Controlling the false-positive rate in multilocus genome scans for selection

Rapid typing of genetic variation at many regions of the genome is an efficient way to survey variability in natural populations in an effort to identify segments of the genome that have experienced recent natural selection. Following such a genome scan, individual regions may be chosen for further sequencing and a more detailed analysis of patterns of variability, often to perform a parametric test for selection and to estimate the strength of a recent selective sweep. We show here that not accounting for the ascertainment of loci in such analyses leads to false inference of natural selection when the true model is selective neutrality, because the procedure of choosing unusual loci (in comparison to the rest of the genome-scan data) selects regions of the genome with genealogies similar to those expected under models of recent directional selection. We describe a simple and efficient correction for this ascertainment bias, which restores the false-positive rate to near-nominal levels. For the parameters considered here, we find that obtaining a test with the expected distribution of P-values depends on accurately accounting both for ascertainment of regions and for demography. Finally, we use simulations to explore the utility of relying on outlier loci to detect recent selective sweeps. We find that measures of diversity and of population differentiation are more effective than summaries of the site-frequency spectrum and that sequencing larger regions (2.5 kbp) in genome-scan studies leads to more power to detect recent selective sweeps.     

Estimates of the average strength of natural selection are not inflated by sampling error or publication bias

Kingsolver et al.'s review of phenotypic selection gradients from natural populations provided a glimpse of the form and strength of selection in nature and how selection on different organisms and traits varies. Because this review's underlying database could be a key tool for answering fundamental questions concerning natural selection, it has spawned discussion of potential biases inherent in the review process. Here, we explicitly test for two commonly discussed sources of bias: sampling error and publication bias. We model the relationship between variance among selection gradients and sample size that sampling error produces by subsampling large empirical data sets containing measurements of traits and fitness. We find that this relationship was not mimicked by the review data set and therefore conclude that sampling error does not bias estimations of the average strength of selection. Using graphical tests, we find evidence for bias against publishing weak estimates of selection only among very small studies (N<38). However, this evidence is counteracted by excess weak estimates in larger studies. Thus, estimates of average strength of selection from the review are less biased than is often assumed. Devising and conducting straightforward tests for different biases allows concern to be focused on the most troublesome factors.     

Reducing environmental bias when measuring natural selection

Abstract.— Crucial to understanding the process of natural selection is characterizing phenotypic selection. Measures of phenotypic selection can be biased by environmental variation among individuals that causes a spurious correlation between a trait and fitness. One solution is analyzing genotypic data, rather than phenotypic data. Genotypic data, however, are difficult to gather, can be gathered from few species, and typically have low statistical power. Environmental correlations may act through traits other than through fitness itself. A path analytic framework, which includes measures of such traits, may reduce environmental bias in estimates of selection coefficients. We tested the efficacy of path analysis to reduce bias by re-analyzing three experiments where both phenotypic and genotypic data were available. All three consisted of plant species (Impatiens capensis, Arabidopsis thaliana , and Raphanus sativus) grown in experimental plots or the greenhouse. We found that selection coefficients estimated by path analysis using phenotypic data were highly correlated with those based on genotypic data with little systematic bias in estimating the strength of selection. Although not a panacea, using path analysis can substantially reduce environmental biases in estimates of selection coefficients. Such confidence in phenotypic selection estimates is critical for progress in the study of natural selection.     

黑眶蟾蜍的两性异形与选型配对模式

本研究以黑眶蟾蜍(Duttaphrynus melanostictus)为研究对象,通过对比黑眶蟾蜍抱对个体的体长、头长、头宽、眼间距、鼓膜径、耳后腺长、眼径、前臂及手长、前肢长以及后肢长等形态特征,分析雌性黑眶蟾蜍繁殖输出与其体型的关系,探究黑眶蟾蜍两性异形模式及其与雌性生育力的关系;同时通过对配对个体形态学特征的相关性分析探究了黑眶蟾蜍的配对模式。结果表明,黑眶蟾蜍雌性体长和体重显著大于雄体;两性的所有局部形态特征均与体长成正相关;去除体长因素影响后,雄性头长以及后肢长均明显大于雌性,其余局部形态特征两性间则皆无显著差异。雌体的窝卵重、窝卵数均与其体长和体重成正相关关系。雌性成体的前肢长与抱对雄性成体的前肢长之间呈显著正相关,其余形态特征两性间均无相关性。研究表明,生育力选择是导致黑眶蟾蜍两性异形的重要驱动力;黑眶蟾蜍的选型配对模式未表现在个体大小上,而是体现在局部特征(前肢长),这不仅为揭示两栖类配对模式的普遍性提供了参考,还表明对两栖类选型配对的研究应以多个性状为对象。     

