Apparent directional selection by biased pleiotropic mutation

Pleiotropic effects of deleterious mutations are considered to be among the factors responsible for genetic constraints on evolution by long-term directional selection acting on a quantitative trait. If pleiotropic phenotypic effects are biased in a particular direction, mutations generate apparent directional selection, which refers to the covariance between fitness and the trait owing to a linear association between the number of mutations possessed by individuals and the genotypic values of the trait. The present analysis has shown how the equilibrium mean value of the trait is determined by a balance between directional selection and biased pleiotropic mutations. Assuming that genes act additively both on the trait and on fitness, the total variance-standardized directional selection gradient was decomposed into apparent and true components. Experimental data on mutation bias from the bristle traits of Drosophila and life history traits of Daphnia suggest that apparent selection explains a small but significant fraction of directional selection pressure that is observed in nature; the data suggest that changes induced in a trait by biased pleiotropic mutation (i.e., by apparent directional selection) are easily compensated for by (true) directional selection.     

Fluctuating natural selection accounts for the evolution of diversification bet hedging

Natural environments are characterized by unpredictability over all time scales. This stochasticity is expected on theoretical grounds to result in the evolution of ‘bet-hedging’ traits that maximize the long term, or geometric mean fitness even though such traits do not maximize fitness over shorter time scales. The geometric mean principle is thus central to our interpretation of optimality and adaptation; however, quantitative empirical support for bet hedging is lacking. Here, I report a quantitative test using the timing of seed germination—a model diversification bet-hedging trait—in Lobelia inflata under field conditions. In a phenotypic manipulation study, I find the magnitude of fluctuating selection acting on seed germination timing—across 70 intervals throughout five seasons—to be extreme: fitness functions for survival are complex and multimodal within seasons and significantly dissimilar among seasons. I confirm that the observed magnitude of fluctuating selection is sufficient to account for the degree of diversification behaviour characteristic of individuals of this species. The geometric mean principle has been known to economic theory for over two centuries; this study now provides a quantitative test of optimality of a bet-hedging trait in nature.     

STABILIZING SELECTION DETECTED FOR BRISTLE NUMBER IN DROSOPHILA MELANOGASTER

Stabilizing selection, which favors intermediate phenotypes, is frequently invoked as the selective force maintaining a population's status quo. Two main alternative reasons for stabilizing selection on a quantitative trait are possible: (1) intermediate trait values can be favored through the causal effect of the trait on fitness (direct stabilizing selection); or (2) through a pleiotropic, deleterious side effect on fitness of mutants affecting the trait (apparent stabilizing selection). Up to now, these alternatives have never been experimentally disentangled. Here we measure fitness as a function of the number of abdominal bristles within four Drosophila melanogaster lines, one with high, one with low, and two with intermediate average bristle number. The four were inbred nonsegregating lines, so that apparent selection due to pleiotropy is not possible. Individual fitness significantly increased (decreased) with bristles number in the low (high) line. No significant fitness-trait association was detected within each intermediate line. These results reveal substantial direct stabilizing selection on the trait.     

Don'T fall off the adaptation cliff: when asymmetrical fitness selects for suboptimal traits

The cliff-edge hypothesis introduces the counterintuitive idea that the trait value associated with the maximum of an asymmetrical fitness function is not necessarily the value that is selected for if the trait shows variability in its phenotypic expression. We develop a model of population dynamics to show that, in such a system, the evolutionary stable strategy depends on both the shape of the fitness function around its maximum and the amount of phenotypic variance. The model provides quantitative predictions of the expected trait value distribution and provides an alternative quantity that should be maximized ("genotype fitness") instead of the classical fitness function ("phenotype fitness"). We test the model's predictions on three examples: (1) litter size in guinea pigs, (2) sexual selection in damselflies, and (3) the geometry of the human lung. In all three cases, the model's predictions give a closer match to empirical data than traditional optimization theory models. Our model can be extended to most ecological situations, and the evolutionary conditions for its application are expected to be common in nature.     

Deleterious Mutations, Apparent Stabilizing Selection and the Maintenance of Quantitative Variation

Apparent stabilizing selection on a quantitative trait that is not causally connected to fitness can result from the pleiotropic effects of unconditionally deleterious mutations, because as N. Barton noted, "...individuals with extreme values of the trait will tend to carry more deleterious alleles...." We use a simple model to investigate the dependence of this apparent selection on the genomic deleterious mutation rate, U; the equilibrium distribution of K, the number of deleterious mutations per genome; and the parameters describing directional selection against deleterious mutations. Unlike previous analyses, we allow for epistatic selection against deleterious alleles. For various selection functions and realistic parameter values, the distribution of K, the distribution of breeding values for a pleiotropically affected trait, and the apparent stabilizing selection function are all nearly Gaussian. The additive genetic variance for the quantitative trait is kQa2, where k is the average number of deleterious mutations per genome, Q is the proportion of deleterious mutations that affect the trait, and a2 is the variance of pleiotropic effects for individual mutations that do affect the trait. In contrast, when the trait is measured in units of its additive standard deviation, the apparent fitness function is essentially independent of Q and a2; and beta, the intensity of selection, measured as the ratio of additive genetic variance to the "variance" of the fitness curve, is very close to s = U/k, the selection coefficient against individual deleterious mutations at equilibrium. Therefore, this model predicts appreciable apparent stabilizing selection if s exceeds about 0.03, which is consistent with various data. However, the model also predicts that beta must equal Vm/VG, the ratio of new additive variance for the trait introduced each generation by mutation to the standing additive variance. Most, although not all, estimates of this ratio imply apparent stabilizing selection weaker than generally observed. A qualitative argument suggests that even when direct selection is responsible for most of the selection observed on a character, it may be essentially irrelevant to the maintenance of variation for the character by mutation-selection balance. Simple experiments can indicate the fraction of observed stabilizing selection attributable to the pleiotropic effects of deleterious mutations.     

