatum). Within the study region, A. maculatum co‐occur with the predatory marbled salamander (Ambystoma opacum) in some ponds, and past studies have established a link between predation risk and adaptive trait variation in A. maculatum. Using 14 microsatellite loci, we found a significant pattern of genetic divergence among A. maculatum populations corresponding to levels of A. opacum predation risk. Additionally, A. maculatum foraging rate was strongly associated with predation risk, genetic divergence, and the spatial relationship of ponds on the landscape. Our results indicate the sorting of adaptive genotypes by selection regime and strongly suggest that substantial selective barriers operate against gene flow. This outcome suggests that microgeographic adaptation in A. maculatum is possible because strong antagonistic selection quickly eliminates maladapted phenotypes despite ongoing and substantial immigration. Increasing evidence for microgeographic adaptation suggests a strong role for selective barriers in counteracting the homogenizing influence of gene flow.     

Eco-evolutionary metapopulation dynamics and the spatial scale of adaptation

We construct a model that combines extinction-colonization dynamics with the dynamics of local adaptation in a network of habitat patches of dissimilar qualities. We derive a deterministic approximation for the stochastic model that allows the calculation of patch-specific incidences of occupancy and levels of adaptation at steady state. Depending on (i) the strength of local selection, (ii) the amount of genetic variance, (iii) the demographic cost of maladaptation, (iv) the spatial scale of gene flow, and (v) the amount of habitat heterogeneity, the model predicts adaptation at different spatial scales. Local adaptation is predicted when there is much genetic variance and strong selection, while network-level adaptation occurs when the demographic cost of maladaptation is low. For little genetic variance and high cost of maladaptation, the model predicts network-level habitat specialization in species with long-range migration but an intermediate scale of adaptation (mosaic specialization) in species with short-range migration. In fragmented landscapes, the evolutionary dynamics of adaptation may both decrease and enhance metapopulation viability in comparison with no evolution. The model can be applied to real patch networks with given sizes, qualities, and spatial positions of habitat patches.     

Continental-Scale Footprint of Balancing and Positive Selection in a Small Rodent (Microtus arvalis)

Genetic adaptation to different environmental conditions is expected to lead to large differences between populations at selected loci, thus providing a signature of positive selection. Whereas balancing selection can maintain polymorphisms over long evolutionary periods and even geographic scale, thus leads to low levels of divergence between populations at selected loci. However, little is known about the relative importance of these two selective forces in shaping genomic diversity, partly due to difficulties in recognizing balancing selection in species showing low levels of differentiation. Here we address this problem by studying genomic diversity in the European common vole (Microtus arvalis) presenting high levels of differentiation between populations (average F _ST = 0.31). We studied 3,839 Amplified Fragment Length Polymorphism (AFLP) markers genotyped in 444 individuals from 21 populations distributed across the European continent and hence over different environmental conditions. Our statistical approach to detect markers under selection is based on a Bayesian method specifically developed for AFLP markers, which treats AFLPs as a nearly codominant marker system, and therefore has increased power to detect selection. The high number of screened populations allowed us to detect the signature of balancing selection across a large geographic area. We detected 33 markers potentially under balancing selection, hence strong evidence of stabilizing selection in 21 populations across Europe. However, our analyses identified four-times more markers (138) being under positive selection, and geographical patterns suggest that some of these markers are probably associated with alpine regions, which seem to have environmental conditions that favour adaptation. We conclude that despite favourable conditions in this study for the detection of balancing selection, this evolutionary force seems to play a relatively minor role in shaping the genomic diversity of the common vole, which is more influenced by positive selection and neutral processes like drift and demographic history.     

Coevolutionary clines across selection mosaics

Abstract. Much of the dynamics of coevolution may be driven by the interplay between geographic variation in reciprocal selection (selection mosaics) and the homogenizing action of gene flow. We develop a genetic model of geographically structured coevolution in which gene flow links coevolving communities that may differ in both the direction and magnitude of reciprocal selection. The results show that geographically structured coevolution may lead to allele-frequency clines within both interacting species when fitnesses are spatially uniform or spatially heterogeneous. Furthermore, the results show that the behavior and shape of clines differ dramatically among different types of coevolutionary interaction. Antagonistic interactions produce dynamic clines that change shape rapidly through time, producing shifting patterns of local adaptation and maladaptation. Unlike antagonistic interactions, mutualisms generate stable equilibrium patterns that lead to fixed spatial patterns of adaptation. Interactions that vary between mutualism and antagonism produce both equilibrium and dynamic clines. Furthermore, the results demonstrate that these interactions may allow mutualisms to persist throughout the geographic range of an interaction, despite pockets of locally antagonistic selection. In all cases, the coevolved spatial patterns of allele frequencies are sensitive to the relative contributions of gene flow, selection, and overall habitat size, indicating that the appropriate scale for studies of geographically structured coevolution depends on the relative contributions of each of these factors.     

