Genetic diversity and sex‐bias dispersal of plateau pika in Tibetan plateau

Dispersal is an important aspect in organism's life history which could influence the rate and outcome of evolution of organism. Plateau pika is the keystone species in community of grasslands in Tibetan Plateau. In this study, we combine genetic and field data to character the population genetic pattern and dispersal dynamics in plateau pika (Ochotona curzoniae). Totally, 1,352 individual samples were collected, and 10 microsatellite loci were analyzed. Results revealed that plateau pika possessed high genetic diversity and inbreeding coefficient in a fine‐scale population. Dispersal distance is short and restricted in about 20 m. An effective sex‐biased dispersal strategy is employed by plateau pika: males disperse in breeding period for mating while females do it after reproduction for offspring and resource. Inbreeding avoiding was shown as the common driving force of dispersal, together with the other two factors, environment and resource. In addition, natal dispersal is female biased. More detailed genetic analyzes are needed to confirm the role of inbreeding avoidance and resource competition as ultimate cause of dispersal patterns in plateau pika.     

Artificial selection for increased dispersal results in lower fitness

Dispersal often covaries with other traits, and this covariation was shown to have a genetic basis. Here, we wanted to explore to what extent genetic constraints and correlational selection can explain patterns of covariation between dispersal and key life‐history traits—lifespan and reproduction. A prediction from the fitness‐associated dispersal hypothesis was that lower genetic quality is associated with higher dispersal propensity as driven by the benefits of genetic mixing. We wanted to contrast it with a prediction from a different model that individuals putting more emphasis on current rather than future reproduction disperse more, as they are expected to be more risk‐prone and exploratory. However, if dispersal has inherent costs, this will also result in a negative genetic correlation between higher rates of dispersal and some aspects of performance. To explore this issue, we used the dioecious nematode Caenorhabditis remanei and selected for increased and decreased dispersal propensity for 10 generations, followed by five generations of relaxed selection. Dispersal propensity responded to selection, and females from high‐dispersal lines dispersed more than females from low‐dispersal lines. Females selected for increased dispersal propensity produced fewer offspring and were more likely to die from matricide, which is associated with a low physiological condition in Caenorhabditis nematodes. There was no evidence for differences in age‐specific reproductive effort between high‐ and low‐dispersal females. Rather, reproductive output of high‐dispersal females was consistently reduced. We argue that our data provide support for the fitness‐associated dispersal hypothesis.     

The evolution of genetic architectures underlying quantitative traits

In the classic view introduced by R. A. Fisher, a quantitative trait is encoded by many loci with small, additive effects. Recent advances in quantitative trait loci mapping have begun to elucidate the genetic architectures underlying vast numbers of phenotypes across diverse taxa, producing observations that sometimes contrast with Fisher''s blueprint. Despite these considerable empirical efforts to map the genetic determinants of traits, it remains poorly understood how the genetic architecture of a trait should evolve, or how it depends on the selection pressures on the trait. Here, we develop a simple, population-genetic model for the evolution of genetic architectures. Our model predicts that traits under moderate selection should be encoded by many loci with highly variable effects, whereas traits under either weak or strong selection should be encoded by relatively few loci. We compare these theoretical predictions with qualitative trends in the genetics of human traits, and with systematic data on the genetics of gene expression levels in yeast. Our analysis provides an evolutionary explanation for broad empirical patterns in the genetic basis for traits, and it introduces a single framework that unifies the diversity of observed genetic architectures, ranging from Mendelian to Fisherian.     

THE CONTRIBUTION OF MATERNAL EFFECTS TO SELECTION RESPONSE: AN EMPIRICAL TEST OF COMPETING MODELS

Maternal effects can dramatically influence the evolutionary process, in some cases facilitating and in others hindering adaptive evolution. Maternal effects have been incorporated into quantitative genetic models using two theoretical frameworks: the variance‐components approach, which partitions variance into direct and maternal components, and the trait‐based approach, which assumes that maternal effects are mediated by specific maternal traits. Here, we demonstrate parallels between these models and test their ability to predict evolutionary change. First, we show that the two approaches predict equivalent responses to selection in the absence of maternal effects mediated by traits that are themselves maternally influenced. We also introduce a correction factor that may be applied when such cascading maternal effects are present. Second, we use several maternal effect models, as well as the standard breeder's equation, to predict evolution in response to artificial selection on flowering time in American bellflower, Campanulastrum americanum. Models that included maternal effects made much more accurate predictions of selection response than the breeder's equation. Maternal effect models differed somewhat in their fit, with a version of the trait‐based model providing the best fit. We recommend fitting such trait‐based models when possible and appropriate to make the most accurate evolutionary predictions.     