Two-trait selection response with marker-based assortative mating

 Marker-based assortative mating (MAM) – the mating of individuals that have similar genotypes at random marker loci – can increase selection response for a single trait by 3–8% over random mating (RM). Genetic gain is usually desired for multiple traits rather than for a single trait. My objectives in this study were to (1) compare MAM, phenotypic assortative mating (PAM), and RM of selected individuals for improving two traits and (2) determine when MAM will be most useful for improving two traits. I simulated 20 generations of selecting 32 out of 200 individuals in an F₂ population. The individuals were selected based on an index (SI) of two traits and were intermated by MAM, PAM, or RM. I studied eight genetic models that differed in three contrasts: (1) weight, number of quantitative trait loci (QTL), and heritability (h ²) for each trait; (2) linkage of QTL for each trait; and (3) trait means of the inbred parents of the F₂. For SI and the two component traits, MAM increased short-term selection response by 5–8% in six out of the eight genetic models. The MAM procedure was least effective in two genetic models, wherein the QTL for one trait were unlinked to the QTL for the other trait and the parents of the F₂ had divergent means for each trait. The loss of QTL heterozygosity was much greater with MAM than with PAM or RM. Consequently, the advantage of MAM over RM dissipated after 5–7 generations. Differences were small between selection responses with PAM and RM. The MAM procedure can enhance short-term selection response for two traits when selection is not stringent, h ² is low, and the means of the parents of the F₂ are equal for each trait. Received: 10 June 1998 / Accepted: 5 August 1998     

On the effect of phenotypic dimensionality on adaptation and optimality

What proportion of the traits of individuals has been optimally shaped by natural selection and what has not? Here, we estimate the maximal number of those traits using a mathematical model for natural selection in multitrait organisms. The model represents the most ideal conditions for natural selection: a simple genotype–phenotype map and independent variation between traits. The model is also used to disentangle the influence of fitness functions and the number of traits, n, per se on the efficiency of natural selection. We also allow n to evolve. Our simulations show that, for all fitness functions and even in the best conditions optimal phenotypes are rarely encountered, only for n = 1, and that a large proportion of traits are always far from their optimum, specially for large n. This happens to different degrees depending on the fitness functions (additive linear, additive nonlinear, Gaussian and multiplicative). The traits that arise earlier in evolution account for a larger proportion of the absolute fitness of individuals. Thus, complex phenotypes have, in proportion, more traits that are far from optimal and the closeness to the optimum correlates with the age of the trait. Based on estimated population sizes, mutation rates and selection coefficients, we provide an upper estimation of the number of traits that can become and remain adapted by direct natural selection.     

The estimation of the fitness function from two samples taken from a population

The fitness of animals subjected to natural selection can be defined as the probability of surviving selection for a given interval of time, or some convenient multiple of this probability. If the fitness of animals is related to some quantitative variable X (such as size) then this relationship is expressed mathematically in the fitness function w(x) and this function can be estimated by comparing the distribution of X in samples taken before and after selection. In this note five methods for estimating the fitness function on the basis of samples from a large population are discussed. They are compared on three previously published sets of data and as a result estimation according to weighted multiple regression is recommended.     

REDUCED GENETIC VARIANCE AMONG HIGH FITNESS INDIVIDUALS: INFERRING STABILIZING SELECTION ON MALE SEXUAL DISPLAYS IN DROSOPHILA SERRATA

Directional selection is prevalent in nature, yet phenotypes tend to remain relatively constant, suggesting a limit to trait evolution. However, the genetic basis of this limit is unresolved. Given widespread pleiotropy, opposing selection on a trait may arise from the effects of the underlying alleles on other traits under selection, generating net stabilizing selection on trait genetic variance. These pleiotropic costs of trait exaggeration may arise through any number of other traits, making them hard to detect in phenotypic analyses. Stabilizing selection can be inferred, however, if genetic variance is greater among low‐ compared to high‐fitness individuals. We extend a recently suggested approach to provide a direct test of a difference in genetic variance for a suite of cuticular hydrocarbons (CHCs) in Drosophila serrata. Despite strong directional sexual selection on these traits, genetic variance differed between high‐ and low‐fitness individuals and was greater among the low‐fitness males for seven of eight CHCs, significantly more than expected by chance. Univariate tests of a difference in genetic variance were nonsignificant but likely have low power. Our results suggest that further CHC exaggeration in D. serrata in response to sexual selection is limited by pleiotropic costs mediated through other traits.     