Comparing the consequences of natural selection,adaptive phenotypic plasticity,and matching habitat choice for phenotype–environment matching,population genetic structure,and reproductive isolation in meta‐populations

Organisms commonly experience significant spatiotemporal variation in their environments. In response to such heterogeneity, different mechanisms may act that enhance ecological performance locally. However, depending on the nature of the mechanism involved, the consequences for populations may differ greatly. Building on a previous model that investigated the conditions under which different adaptive mechanisms (co)evolve, this study compares the ecological and evolutionary population consequences of three very different responses to environmental heterogeneity: matching habitat choice (directed gene flow), adaptive plasticity (associated with random gene flow), and divergent natural selection. Using individual‐based simulations, we show that matching habitat choice can have a greater adaptive potential than plasticity or natural selection: it allows for local adaptation while protecting genetic polymorphism despite global mating or strong environmental changes. Our simulations further reveal that increasing environmental fluctuations and unpredictability generally favor the emergence of specialist genotypes but that matching habitat choice is better at preventing local maladaptation by individuals. This confirms that matching habitat choice can speed up the genetic divergence among populations, cause indirect assortative mating via spatial clustering, and hence even facilitate sympatric speciation. This study highlights the potential importance of directed dispersal in local adaptation and speciation, stresses the difficulty of deriving its operation from nonexperimental observational data alone, and helps define a set of ecological conditions which should favor its emergence and subsequent detection in nature.     

Environmental heterogeneity and balancing selection in the acorn barnacle Semibalanus balanoides

The northern acorn barnacle Semibalans banlanoides occupies several intertidal microhabitats which vary greatly in their degree of physical stress. This environmental heterogeneity creates distinct selection regimes which can maintain genetic variation in natural populations. Despite considerable attention placed on the link between spatial variation in fitness and balancing selection at specific loci, experimental manipulations and fitness estimates for molecular polymorphisms have rarely been conducted in the wild. The aim of this transplant experiment was to manipulate the level of physical stress experienced by a cohort of barnacles in the field and then investigate the spatial variation in fitness for genotypes at three loci: two candidate allozymes and the mitochondrial DNA control region. The viability of mannose-6-phosphate isomerase (Mpi) genotypes was dependent on the level of physical stress experienced in the various treatments; alternative homozygotes were favoured in alternative high stress-low stress environments. In contrast, the fitness of genotypes at other loci was equivalent among treatments and unaffected by the manipulation. Evaluated in the light of balancing selection models, these data indicate that the presence of multiple environmental niches is sufficient to promote a stable Mpi polymorphism in barnacle populations and that allelic variation at this locus reflects the process of adaptation to the heterogeneous intertidal landscape.     

Emergence of long‐term balanced polymorphism under cyclic selection of spatially variable magnitude

A fundamental question in evolutionary biology is what promotes genetic variation at nonneutral loci, a major precursor to adaptation in changing environments. In particular, balanced polymorphism under realistic evolutionary models of temporally varying environments in finite natural populations remains to be demonstrated. Here, we propose a novel mechanism of balancing selection under temporally varying fitnesses. Using forward‐in‐time computer simulations and mathematical analysis, we show that cyclic selection that spatially varies in magnitude, such as along an environmental gradient, can lead to elevated levels of nonneutral genetic polymorphism in finite populations. Balanced polymorphism is more likely with an increase in gene flow, magnitude and period of fitness oscillations, and spatial heterogeneity. This polymorphism‐promoting effect is robust to small systematic fitness differences between competing alleles or to random environmental perturbation. Furthermore, we demonstrate analytically that protected polymorphism arises as spatially heterogeneous cyclic fitness oscillations generate a type of storage effect that leads to negative frequency dependent selection. Our findings imply that spatially variable cyclic environments can promote elevated levels of nonneutral genetic variation in natural populations.     

