Sexual selection and temporal phenotypic variation in a damselfly population

Temporal variation in selection can be generated by temporal variation in either the fitness surface or phenotypic distributions around a static fitness surface, or both concurrently. Here, we use within- and between-generation sampling of fitness surfaces and phenotypic distributions over 2 years to investigate the causes of temporal variation in the form of sexual selection on body size in the damselfly Enallagma aspersum. Within a year, when the average female body size differed substantially from the average male body size, male body size experienced directional selection. In contrast, when male and female size distributions overlapped, male body size experienced stabilizing selection when variances in body size were large, but no appreciable selection when the variances in body size were small. The causes of temporal variation in the form of selection can only be inferred by accounting for changes in both the fitness surface and changes in the distribution of phenotypes.     

The evolution of genetic canalization under fluctuating selection

Abstract.— If the direction of selection changes from generation to generation, the ability to respond to selection is maladaptive: the response to selection in one generation leads to reduced fitness in the next. Because the response is determined by the amount of genetic variance expressed at the phenotypic level, rapidly fluctuating selection should favor modifier genes that reduce the phenotypic effect of alleles segregating at structural loci underlying the trait. Such reduction in phenotypic expression of genetic variation has been named "genetic canalization." I support this argument with a series of two- and multilocus models with alternating linear selection and Gaussian selection with fluctuating optimum. A canalizing modifier gene affects the fitness of its carriers in three ways: (1) it reduces the phenotypic consequences of genetic response to previous selection; (2) it reduces the genetic response to selection, which is manifested as linkage disequilibrium between the modifier and structural loci; and (3) it reduces the phenotypic variance. The first two effects reduce fitness under directional selection sustained for several generations, but improve fitness when the direction of selection has just been reversed. The net effect tends to favor a canalizing modifier under rapidly fluctuating selection regimes (period of eight generations or less). The third effect improves fitness of the modifier allele if the fitness function is convex and reduces it if the function is concave. Under fluctuating Gaussian selection, the population is more likely to experience the concave portion of the fitness function when selection is stronger. Therefore, only weak to moderately strong fluctuating Gaussian selection favors genetic canalization. This paper considerably broadens the conditions that favor genetic canalization, which so far has only been postulated to evolve under long-term stabilizing selection.     

Selection on skewed characters and the paradox of stasis

Observed phenotypic responses to selection in the wild often differ from predictions based on measurements of selection and genetic variance. An overlooked hypothesis to explain this paradox of stasis is that a skewed phenotypic distribution affects natural selection and evolution. We show through mathematical modeling that, when a trait selected for an optimum phenotype has a skewed distribution, directional selection is detected even at evolutionary equilibrium, where it causes no change in the mean phenotype. When environmental effects are skewed, Lande and Arnold's (1983) directional gradient is in the direction opposite to the skew. In contrast, skewed breeding values can displace the mean phenotype from the optimum, causing directional selection in the direction of the skew. These effects can be partitioned out using alternative selection estimates based on average derivatives of individual relative fitness, or additive genetic covariances between relative fitness and trait (Robertson–Price identity). We assess the validity of these predictions using simulations of selection estimation under moderate sample sizes. Ecologically relevant traits may commonly have skewed distributions, as we here exemplify with avian laying date — repeatedly described as more evolutionarily stable than expected — so this skewness should be accounted for when investigating evolutionary dynamics in the wild.     

Quantification and decomposition of environment‐selection relationships

In nature, selection varies across time in most environments, but we lack an understanding of how specific ecological changes drive this variation. Ecological factors can alter phenotypic selection coefficients through changes in trait distributions or individual mean fitness, even when the trait‐absolute fitness relationship remains constant. We apply and extend a regression‐based approach in a population of Soay sheep (Ovis aries) and suggest metrics of environment‐selection relationships that can be compared across studies. We then introduce a novel method that constructs an environmentally structured fitness function. This allows calculation of full (as in existing approaches) and partial (acting separately through the absolute fitness function slope, mean fitness, and phenotype distribution) sensitivities of selection to an ecological variable. Both approaches show positive overall effects of density on viability selection of lamb mass. However, the second approach demonstrates that this relationship is largely driven by effects of density on mean fitness, rather than on the trait‐fitness relationship slope. If such mechanisms of environmental dependence of selection are common, this could have important implications regarding the frequency of fluctuating selection, and how previous selection inferences relate to longer term evolutionary dynamics.     