The strength of phenotypic selection in natural populations

How strong is phenotypic selection on quantitative traits in the wild? We reviewed the literature from 1984 through 1997 for studies that estimated the strength of linear and quadratic selection in terms of standardized selection gradients or differentials on natural variation in quantitative traits for field populations. We tabulated 63 published studies of 62 species that reported over 2,500 estimates of linear or quadratic selection. More than 80% of the estimates were for morphological traits; there is very little data for behavioral or physiological traits. Most published selection studies were unreplicated and had sample sizes below 135 individuals, resulting in low statistical power to detect selection of the magnitude typically reported for natural populations. The absolute values of linear selection gradients |beta| were exponentially distributed with an overall median of 0.16, suggesting that strong directional selection was uncommon. The values of |beta| for selection on morphological and on life-history/phenological traits were significantly different: on average, selection on morphology was stronger than selection on phenology/life history. Similarly, the values of |beta| for selection via aspects of survival, fecundity, and mating success were significantly different: on average, selection on mating success was stronger than on survival. Comparisons of estimated linear selection gradients and differentials suggest that indirect components of phenotypic selection were usually modest relative to direct components. The absolute values of quadratic selection gradients |gamma| were exponentially distributed with an overall median of only 0.10, suggesting that quadratic selection is typically quite weak. The distribution of gamma values was symmetric about 0, providing no evidence that stabilizing selection is stronger or more common than disruptive selection in nature.     

SPATIAL VARIATION IN SELECTIVE REGIMES: SEXUAL SELECTION IN THE WATER STRIDER,GERRIS ODONTOGASTER

Studies of phenotypic selection in natural populations are often concerned with simply detecting selection. In adopting a more mechanistic approach, this study compares the sexual selection regimes in natural populations of the water strider Gerris odontogaster with a priori predictions of selection, based on a number of previous field and laboratory studies of the behavioral mechanisms of selection. In this species, a general reluctance of females to mate allows for intersexual selection for ability to subdue reluctant females in males. Female reluctance to mate has been shown to decrease with increasing population density, suggesting that sexual selection should be weaker in high density populations. Three different populations with large differences in population density were studied. A number of traits including parasite load, body mass, body size and male abdominal process length were found to experience significant sexual selection. The investigated populations differed considerably with regard to the total strength of selection on the measured traits and the form of selection on single traits. In general, males in the population with the highest density experienced the weakest selection for grasping ability. This pattern is ascribed to density-related alterations of female mating behavior. Selection for male grasping ability, as reflected by selection on male abdominal process length, is reduced in high-density populations where reluctant females are more easily subdued. Further, the studied populations differed significantly in mean phenotype and phenotypic variance for male abdominal process length. It is suggested that interpopulational differences in selective regimes may generate local adaptations with respect to male abdominal process length, and that gene flow may contribute to the maintenance of the high genetic variation in this trait. It is further suggested that more empirical effort should be made in quantifying and understanding spatial and temporal variation in selection in natural populations, since this may provide information on the prevalence of local adaptations in metric traits and on the mechanisms of selection.     

The evolution of preference strength under sensory bias: a role for indirect selection?

Evidence suggests that female preferences may sometimes arise through sensory bias, and that males may subsequently evolve traits that increase their conspicuousness to females. Here, we ask whether indirect selection, arising through genetic associations (linkage disequilibrium) during the sexual selection that sensory bias imposes, can itself influence the evolution of preference strength. Specifically, we use population genetic models to consider whether or not modifiers of preference strength can spread under different ecological conditions when female mate choice is driven by sensory bias. We focus on male traits that make a male more conspicuous in certain habitats-and thus both more visible to predators and more attractive to females-and examine modifiers of the strength of preference for conspicuous males. We first solve for the rate of spread of a modifier that strengthens preference within an environmentally uniform population; we illustrate that this spread will be extremely slow. Second, we used a series of simulations to consider the role of habitat structure and movement on the evolution of a modifier of preference strength, using male color polymorphisms as a case study. We find that in most cases, indirect selection does not allow the evolution of stronger or weaker preferences for sensory bias. Only in a "two-island" model, where there is restricted migration between different patches that favor different male phenotypes, did we find that preference strength could evolve. The role of indirect selection in the evolution of sensory bias is of particular interest because of ongoing speculation regarding the role of sensory bias in the evolution of reproductive isolation.     