LOCAL ADAPTATION MAINTAINS CLINAL VARIATION IN MELANIN‐BASED COLORATION OF EUROPEAN BARN OWLS (TYTO ALBA)

Ecological parameters vary in space, and the resulting heterogeneity of selective forces can drive adaptive population divergence. Clinal variation represents a classical model to study the interplay of gene flow and selection in the dynamics of this local adaptation process. Although geographic variation in phenotypic traits in discrete populations could be remainders of past adaptation, maintenance of adaptive clinal variation requires recurrent selection. Clinal variation in genetically determined traits is generally attributed to adaptation of different genotypes to local conditions along an environmental gradient, although it can as well arise from neutral processes. Here, we investigated whether selection accounts for the strong clinal variation observed in a highly heritable pheomelanin‐based color trait in the European barn owl by comparing spatial differentiation of color and of neutral genes among populations. Barn owl's coloration varies continuously from white in southwestern Europe to reddish‐brown in northeastern Europe. A very low differentiation at neutral genetic markers suggests that substantial gene flow occurs among populations. The persistence of pronounced color differentiation despite this strong gene flow is consistent with the hypothesis that selection is the primary force maintaining color variation among European populations. Therefore, the color cline is most likely the result of local adaptation.     

Lack of Spatial Immunogenetic Structure among Wolverine (Gulo gulo) Populations Suggestive of Broad Scale Balancing Selection

Elucidating the adaptive genetic potential of wildlife populations to environmental selective pressures is fundamental for species conservation. Genes of the major histocompatibility complex (MHC) are highly polymorphic, and play a key role in the adaptive immune response against pathogens. MHC polymorphism has been linked to balancing selection or heterogeneous selection promoting local adaptation. However, spatial patterns of MHC polymorphism are also influenced by gene flow and drift. Wolverines are highly vagile, inhabiting varied ecoregions that include boreal forest, taiga, tundra, and high alpine ecosystems. Here, we investigated the immunogenetic variation of wolverines in Canada as a surrogate for identifying local adaptation by contrasting the genetic structure at MHC relative to the structure at 11 neutral microsatellites to account for gene flow and drift. Evidence of historical positive selection was detected at MHC using maximum likelihood codon-based methods. Bayesian and multivariate cluster analyses revealed weaker population genetic differentiation at MHC relative to the increasing microsatellite genetic structure towards the eastern wolverine distribution. Mantel correlations of MHC against geographical distances showed no pattern of isolation by distance (IBD: r = -0.03, p = 0.9), whereas for microsatellites we found a relatively strong and significant IBD (r = 0.54, p = 0.01). Moreover, we found a significant correlation between microsatellite allelic richness and the mean number of MHC alleles, but we did not observe low MHC diversity in small populations. Overall these results suggest that MHC polymorphism has been influenced primarily by balancing selection and to a lesser extent by neutral processes such as genetic drift, with no clear evidence for local adaptation. This study contributes to our understanding of how vulnerable populations of wolverines may respond to selective pressures across their range.     

Single-locus polymorphism in a heterogeneous two-deme model

Environmental heterogeneity has long been considered a likely explanation for the high levels of genetic variation found in most natural populations: selection in a spatially heterogeneous environment can maintain more variation. While this theoretical result has been extensively studied in models with limited parameters (e.g., two alleles, fixed gene flow, and particular selection schemes), the effect of spatial heterogeneity is poorly understood for models with a wider range of parameters (e.g., multiple alleles, different levels of gene flow, and more general selection schemes). We have compared the volume of fitness space that maintains variation in a single-deme model to the volume in a two-deme model for multiple alleles, random selection schemes, and various levels of migration. Furthermore, equilibrium allele-frequency vectors were examined to see if particular patterns of variation are more prevalent than first expected. The two-deme model maintains variation for substantially larger volumes of fitness space with lower heterozygote fitness than the single-deme model. This result implies that selection schemes in the two-deme model can have a wider range of fitness patterns while still maintaining variation. The equilibrium allele-frequency patterns emerging from the two-deme model are more variable and strongly influenced by gene flow.     