Can natural selection maintain long-distance dispersal? Insight from a stream salamander system

Dispersal distributions are often characterized by many individuals that stay close to their origin and large variation in the distances moved by those that leave. This variation in dispersal distance can strongly influence demographic, ecological, and evolutionary processes. However, a lack of data on the fitness and phenotype of individual dispersers has impeded research on the role of natural selection in maintaining variation in dispersal distance. Six years of spatially explicit capture-mark-recapture data showed that survival increased with dispersal distance in the stream salamander Gyrinophilus porphyriticus. To understand the evolutionary implications of this fitness response, we tested whether variation in dispersal distance has a phenotypic basis. We used photographs of marked individuals to measure head, trunk, and leg morphology. We then tested whether dispersal distances over the six-year study period were predicted by these traits. Dispersal distance was significantly related to leg morphology: individuals with relatively long forelimbs and short hindlimbs dispersed the farthest. These results support the hypothesis that positive fitness consequences maintain phenotypes enabling long-distance dispersal. More broadly, they suggest that natural selection can promote variation in dispersal distance and associated phenotypes, offering an alternative to the view that dispersal distance is driven by stochastic or landscape-specific mechanisms.     

Dispersal and alternative breeding site fidelity strategies in an amphibian

Dispersal (i.e. movement from a natal or breeding site to another breeding site) is a central process in ecology and evolution as it affects the eco‐evolutionary dynamics of spatially structured populations. Dispersal evolution is regulated by the balance between costs and benefits, which is influenced by the individual phenotype (i.e. phenotype‐dependent dispersal) and environmental factors (i.e. condition‐dependent dispersal). Even though these processes have been extensively studied in species with simple life cycles, our knowledge about these mechanisms in organisms displaying complex life cycles remains fragmentary. In fact, little is specifically known about how the interplay between individual and environmental factors may lead to alternative dispersal strategies that, in turn, lead to the coexistence of contrasted site fidelity phenotypes. In this paper, we examined breeding dispersal in a pond‐breeding amphibian, the great crested newt Triturus cristatus, within usual walking distances for a newt. We took advantage of recent developments in multi‐event capture–recapture models and used capture–recapture data (946 newts marked) collected in a spatially structured population occupying a large pond network (73 ponds). We showed a high rate of breeding site infidelity (i.e. pond use) and the coexistence of two dispersal phenotypes, namely, a highly pond faithful phenotype and a dispersing phenotype. Individuals that were site faithful at time t – 1 were therefore more likely to remain site faithful at time t. Our results also demonstrated that the probability that individuals belong to one or the other dispersal phenotypes depended on environmental and individual factors. In particular, we highlighted the existence of a dispersal syndrome implying a covariation pattern among dispersal behavior, body size, and survival. Our work opens new research prospects in the evolution of dispersal in organisms displaying complex life cycles and raises interesting questions about the evolutionary pathways that contribute to the diversification of movement strategies in the wild.     

Environment-dependent inbreeding depression: its ecological and evolutionary significance

Inbreeding depression is a major evolutionary and ecological force that influences population dynamics and the evolution of inbreeding-avoidance traits such as mating systems and dispersal. There is now compelling evidence that inbreeding depression is environment-dependent. Here, we discuss ecological and evolutionary consequences of environment-dependent inbreeding depression. The environmental dependence of inbreeding depression may be caused by environment-dependent phenotypic expression, environment-dependent dominance, and environment-dependent natural selection. The existence of environment-dependent inbreeding depression challenges classical models of inbreeding as caused by unconditionally deleterious alleles, and suggests that balancing selection may shape inbreeding depression in natural populations; loci associated with inbreeding depression in some environments may even contribute to adaptation to others. Environment-dependent inbreeding depression also has important, often neglected, ecological and evolutionary consequences: it can influence the demography of marginal or colonizing populations and alter adaptive optima of mating systems, dispersal, and their associated traits. Incorporating the environmental dependence of inbreeding depression into theoretical models and empirical studies is necessary for understanding the genetic and ecological basis of inbreeding depression and its consequences in natural populations.     