It's about time: the temporal dynamics of phenotypic selection in the wild

Selection is a central process in nature. Although our understanding of the strength and form of selection has increased, a general understanding of the temporal dynamics of selection in nature is lacking. Here, we assembled a database of temporal replicates of selection from studies of wild populations to synthesize what we do (and do not) know about the temporal dynamics of selection. Our database contains 5519 estimates of selection from 89 studies, including estimates of both direct and indirect selection as well as linear and nonlinear selection. Morphological traits and studies focused on vertebrates were well-represented, with other traits and taxonomic groups less well-represented. Overall, three major features characterize the temporal dynamics of selection. First, the strength of selection often varies considerably from year to year, although random sampling error of selection coefficients may impose bias in estimates of the magnitude of such variation. Second, changes in the direction of selection are frequent. Third, changes in the form of selection are likely common, but harder to quantify. Although few studies have identified causal mechanisms underlying temporal variation in the strength, direction and form of selection, variation in environmental conditions driven by climatic fluctuations appear to be common and important.     

Differential fitness effects of immunocompetence and neighbourhood density in alternative female lizard morphs

1. A growing number of studies demonstrate that natural selection acts on traits important in whole animal performance and physiology. 2. Here we describe a heritable polymorphism in female dorsal pattern in the lizard Anolis sagrei (Dumeril & Bibron 1837). 3. Morphs did not differ in body size or habitat use (perch diameter), however, we show that the social environment, estimated by the number of female neighbours, had different selective effects on alternative morphs in nature. 4. We show that morphs displayed a significantly different immune response to phytohaemagglutinin. Furthermore, natural selection differentially acted on combinations of female morph and immunocompetence, favouring high levels of immune function in one morph and low levels of immune function in the other. 5. We discuss the possibility that morph-specific investments in life-history traits may lead to correlational selection between traits, even when those traits are likely to be determined by different genetic loci.     

Individual-level selection as a cause of Cope's rule of phyletic size increase

Cope's rule, the tendency for species within a lineage to evolve towards larger body size, has been widely reported in the fossil record, but the mechanisms leading to such phyletic size increase remain unclear. Here we show that selection acting on individual organisms generally favors larger body size. We performed an analysis of the strength of directional selection on size compared with other quantitative traits by evaluating 854 selection estimates from 42 studies of contemporaneous natural populations. For size, more than 79% of selection estimates exceed zero, whereas for other morphological traits positive and negative values are similar in frequency. The selective advantage of increased size occurs for traits implicated in both natural selection (e.g., differences in survival) and sexual selection (e.g., differences in mating success). The predominance of positive directional selection on size within populations could translate into a macroevolutionary trend toward increased size and thereby explain Cope's rule.     

COMPARING STRENGTHS OF DIRECTIONAL SELECTION: HOW STRONG IS STRONG?

The fundamental equation in evolutionary quantitative genetics, the Lande equation, describes the response to directional selection as a product of the additive genetic variance and the selection gradient of trait value on relative fitness. Comparisons of both genetic variances and selection gradients across traits or populations require standardization, as both are scale dependent. The Lande equation can be standardized in two ways. Standardizing by the variance of the selected trait yields the response in units of standard deviation as the product of the heritability and the variance-standardized selection gradient. This standardization conflates selection and variation because the phenotypic variance is a function of the genetic variance. Alternatively, one can standardize the Lande equation using the trait mean, yielding the proportional response to selection as the product of the squared coefficient of additive genetic variance and the mean-standardized selection gradient. Mean-standardized selection gradients are particularly useful for summarizing the strength of selection because the mean-standardized gradient for fitness itself is one, a convenient benchmark for strong selection. We review published estimates of directional selection in natural populations using mean-standardized selection gradients. Only 38 published studies provided all the necessary information for calculation of mean-standardized gradients. The median absolute value of multivariate mean-standardized gradients shows that selection is on average 54% as strong as selection on fitness. Correcting for the upward bias introduced by taking absolute values lowers the median to 31%, still very strong selection. Such large estimates clearly cannot be representative of selection on all traits. Some possible sources of overestimation of the strength of selection include confounding environmental and genotypic effects on fitness, the use of fitness components as proxies for fitness, and biases in publication or choice of traits to study.     