The Effect of Breeding System on Polymorphism in Mitochondrial Genes of Silene

Gynodioecy is a breeding system characterized by the co-occurrence of hermaphrodite and female individuals, generally as the result of nuclear–cytoplasmic interactions. The question remains whether the genetic factors controlling gynodioecy are maintained in species over long evolutionary timescales by balancing selection or are continually arising and being replaced in epidemic sweeps. If balancing selection maintains these factors, then neutral cytoplasmic diversity should be greater in gynodioecious than hermaphroditic species. In contrast, epidemic sweeps of factors controlling gynodioecy should decrease cytoplasmic diversity in gynodioecious relative to hermaphroditic species. We took a comparative approach in which we sequenced two mitochondrial genes, cytochrome b (cob) and cytochrome oxidase (cox1), for multiple populations of several hermaphroditic, gynodioecious, and dioecious species in the genus Silene. Breeding system was predictive of polymorphism. Gynodioecious species harbor many old haplotypes while hermaphroditic and dioecious species have little to no nucleotide diversity. The genealogical structure of neither gene departed from neutral expectations. Taken together, our results suggest that balancing selection acts on cytoplasmic male-sterility factors in several gynodioecious species in the genus.     

GENE FLOW AND SELECTION ON PHENOTYPIC PLASTICITY IN AN ISLAND SYSTEM OF RANA TEMPORARIA

Gene flow is often considered to be one of the main factors that constrains local adaptation in a heterogeneous environment. However, gene flow may also lead to the evolution of phenotypic plasticity. We investigated the effect of gene flow on local adaptation and phenotypic plasticity in development time in island populations of the common frog Rana temporaria which breed in pools that differ in drying regimes. This was done by investigating associations between traits (measured in a common garden experiment) and selective factors (pool drying regimes and gene flow from other populations inhabiting different environments) by regression analyses and by comparing pairwise F_ST values (obtained from microsatellite analyses) with pairwise Q_ST values. We found that the degree of phenotypic plasticity was positively correlated with gene flow from other populations inhabiting different environments (among‐island environmental heterogeneity), as well as with local environmental heterogeneity within each population. Furthermore, local adaptation, manifested in the correlation between development time and the degree of pool drying on the islands, appears to have been caused by divergent selection pressures. The local adaptation in development time and phenotypic plasticity is quite remarkable, because the populations are young (less than 300 generations) and substantial gene flow is present among islands.     

Island isolation and habitat heterogeneity correlate with DNA variation in a marine snail (Littorina saxatilis)

The null assumption of molecular variation is that most of it is neutral to natural selection. This is in contrast to variation in morphological traits that we generally assume is maintained by selection, and therefore often by selection coupled to environmental heterogeneity in time and space. Examples of molecular variation that vary over habitat-shifts, particularly in allozymes, show that the relative impact of non-neutral variation as compared to neutral variation might be substantial in some systems. To assess the importance of habitat-generated variation in relation to variation generated by random processes in nuclear DNA markers at small spatial scales, we compared the effects of island isolation and habitat heterogeneity on genetic substructuring in a rocky shore snail ( Littorina saxatilis ). This species has a restricted migration among islands owing to the lack of free-floating larvae. Earlier studies show that allozymes vary extensively as a consequence of isolation by water barriers among islands, but also as a consequence of divergent selection among different microhabitats within islands. In the DNA markers we observed genetic differentiation owing to island isolation at three of nine loci. In addition, variation at three loci correlated with habitat type, but the correlation for two of the loci was weak. Overall, isolation contributed slightly more to the genetic variation among populations than did habitat-related factors but the difference was small. It is concluded that both island isolation, which interrupts gene flow, and a heterogeneous habitat cause genetic substructuring at the DNA level in L. saxatilis in the studied area, and thus in this species we need to be somewhat concerned about habitat heterogeneity also at DNA loci.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 377–384.     