Gene networks and metacommunities: dispersal differences can override adaptive advantage

Dispersal is an important mechanism contributing to both ecological and evolutionary dynamics. In metapopulation and metacommunity ecology, dispersal enables new patches to be colonized; in evolution, dispersal counter-acts local selection, leading to regional homogenization. Here, I consider a three-patch metacommunity in which two species, each with a limiting quantitative trait underlain by gene networks of 16 to 256 genes, compete with one another and disperse among patches. Incorporating dispersal among heterogeneous patches introduces a tradeoff not observed in single-patch simulations: if the difference between gene network size of the two species is greater than the difference in dispersal ability (e.g., if the ratio of network sizes is larger than the ratio of dispersal abilities), then genetic architecture drives community outcome. However, if the difference in dispersal abilities is greater than gene network differences, then any adaptive advantages afforded by genetic architecture are over-ridden by dispersal. Thus, in addition to the selective pressures imposed by competition that shape the genetic architecture of quantitative traits, dispersal among patches creates an escape that may further alter the effects of different genetic architectures. These results provide a theoretical expectation for what we may observe as the field of ecological genomics develops.     

Relaxation of herbivore‐mediated selection drives the evolution of genetic covariances between plant competitive and defense traits

Insect herbivores are important mediators of selection on traits that impact plant defense against herbivory and competitive ability. Although recent experiments demonstrate a central role for herbivory in driving rapid evolution of defense and competition‐mediating traits, whether and how herbivory shapes heritable variation in these traits remains poorly understood. Here, we evaluate the structure and evolutionary stability of the G matrix for plant metabolites that are involved in defense and allelopathy in the tall goldenrod, Solidago altissima. We show that G has evolutionarily diverged between experimentally replicated populations that evolved in the presence versus the absence of ambient herbivory, providing direct evidence for the evolution of G by natural selection. Specifically, evolution in an herbivore‐free habitat altered the orientation of G , revealing a negative genetic covariation between defense‐ and competition‐related metabolites that is typically masked in herbivore‐exposed populations. Our results may be explained by predictions of classical quantitative genetic theory, as well as the theory of acquisition‐allocation trade‐offs. The study provides compelling evidence that herbivory drives the evolution of plant genetic architecture.     

The evolution of phenotypic integration: How directional selection reshapes covariation in mice

Variation is the basis for evolution, and understanding how variation can evolve is a central question in biology. In complex phenotypes, covariation plays an even more important role, as genetic associations between traits can bias and alter evolutionary change. Covariation can be shaped by complex interactions between loci, and this genetic architecture can also change during evolution. In this article, we analyzed mouse lines experimentally selected for changes in size to address the question of how multivariate covariation changes under directional selection, as well as to identify the consequences of these changes to evolution. Selected lines showed a clear restructuring of covariation in their cranium and, instead of depleting their size variation, these lines increased their magnitude of integration and the proportion of variation associated with the direction of selection. This result is compatible with recent theoretical works on the evolution of covariation that take the complexities of genetic architecture into account. This result also contradicts the traditional view of the effects of selection on available covariation and suggests a much more complex view of how populations respond to selection.     

Evolution and genetic architecture of disassortative mating at a locus under heterozygote advantage

The evolution of mate choice is a major topic in evolutionary biology because it is thought to be a key factor in trait and species diversification. Here, we aim at uncovering the ecological conditions and genetic architecture enabling the puzzling evolution of disassortative mating based on adaptive traits. This rare form of mate choice is observed for some polymorphic traits but theoretical predictions on the emergence and persistence of this behavior are largely lacking. Thus, we developed a mathematical model to specifically understand the evolution of disassortative mating based on mimetic color pattern in the polymorphic butterfly Heliconius numata. We confirm that heterozygote advantage favors the evolution of disassortative mating and show that disassortative mating is more likely to emerge if at least one allele at the trait locus is free from any recessive deleterious mutations. We modeled different possible genetic architectures underlying mate choice behavior, such as self‐referencing alleles, or specific preference or rejection alleles. Our results showed that self‐referencing or rejection alleles linked to the color pattern locus enable the emergence of disassortative mating. However, rejection alleles allow the emergence of disassortative mating only when the color pattern and preference loci are tightly linked.     

Cooperation‐mediated plasticity in dispersal and colonization

Kin selection theory predicts that costly cooperative behaviors evolve most readily when directed toward kin. Dispersal plays a controversial role in the evolution of cooperation: dispersal decreases local population relatedness and thus opposes the evolution of cooperation, but limited dispersal increases kin competition and can negate the benefits of cooperation. Theoretical work has suggested that plasticity of dispersal, where individuals can adjust their dispersal decisions according to the social context, might help resolve this paradox and promote the evolution of cooperation. Here, we experimentally tested the hypothesis that conditional dispersal decisions are mediated by a cooperative strategy: we quantified the density‐dependent dispersal decisions and subsequent colonization efficiency from single cells or groups of cells among six genetic strains of the unicellular Tetrahymena thermophila that differ in their aggregation level (high, medium, and low), a behavior associated with cooperation strategy. We found that the plastic reaction norms of dispersal rate relative to density differed according to aggregation level: highly aggregative genotypes showed negative density‐dependent dispersal, whereas low‐aggregation genotypes showed maximum dispersal rates at intermediate density, and medium‐aggregation genotypes showed density‐independent dispersal with intermediate dispersal rate. Dispersers from highly aggregative genotypes had specialized long‐distance dispersal phenotypes, contrary to low‐aggregation genotypes; medium‐aggregation genotypes showing intermediate dispersal phenotype. Moreover, highly aggregation genotypes showed evidence for beneficial kin‐cooperation during dispersal. Our experimental results should help to resolve the evolutionary conflict between cooperation and dispersal: cooperative individuals are expected to avoid kin‐competition by dispersing long distances, but maintain the benefits of cooperation by dispersing in small groups.     