A composite-likelihood approach for detecting directional selection from DNA sequence data

We present a novel composite-likelihood-ratio test (CLRT) for detecting genes and genomic regions that are subject to recurrent natural selection (either positive or negative). The method uses the likelihood functions of Hartl et al. (1994) for inference in a Wright-Fisher genic selection model and corrects for nonindependence among sites by application of coalescent simulations with recombination. Here, we (1) characterize the distribution of the CLRT statistic (Lambda) as a function of the population recombination rate (R=4Ner); (2) explore the effects of bias in estimation of R on the size (type I error) of the CLRT; (3) explore the robustness of the model to population growth, bottlenecks, and migration; (4) explore the power of the CLRT under varying levels of mutation, selection, and recombination; (5) explore the discriminatory power of the test in distinguishing negative selection from population growth; and (6) evaluate the performance of maximum composite-likelihood estimation (MCLE) of the selection coefficient. We find that the test has excellent power to detect weak negative selection and moderate power to detect positive selection. Moreover, the test is quite robust to bias in the estimate of local recombination rate, but not to certain demographic scenarios such as population growth or a recent bottleneck. Last, we demonstrate that the MCLE of the selection parameter has little bias for weak negative selection and has downward bias for positively selected mutations.     

Sexual selection and ecological generalism are correlated in antbirds

Sexual selection is thought to counteract natural selection on the grounds that secondary sexual traits are inherently costly and evolve at the expense of naturally selected traits. It is therefore commonly predicted that increased sexual selection is associated with decreased physiological tolerance or ecological plasticity. Using phylogenetic comparative methods, we test this prediction by exploring relationships between traits assumed to be sexually selected (plumage dichromatism and song structure) and traits assumed to be naturally selected (altitudinal range and habitat range) in a diverse family of tropical birds. Contrary to expectations, we find that taxa with higher levels of dichromatism, and lower song pitch, occupy a wider variety of habitats and elevations. In other words, indices of sexual selection are positively related to two standard measures of ecological generalism. One interpretation of this pattern is that sexual selection combines synergistically with natural selection, thereby increasing physiological tolerance or the propensity to adapt to novel environments. An alternative possibility is that ecological generalism increases population density, which in turn promotes sexual selection in the form of greater competition for mates. Overall, our results suggest that a synergism between natural selection and sexual selection may be widespread, but the processes underlying this pattern remain to be investigated.     

Conceptual issues in local adaptation

Studies of local adaptation provide important insights into the power of natural selection relative to gene flow and other evolutionary forces. They are a paradigm for testing evolutionary hypotheses about traits favoured by particular environmental factors. This paper is an attempt to summarize the conceptual framework for local adaptation studies. We first review theoretical work relevant for local adaptation. Then we discuss reciprocal transplant and common garden experiments designed to detect local adaptation in the pattern of deme × habitat interaction for fitness. Finally, we review research questions and approaches to studying the processes of local adaptation – divergent natural selection, dispersal and gene flow, and other processes affecting adaptive differentiation of local demes. We advocate multifaceted approaches to the study of local adaptation, and stress the need for experiments explicitly addressing hypotheses about the role of particular ecological and genetic factors that promote or hinder local adaptation. Experimental evolution of replicated populations in controlled spatially heterogeneous environments allow direct tests of such hypotheses, and thus would be a valuable way to complement research on natural populations.     

Dietary stress increases the total opportunity for sexual selection and modifies selection on condition‐dependent traits

Although it is often expected that adverse environmental conditions depress the expression of condition‐dependent sexually selected traits, the full consequences of environmental change for the action of sexual selection, in terms of the opportunity for total sexual selection and patterns of phenotypic selection, are unknown. Here we show that dietary stress in guppies, Poecilia reticulata, reduces the expression of several sexually selected traits and increases the opportunity for total sexual selection (standardized variance in reproductive success) in males. Furthermore, our results show that dietary stress modulates the relative importance of precopulatory (mating success) and postcopulatory (relative fertilization success) sexual selection, and that the form of multivariate sexual selection (linear vs. nonlinear) depends on dietary regime. Overall, our results are consistent with a pattern of heightened directional selection on condition‐dependent sexually selected traits under environmental stress, and underscore the importance of sexual selection in shaping adaptation in a changing world.     