Spatially explicit models of divergence and genome hitchhiking

Strong barriers to genetic exchange can exist at divergently selected loci, whereas alleles at neutral loci flow more readily between populations, thus impeding divergence and speciation in the face of gene flow. However, ‘divergence hitchhiking’ theory posits that divergent selection can generate large regions of differentiation around selected loci. ‘Genome hitchhiking’ theory suggests that selection can also cause reductions in average genome‐wide rates of gene flow, resulting in widespread genomic divergence (rather than divergence only around specific selected loci). Spatial heterogeneity is ubiquitous in nature, yet previous models of genetic barriers to gene flow have explored limited combinations of spatial and selective scenarios. Using simulations of secondary contact of populations, we explore barriers to gene flow in various selective and spatial contexts in continuous, two‐dimensional, spatially explicit environments. In general, the effects of hitchhiking are strongest in environments with regular spatial patterning of starkly divergent habitat types. When divergent selection is very strong, the absence of intermediate habitat types increases the effects of hitchhiking. However, when selection is moderate or weak, regular (vs. random) spatial arrangement of habitat types becomes more important than the presence of intermediate habitats per se. We also document counterintuitive processes arising from the stochastic interplay between selection, gene flow and drift. Our results indicate that generalization of results from two‐deme models requires caution and increase understanding of the genomic and geographic basis of population divergence.     

Genomics of local adaptation with gene flow

Gene flow is a fundamental evolutionary force in adaptation that is especially important to understand as humans are rapidly changing both the natural environment and natural levels of gene flow. Theory proposes a multifaceted role for gene flow in adaptation, but it focuses mainly on the disruptive effect that gene flow has on adaptation when selection is not strong enough to prevent the loss of locally adapted alleles. The role of gene flow in adaptation is now better understood due to the recent development of both genomic models of adaptive evolution and genomic techniques, which both point to the importance of genetic architecture in the origin and maintenance of adaptation with gene flow. In this review, we discuss three main topics on the genomics of adaptation with gene flow. First, we investigate selection on migration and gene flow. Second, we discuss the three potential sources of adaptive variation in relation to the role of gene flow in the origin of adaptation. Third, we explain how local adaptation is maintained despite gene flow: we provide a synthesis of recent genomic models of adaptation, discuss the genomic mechanisms and review empirical studies on the genomics of adaptation with gene flow. Despite predictions on the disruptive effect of gene flow in adaptation, an increasing number of studies show that gene flow can promote adaptation, that local adaptations can be maintained despite high gene flow, and that genetic architecture plays a fundamental role in the origin and maintenance of local adaptation with gene flow.     

ON THE EVOLUTION OF MIGRATION IN HETEROGENEOUS ENVIRONMENTS

Populations often experience variable conditions, both in time and space. Here we develop a novel theoretical framework to study the evolution of migration under the influence of spatially and temporally variable selection and genetic drift. First, we examine when polymorphism is maintained at a locus under heterogeneous selection, as a function of the pattern of spatial heterogeneity and the migration rate. In a second step, we study how levels of migration evolve under the joint action of kin competition and local adaptation at a polymorphic locus. This analysis reveals the existence of evolutionary bistability, whereby a low or a high migration rate may evolve depending on the initial conditions. Last, we relax several assumptions regarding selection heterogeneity commonly made in previous studies and explore the consequences of more complex spatial and temporal patterns of variability in selection on the evolution of migration. We found that small modifications in the pattern of environmental heterogeneity may have dramatic effects on the evolution of migration. This work highlights the importance of considering more general scenarios of environmental heterogeneity when studying the evolution of life‐history traits in ecologically complex settings.     

The evolution of species interactions across natural landscapes

Given the potential for rapid and microgeographical adaptation, ecologists increasingly are exploring evolutionary explanations for community patterns. Biotic selection can generate local adaptations that alter species interactions. Although some gene flow might be necessary to fuel local adaptation, higher gene flow can homogenise traits across regions and generate local maladaptation. Herein, I estimate the contributions of local biotic selection, gene flow and spatially autocorrelated biotic selection to among-population divergence in traits involved in species interactions across 75 studies. Local biotic selection explained 6.9% of inter-population trait divergence, an indirect estimate of restricted gene flow explained 0.1%, and spatially autocorrelated selection explained 9.3%. Together, biotic selection explained 16% of the variance in population trait means. Most biotic selection regimes were spatially autocorrelated. Hence, most populations receive gene flow from populations facing similar selection, which could allow for local adaptation despite moderate gene flow. Gene flow constrained adaptation in studies conducted at finer spatial scales as expected, but this effect was often confounded with spatially autocorrelated selection. Results indicate that traits involved in species interactions might often evolve across landscapes, especially when biotic selection is spatially autocorrelated. The frequent evolution of species interactions suggests that evolutionary processes might often influence community ecology.