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.     

UNIFICATION OF REGRESSION‐BASED METHODS FOR THE ANALYSIS OF NATURAL SELECTION

Regression analyses are central to characterization of the form and strength of natural selection in nature. Two common analyses that are currently used to characterize selection are (1) least squares–based approximation of the individual relative fitness surface for the purpose of obtaining quantitatively useful selection gradients, and (2) spline‐based estimation of (absolute) fitness functions to obtain flexible inference of the shape of functions by which fitness and phenotype are related. These two sets of methodologies are often implemented in parallel to provide complementary inferences of the form of natural selection. We unify these two analyses, providing a method whereby selection gradients can be obtained for a given observed distribution of phenotype and characterization of a function relating phenotype to fitness. The method allows quantitatively useful selection gradients to be obtained from analyses of selection that adequately model nonnormal distributions of fitness, and provides unification of the two previously separate regression‐based fitness analyses. We demonstrate the method by calculating directional and quadratic selection gradients associated with a smooth regression‐based generalized additive model of the relationship between neonatal survival and the phenotypic traits of gestation length and birth mass in humans.     

Synthetic analyses of phenotypic selection in natural populations: lessons, limitations and future directions

There are now thousands of estimates of phenotypic selection in natural populations, resulting in multiple synthetic reviews of these data. Here we consider several major lessons and limitations emerging from these syntheses, and how they may guide future studies of selection in the wild. First, we review past analyses of the patterns of directional selection. We present new meta-analyses that confirm differences in the direction and magnitude of selection for different types of traits and fitness components. Second, we describe patterns of temporal and spatial variation in directional selection, and their implications for cumulative selection and directional evolution. Meta-analyses suggest that sampling error contributes importantly to observed temporal variation in selection, and indicate that evidence for frequent temporal changes in the direction of selection in natural populations is limited. Third, we review the apparent lack of evidence for widespread stabilizing selection, and discuss biological and methodological explanations for this pattern. Finally, we describe how sampling error, statistical biases, choice of traits, fitness measures and selection metrics, environmental covariance and other factors may limit the inferences we can draw from analyses of selection coefficients. Current standardized selection metrics based on simple parametric statistical models may be inadequate for understanding patterns of non-linear selection and complex fitness surfaces. We highlight three promising areas for expanding our understanding of selection in the wild: (1) field studies of stabilizing selection, selection on physiological and behavioral traits, and the ecological causes of selection; (2) new statistical models and methods that connect phenotypic variation to population demography and selection; and (3) availability of the underlying individual-level data sets from past and future selection studies, which will allow comprehensive modeling of selection and fitness variation within and across systems, rather than meta-analyses of standardized selection metrics.     

Evolutionary stasis of a heritable morphological trait in a wild fish population despite apparent directional selection

Comparing observed versus theoretically expected evolutionary responses is important for our understanding of the evolutionary process, and for assessing how species may cope with anthropogenic change. Here, we document directional selection for larger female size in Atlantic salmon, using pedigree‐derived estimates of lifetime reproductive success as a fitness measure. We show the trait is heritable and, thus, capable of responding to selection. The Breeder's Equation, which predicts microevolution as the product of phenotypic selection and heritability, predicted evolution of larger size. This was at odds, however, with the observed lack of either phenotypic or genetic temporal trends in body size, a so‐called “paradox of stasis.” To investigate this paradox, we estimated the additive genetic covariance between trait and fitness, which provides a prediction of evolutionary change according to Robertson's secondary theorem of selection (STS) that is unbiased by missing variables. The STS prediction was consistent with the observed stasis. Decomposition of phenotypic selection gradients into genetic and environmental components revealed a potential upward bias, implying unmeasured factors that covary with trait and fitness. These results showcase the power of pedigreed, wild population studies—which have largely been limited to birds and mammals—to study evolutionary processes on contemporary timescales.     

Adaptive topography of fluctuating selection in a Mendelian population

An adaptive topography is derived for a large randomly mating diploid population under weak density-independent selection in a fluctuating environment. Assuming a stationary distribution of environmental states with no temporal autocorrelation, a diffusion approximation for population size and allele frequency, p, reveals that the expected change in p involves the gradient with respect to p of the stochastic intrinsic rate of increase (the density-independent long-run growth rate), r = r - sigma 2 e/2, where r is the mean Malthusian fitness in the average environment and is the environmental variance in population growth rate. The expected relative fitness of a genotype is its Malthusian fitness in the average environment minus the covariance of its fitness with population growth rate. The influence of fitness correlation between genotypes is illustrated by an analysis of the Haldane-Jayakar model of fluctuating selection on a single diallelic locus, and on two loci with additive effects on a quantitative character.     