Natural selection, evolvability and bias due to environmental covariance in the field in an annual plant

Estimates of the form and magnitude of natural selection based on phenotypic relationships between traits and fitness measures can be biased when environmental factors influence both relative fitness and phenotypic trait values. I quantified genetic variances and covariances, and estimated linear and quadratic selection coefficients, for seven traits of an annual plant grown in the field. For replicates of 50 paternal half-sib families, coefficients of selection were calculated both for individual phenotypic values of the traits and for half-sib family mean values. The potential for evolutionary response was supported by significant heritability and phenotypic directional selection for several traits but contradicted by the absence of significant genetic variation for fitness estimates and evidence of bias in phenotypic selection coefficients due to environmental covariance for at least two of the traits analysed. Only studies of a much wider range of organisms and traits will reveal the frequency and extent of such bias.     

GENETIC CONSTRAINTS ON ADAPTATION TO A CHANGING ENVIRONMENT

Genetic correlations between traits can constrain responses to natural selection. To what extent such correlations limit adaptation depends on patterns of directional selection. I derive the expected rate of adaptation (or evolvability) under randomly changing selection gradients. When directional selection gradients have an arbitrary covariance matrix, the average rate of adaptation depends on genetic correlations between traits, contrary to the isotropic case investigated in previous studies. Adaptation may be faster on average with more genetic correlation between traits, if these traits are selected to change jointly more often than the average pair of traits. However, natural selection maximizes the long‐term fitness of a population, not necessarily its rate of adaptation. I therefore derive the average lag load caused by deviations of the mean phenotype from an optimum, under several forms of environmental changes typically experienced by natural populations, both stochastic and deterministic. Simple formulas are produced for how the G matrix affects long‐term fitness in these contexts, and I discuss how their parameters can be estimated empirically.     

Operational sex ratio and density do not affect directional selection on male sexual ornaments and behavior

Demographic parameters including operational sex ratio (OSR) and population density may influence the opportunity for, and strength of sexual selection. Traditionally, male-biased OSRs and high population densities have been thought to increase the opportunity for sexual selection on male sexual traits due to increased male competition for mates. Recent experimental evidence, however, suggests that male-biased OSRs might reduce the opportunity for sexual selection due to increased sexual coercion experienced by females. How OSR, density, and any resultant changes in the opportunity for sexual selection actually affect selection on male sexual traits is unclear. In this study, we independently manipulated OSR and density in the guppy (Poecilia reticulata) without altering the number of males present. We recorded male and female behavior and used DNA microsatellite data to assign paternity to offspring and estimate male reproductive success. We then used linear selection analyses to examine the effects of OSR and density on directional sexual selection on male behavioral and morphological traits. We found that females were pursued more by males in male-biased treatments, despite no change in individual male behavior. There were no differences in sexual behavior experienced by females or performed by males in relation to density. Neither OSR nor density significantly altered the opportunity for sexual selection. Also, Although there was significant multivariate linear selection operating on males, neither OSR nor density altered the pattern of sexual selection on male traits. Our results suggest that differences in either OSR or density (independent of the number of males present) are unlikely to alter directional evolutionary change in male sexual traits.     

The concurrent evolution of cooperation and the population structures that support it

The evolution of cooperation often depends upon population structure, yet nearly all models of cooperation implicitly assume that this structure remains static. This is a simplifying assumption, because most organisms possess genetic traits that affect their population structure to some degree. These traits, such as a group size preference, affect the relatedness of interacting individuals and hence the opportunity for kin or group selection. We argue that models that do not explicitly consider their evolution cannot provide a satisfactory account of the origin of cooperation, because they cannot explain how the prerequisite population structures arise. Here, we consider the concurrent evolution of genetic traits that affect population structure, with those that affect social behavior. We show that not only does population structure drive social evolution, as in previous models, but that the opportunity for cooperation can in turn drive the creation of population structures that support it. This occurs through the generation of linkage disequilibrium between socio-behavioral and population-structuring traits, such that direct kin selection on social behavior creates indirect selection pressure on population structure. We illustrate our argument with a model of the concurrent evolution of group size preference and social behavior.