MUTATIONAL CONTRIBUTIONS TO GENETIC VARIANCE-COVARIANCE MATRICES: AN EXPERIMENTAL APPROACH USING INDUCED MUTATIONS IN ARABIDOPSIS THALIANA

Genetic potential for evolutionary change and covariational constraints are typically summarized as the genetic variance-covariance matrix G , and there is currently debate over the extent to which G remains effectively constant during the course of adaptive evolution. However, G provides only a temporally restricted view of constraints that ignores possible biases in how new mutations affect multivariate phenotypes. We used chemical mutagenesis to study the effect of mutations as summarized by the mutational covariance matrix, M , in Arabidopsis thaliana. By introducing mutations into three isogenic strains of A. thaliana, we were able to quantify M directly as the genetic variance-covariance matrix of mutagenized lines. Induced mutations generally did not alter the means of the six morphology and life-history traits we measured, but they did affect the levels of available genetic variation and the covariances among traits. However, these effects were not consistent among the three isogenic lines; that is, there were significant differences among the lines in both the number of mutations produced by ethyl-methane-sulfonate treatment and the M matrices they induced. The evolutionary implications of the dependence of M on the number of mutations, the particular genetic background, and the mutagenic sampling of loci in the genome are discussed in light of commonly applied models of multivariate evolution and the potential for the genetic architecture itself to change in ways that facilitate the coordinated evolution of complex phenotypes.     

SPATIALLY CORRELATED EXTINCTIONS SELECT FOR LESS EMIGRATION BUT LARGER DISPERSAL DISTANCES IN THE SPIDER MITE TETRANYCHUS URTICAE

Dispersal is a central process to almost all species on earth, as it connects spatially structured populations and thereby increases population persistence. Dispersal is subject to (rapid) evolution and local patch extinctions are an important selective force in this context. In contrast to the randomly distributed local extinctions considered in most theoretical studies, habitat fragmentation or other anthropogenic interventions will lead to spatially correlated extinction patterns. Under such conditions natural selection is thought to lead to more long‐distance dispersal, but this theoretical prediction has not yet been verified empirically. We test this prediction in experimental spatially structured populations of the spider mite Tetranychus urticae and supplement these empirical results with insights from an individual‐based evolutionary model. We demonstrate that the spatial correlation of local extinctions changes the entire distribution of dispersal distances (dispersal kernel) and selects for overall less emigration but more long‐distance dispersal.     

Environmentally induced dispersal‐related life‐history syndrome in the tropical butterfly,Bicyclus anynana

Dispersal is a key process for understanding the persistence of populations as well as the capacity of organisms to respond to environmental change. Therefore, understanding factors that may facilitate or constrain the evolution of dispersal is of crucial interest. Assessments of phenotypic variation in various behavioural, physiological and morphological traits related to insect dispersal and flight performance are common, yet very little is known about the genetic associations among these traits. We have used experiments on the butterfly Bicyclus anynana to estimate genetic variation and covariation in seven behavioural, physiological and morphological traits related to flight potential and hence dispersal. Our goal was to characterize the heritabilities and genetic correlations among these traits and thus to understand more about the evolution of dispersal‐related life‐history syndromes in butterflies. Using a version of the animal model, we showed that all of the traits varied between the sexes, and most were either positively or negatively (phenotypically and/or genetically) correlated with body size. Heritable variation was present in most traits, with the highest heritabilities estimated for body mass and thorax ratio. The variance in flight activity among multiple measurements for the same individual was high even after controlling for the prevailing environmental conditions, indicating the importance of behavioural switching and/or inherent randomness associated with this type of movement. A number of dispersal‐related traits showed phenotypic correlations among one another, but only a few of these were associated with significant genetic correlations indicating that covariances between these traits in Bicyclus anynana are mainly environmentally induced.     