Stabilizing selection and adaptive evolution in a combination of two traits in an arctic ungulate

Stabilizing selection is thought to be common in wild populations and act as one of the main evolutionary mechanisms, which constrain phenotypic variation. When multiple traits interact to create a combined phenotype, correlational selection may be an important process driving adaptive evolution. Here, we report on phenotypic selection and evolutionary changes in two natal traits in a semidomestic population of reindeer (Rangifer tarandus) in northern Finland. The population has been closely monitored since 1969, and detailed data have been collected on individuals since they were born. Over the length of the study period (1969–2015), we found directional and stabilizing selection toward a combination of earlier birth date and heavier birth mass with an intermediate optimum along the major axis of the selection surface. In addition, we demonstrate significant changes in mean traits toward earlier birth date and heavier birth mass, with corresponding genetic changes in breeding values during the study period. Our results demonstrate evolutionary changes in a combination of two traits, which agree closely with estimated patterns of phenotypic selection. Knowledge of the selective surface for combinations of genetically correlated traits are vital to predict how population mean phenotypes and fitness are affected when environments change.     

Estimating selection on neonatal traits in red deer using elasticity path analysis

Van Tienderen recently published a method that links selection gradients between a phenotypic trait and multiple fitness components with the effects of these fitness components on the population growth rate (mean absolute fitness). The method allows selection to be simultaneously estimated across multiple fitness components in a population dynamic framework. In this paper we apply the method to a population of red deer living in the North Block of the Isle of Rum, Scotland. We show that (1) selection on birth date and birth weight can operate through multiple fitness components simultaneously; (2) our estimates of the response to selection are consistent with the observed change in trait values that we cannot explain with environmental and phenotypic covariates; (3) selection on both traits has fluctuated over the course of the study; (4) selection operates through different fitness components in different years; and (5) no environmental covariates correlate with selection because different fitness components respond to density and climatic variation in contrasting ways.     

Evolutionary aspects and sensitivity studies of some major gene models

Extensive biometrical and statistically oriented studies in segregation and pedigree analyses reflect current efforts to demonstrate major gene factors playing a significant role for a whole hierarchy of multifactorial diseases and related risk factors exhibiting continuous variation. The evolutionary aspects of the changes in gene frequencies of some major gene one locus models admitting a broad range of genotype-phenotype associations and different forms of selection functions are investigated. The flexibility of differences among the genotypic-phenotypic distribution can take account of variable penetrance expressivity, complex multifarious heterogeneous background effects, or partial dominance concepts. The phenotype distribution and selection function are assumed to be time invariant such that the environments with which the population interacts do not depend on either the phenotypes or the genotypes present in the population of any particular generation. Viability selection optimizing or directional acts on the phenotypic level. We consider random mating, and concentrate mostly on evaluating the nature of the equilibrium structure for the cases of “strong” and “weak” selection. For weak stabilizing selection the determinants of superior genotypic fitness in the class of phenotypic symmetric distributions reside in minimizing a combination of the phenotypic variance and the deviation of the phenotypic mean from the optimal phenotype. With equal means of central phenotype values, a canalizing selection effect signifying fitness superiority for the genotype with minimal variance is in force. For strong stabilizing selection the genotype-phenotype density at the optimal value determines the relative genotype fitness value. For directional selection the determinants of the selection realizations depend on a “standardized” deviation of the mean phenotype distributional value relative to its total variance. The effects of symmetry as against asymmetry in the genotype distributions with prescribed means and variances were investigated by numerical computations.     

Expected relative fitness and the adaptive topography of fluctuating selection

Wright's adaptive topography describes gene frequency evolution as a maximization of mean fitness in a constant environment. I extended this to a fluctuating environment by unifying theories of stochastic demography and fluctuating selection, assuming small or moderate fluctuations in demographic rates with a stationary distribution, and weak selection among the types. The demography of a large population, composed of haploid genotypes at a single locus or normally distributed phenotypes, can then be approximated as a diffusion process and transformed to produce the dynamics of population size, N, and gene frequency, p, or mean phenotype, . The expected evolution of p or is a product of genetic variability and the gradient of the long-run growth rate of the population, , with respect to p or . This shows that the expected evolution maximizes , the mean Malthusian fitness in the average environment minus half the environmental variance in population growth rate. Thus, as a function of p or represents an adaptive topography that, despite environmental fluctuations, does not change with time. The haploid model is dominated by environmental stochasticity, so the expected maximization is not realized. Different constraints on quantitative genetic variability, and stabilizing selection in the average environment, allow evolution of the mean phenotype to undergo a stochastic maximization of . Although the expected evolution maximizes the long-run growth rate of the population, for a genotype or phenotype the long-run growth rate is not a valid measure of fitness in a fluctuating environment. The haploid and quantitative character models both reveal that the expected relative fitness of a type is its Malthusian fitness in the average environment minus the environmental covariance between its growth rate and that of the population.     

Evolutionary mismatch along salinity gradients in a Neotropical water strider

The evolution of local adaptation is crucial for the in situ persistence of populations in changing environments. However, selection along broad environmental gradients could render local adaptation difficult, and might even result in maladaptation. We address this issue by quantifying fitness trade‐offs (via common garden experiments) along a salinity gradient in two populations of the Neotropical water strider Telmatometra withei—a species found in both fresh (FW) and brackish (BW) water environments across Panama. We found evidence for local adaptation in the FW population in its home FW environment. However, the BW population showed only partial adaptation to the BW environment, with a high magnitude of maladaptation along naturally occurring salinity gradients. Indeed, its overall fitness was ~60% lower than that of the ancestral FW population in its home environment, highlighting the role of phenotypic plasticity, rather than local adaptation, in high salinity environments. This suggests that populations seemingly persisting in high salinity environments might in fact be maladapted, following drastic changes in salinity. Thus, variable selection imposed by salinization could result in evolutionary mismatch, where the fitness of a population is displaced from its optimal environment. Understanding the fitness consequences of persisting in fluctuating salinity environments is crucial to predict the persistence of populations facing increasing salinization. It will also help develop evolutionarily informed management strategies in the context of global change.     

Genetic variation and the potential response to selection on leaf traits after habitat degradation in a long-lived cycad

Rapid evolution may be common in human-dominated landscapes where environmental changes are severe. We used phenotypic selection analyses and a marker-based method to estimate genetic variances and covariances to predict the potential response to selection in populations of a long-lived cycad recently exposed to drastic environmental changes. Patterns of selection in adult fecundity showed that different traits were under directional selection in subpopulations from native-undisturbed habitats and the novel degraded-forest habitat. Plants from a native-habitat subpopulation tend to maximize fitness through larger leaf area or smaller specific leaf area (SLA). In contrast, larger leaf production increased fitness in a degraded-habitat subpopulation, and canopy openness appears to be a major agent of selection for this trait. Leaf production and SLA showed significant additive genetic variance and no genetic trade-offs with examined traits, suggesting that these traits can respond to selection. Directional selection coefficients and heritability values were large, therefore significant phenotypic changes between subpopulations in few generations are possible. These results suggest that recent environmental change can result in strong directional selection in subpopulations of this cycad, and that these subpopulations have the potential to diverge at the genetic level in leaf traits after anthropogenic habitat degradation.     

Phenotypic selection in natural populations: what limits directional selection?

Studies of phenotypic selection document directional selection in many natural populations. What factors reduce total directional selection and the cumulative evolutionary responses to selection? We combine two data sets for phenotypic selection, representing more than 4,600 distinct estimates of selection from 143 studies, to evaluate the potential roles of fitness trade-offs, indirect (correlated) selection, temporally varying selection, and stabilizing selection for reducing net directional selection and cumulative responses to selection. We detected little evidence that trade-offs among different fitness components reduced total directional selection in most study systems. Comparisons of selection gradients and selection differentials suggest that correlated selection frequently reduced total selection on size but not on other types of traits. The direction of selection on a trait often changes over time in many temporally replicated studies, but these fluctuations have limited impact in reducing cumulative directional selection in most study systems. Analyses of quadratic selection gradients indicated stabilizing selection on body size in at least some studies but provided little evidence that stabilizing selection is more common than disruptive selection for most traits or study systems. Our analyses provide little evidence that fitness trade-offs, correlated selection, or stabilizing selection strongly constrains the directional selection reported for most quantitative traits.     