Effects of floral traits and plant genetic composition on pollinator behavior

Pollinator-mediated selection plays a major role in floral evolution and speciation. Floral traits that influence animal pollinator behavior are the target of pollinator-mediated selection, but can only evolve if floral phenotypes have underlying genetic variation. Thus, understanding the genetic basis of a floral trait is a crucial step in studying pollinator-mediated selection. In this study I tested the effect of quantitative trait loci (QTL) underlying floral traits on pollinator behavior in recombinant inbred lines (RILs) in the common sunflower, Helianthus annuus L. and its crop relative. The indirect effects of QTL on pollinator behavior, mediated by floral phenotypes, were analyzed for six insect visitor types using structural equation modeling (SEM) and path analysis. For three of the six visitor types (large and small bees and non-bee insects) valid models were revealed when all three levels (QTL, floral traits, and pollinator behavior) were incorporated. Nested model without genetics were validated for five of the six visitor types. The results suggest that insect behavior as a reaction to floral phenotypes is affected by the genetic architecture of floral traits. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users. Handling editor: Heikki Hokkanen     

Developing approaches for linear mixed modeling in landscape genetics through landscape‐directed dispersal simulations

Dispersal can impact population dynamics and geographic variation, and thus, genetic approaches that can establish which landscape factors influence population connectivity have ecological and evolutionary importance. Mixed models that account for the error structure of pairwise datasets are increasingly used to compare models relating genetic differentiation to pairwise measures of landscape resistance. A model selection framework based on information criteria metrics or explained variance may help disentangle the ecological and landscape factors influencing genetic structure, yet there are currently no consensus for the best protocols. Here, we develop landscape‐directed simulations and test a series of replicates that emulate independent empirical datasets of two species with different life history characteristics (greater sage‐grouse; eastern foxsnake). We determined that in our simulated scenarios, AIC and BIC were the best model selection indices and that marginal R² values were biased toward more complex models. The model coefficients for landscape variables generally reflected the underlying dispersal model with confidence intervals that did not overlap with zero across the entire model set. When we controlled for geographic distance, variables not in the underlying dispersal models (i.e., nontrue) typically overlapped zero. Our study helps establish methods for using linear mixed models to identify the features underlying patterns of dispersal across a variety of landscapes.     

A comparative analysis of dispersal syndromes in terrestrial and semi‐terrestrial animals

Dispersal, the behaviour ensuring gene flow, tends to covary with a number of morphological, ecological and behavioural traits. While species‐specific dispersal behaviours are the product of each species’ unique evolutionary history, there may be distinct interspecific patterns of covariation between dispersal and other traits (‘dispersal syndromes’) due to their shared evolutionary history or shared environments. Using dispersal, phylogeny and trait data for 15 terrestrial and semi‐terrestrial animal Orders (> 700 species), we tested for the existence and consistency of dispersal syndromes across species. At this taxonomic scale, dispersal increased linearly with body size in omnivores, but decreased above a critical length in herbivores and carnivores. Species life history and ecology significantly influenced patterns of covariation, with higher phylogenetic signal of dispersal in aerial dispersers compared with ground dwellers and stronger evidence for dispersal syndromes in aerial dispersers and ectotherms, compared with ground dwellers and endotherms. Our results highlight the complex role of dispersal in the evolution of species life‐history strategies: good dispersal ability was consistently associated with high fecundity and survival, and in aerial dispersers it was associated with early maturation. We discuss the consequences of these findings for species evolution and range shifts in response to future climate change.     

How is dispersal integrated in life histories: a quantitative analysis using butterflies

As dispersal plays a key role in gene flow among populations, its evolutionary dynamics under environmental changes is particularly important. The inter-dependency of dispersal with other life history traits may constrain dispersal evolution, and lead to the indirect selection of other traits as a by-product of this inter-dependency. Identifying the dispersal's relationships to other life-history traits will help to better understand the evolutionary dynamics of dispersal, and the consequences for species persistence and ecosystem functioning under global changes. Dispersal may be linked to other life-history traits as their respective evolutionary dynamics may be inter-dependent, or, because they are mechanistically related to each other. We identify traits that are predicted to co-vary with dispersal, and investigated the correlations that may constrain dispersal using published information on butterflies. Our quantitative analysis revealed that (1) dispersal directly correlated with demographic traits, mostly fecundity, whereas phylogenetic relationships among species had a negligible influence on this pattern, (2) gene flow and individual movements are correlated with ecological specialisation and body size, respectively and (3) routine movements only affected short-distance dispersal. Together, these results provide important insights into evolutionary dynamics under global environmental changes, and are directly applicable to biodiversity conservation.