FISHER'S GEOMETRIC MODEL WITH A MOVING OPTIMUM

Fisher's geometric model has been widely used to study the effects of pleiotropy and organismic complexity on phenotypic adaptation. Here, we study a version of Fisher's model in which a population adapts to a gradually moving optimum. Key parameters are the rate of environmental change, the dimensionality of phenotype space, and the patterns of mutational and selectional correlations. We focus on the distribution of adaptive substitutions, that is, the multivariate distribution of the phenotypic effects of fixed beneficial mutations. Our main results are based on an “adaptive‐walk approximation,” which is checked against individual‐based simulations. We find that (1) the distribution of adaptive substitutions is strongly affected by the ecological dynamics and largely depends on a single composite parameter γ, which scales the rate of environmental change by the “adaptive potential” of the population; (2) the distribution of adaptive substitution reflects the shape of the fitness landscape if the environment changes slowly, whereas it mirrors the distribution of new mutations if the environment changes fast; (3) in contrast to classical models of adaptation assuming a constant optimum, with a moving optimum, more complex organisms evolve via larger adaptive steps.     

The Effects of Stabilizing and Directional Selection on Phenotypic and Genotypic Variation in a Population of RNA Enzymes

The distribution of variation in a quantitative trait and its underlying distribution of genotypic diversity can both be shaped by stabilizing and directional selection. Understanding either distribution is important, because it determines a population’s response to natural selection. Unfortunately, existing theory makes conflicting predictions about how selection shapes these distributions, and very little pertinent experimental evidence exists. Here we study a simple genetic system, an evolving RNA enzyme (ribozyme) in which a combination of high throughput genotyping and measurement of a biochemical phenotype allow us to address this question. We show that directional selection, compared to stabilizing selection, increases the genotypic diversity of an evolving ribozyme population. In contrast, it leaves the variance in the phenotypic trait unchanged.     

Repeated selection of morphometric traits in the Soay sheep on St Kilda

1. Long-term studies allow the outcomes of repeated selection events to be monitored. Here, we investigate phenotypic selection in successive winter mortality events in the Soay sheep of St Kilda, Scotland, between 1985 and 1996. Selection of three quantitative morphometric traits, body weight, hindleg length and incisor arcade breadth, was investigated in different sectors of the population.
2. Evidence from fitness differentials of positive directional selection for large size was repeatedly found in lambs and adult females. Selection in the opposing direction was only found in one year in lambs.
3. Selection gradients showed that in most years when significant selection occurred, body weight was the focus of direct selection, whereas selection of hindleg length and incisor breadth was indirect, arising from their correlation with body weight.
4. Selection was strongest in years of low over-winter survival and almost absent in years when survival was high. Intensity of selection was greatest in lambs, emphasizing the differences in selection pressure experienced by different sectors of the population, in addition to the temporal variation in selection pressure due to population density and environmental conditions.
5. Despite repeated positive selection of body weight, no evidence of a change in the population mean was found over the course of the study.     

Selection in a fluctuating environment leads to decreased genetic variation and facilitates the evolution of phenotypic plasticity

Changes in the environment are expected to induce changes in the quantitative genetic variation, which influences the ability of a population to adapt to environmental change. Furthermore, environmental changes are not constant in time, but fluctuate. Here, we investigate the effect of rapid, continuous and/or fluctuating temperature changes in the seed beetle Callosobruchus maculatus, using an evolution experiment followed by a split-brood experiment. In line with expectations, individuals responded in a plastic way and had an overall higher potential to respond to selection after a rapid change in the environment. After selection in an environment with increasing temperature, plasticity remained unchanged (or decreased) and environmental variation decreased, especially when fluctuations were added; these results were unexpected. As expected, the genetic variation decreased after fluctuating selection. Our results suggest that fluctuations in the environment have major impact on the response of a population to environmental change; in a highly variable environment with low predictability, a plastic response might not be beneficial and the response is genetically and environmentally canalized resulting in a low potential to respond to selection and low environmental sensitivity. Interestingly, we found greater variation for phenotypic plasticity after selection, suggesting that the potential for plasticity to evolve is facilitated after exposure to environmental fluctuations. Our study highlights that environmental fluctuations should be considered when investigating the response of a population to environmental change.