An experimental assessment of artificial within-family selection for fitness in conservation programs

Equalizing familiar contributions is the simplest recommended strategy to maintain genetic diversity in conservation programs. However, this method implies a relaxation of natural selection and the possibility of accumulation of deleterious mutations. Computer simulations have shown that performing selection within families for fitness traits in a conservation program can be useful to alleviate such problems. We thus carried out an experiment with the model species Drosophila melanogaster in order to assess whether or not selection for fitness traits can be useful. We considered a fitness trait (pupa productivity) that was first checked to perform as a typical fitness component. The trait showed an inbreeding depression of 1.2 per 1 % increase in inbreeding and an asymmetrical response to selection with average realized heritabilities of about 0.04 in the upward direction and an order of magnitude larger (0.36) in the downward direction. The management experiment indicated that artificial within-family selection for fitness had only a marginal success for two reasons. First, there was not an appreciable decline in fitness across the experiment despite the low population sizes assumed (N = 10 or 20), even in the population not subjected to selection. This result is compatible with fitness models which imply the segregation of few deleterious mutations of large effect. Second, artificial selection within families had a limited impact on the trait, as one expects for a typical fitness component with very low heritability.     

THE EVOLUTION OF THRESHOLD TRAITS: A QUANTITATIVE GENETIC ANALYSIS OF THE PHYSIOLOGICAL AND LIFE-HISTORY CORRELATES OF WING DIMORPHISM IN THE SAND CRICKET

Many traits are phenotypically discrete but polygenically determined. Such traits can be understood using the threshold model of quantitative genetics that posits a continuously distributed underlying trait, called the liability, and a threshold of response, individuals above the threshold displaying one morph and individuals below the threshold displaying the alternate morph. For many threshold traits the liability probably consists of a hormone or a suite of hormones. Previous experiments have implicated juvenile hormone esterase (JHE), a degratory enzyme of juvenile hormone, as a physiological determinant of wing dimorphism in the crickets Gryllus rubens and G. firmus. The present study uses a half-sib experiment to measure the heritability of JHE in the last nymphal stadium of G. firmus and its genetic correlation with fecundity, a trait that is itself genetically correlated with wing morph. The phenotypic and genetic parameters are consistent with the hypothesis that JHE is a significant component of the liability. Comparison of sire and dam estimates suggest that nonadditive effects may be important. Two models have been proposed to account for the fitness differences between morphs: the dichotomy model, which assumes that each morph can be characterized by a particular suite of traits, and the continuous model, which assumes that the associated fitness traits are correlated with the liability rather than the morphs themselves. The latter model predicts that the fitness differences will not be constant but change with the morph frequencies. Variation in fecundity and flight muscle histolysis are shown to be more consistent with the continuous model. Data from the present experiment on JHE are inconclusive, but results from a previous selection experiment also suggest that variation in JHE is consistent only with the continuous model.     

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.     

Identifying signatures of sexual selection using genomewide selection components analysis

Sexual selection must affect the genome for it to have an evolutionary impact, yet signatures of selection remain elusive. Here we use an individual‐based model to investigate the utility of genome‐wide selection components analysis, which compares allele frequencies of individuals at different life history stages within a single population to detect selection without requiring a priori knowledge of traits under selection. We modeled a diploid, sexually reproducing population and introduced strong mate choice on a quantitative trait to simulate sexual selection. Genome‐wide allele frequencies in adults and offspring were compared using weighted F_ST values. The average number of outlier peaks (i.e., those with significantly large F_ST values) with a quantitative trait locus in close proximity (“real” peaks) represented correct diagnoses of loci under selection, whereas peaks above the F_ST significance threshold without a quantitative trait locus reflected spurious peaks. We found that, even with moderate sample sizes, signatures of strong sexual selection were detectable, but larger sample sizes improved detection rates. The model was better able to detect selection with more neutral markers, and when quantitative trait loci and neutral markers were distributed across multiple chromosomes. Although environmental variation decreased detection rates, the identification of real peaks nevertheless remained feasible. We also found that detection rates can be improved by sampling multiple populations experiencing similar selection regimes. In short, genome‐wide selection components analysis is a challenging but feasible approach for the identification of regions of the genome under selection.     

A general model of the relation between phenotypic selection and genetic response

The phenotypic view of selection assumes that genetic responses can be predicted from selective forces and heritability — or in the classical quantitative genetic equation: R = h²S. However, data on selection in bird populations show that often no selection responses is found, despite consistent selective forces on phenotypes and significant heritable variation. Such discrepancies may arise due to the assumption that selection only acts on observed phenotypes. We derive a general selection equation that takes into account the possibility that some relevant (internal or external) traits are not measured. This equation shows that the classic equation applies if selection directly acts on the measured, phenotypic traits. This is not the case when, for instance, there are unknown internal genetic trade-offs, or unknown common environmental factors affecting both trait and fitness. In such cases, any relationship between phenotypic selection and genetic response is possible. Fortunately, the classical model can be tested by comparing phenotypic and genetic covariances between traits and fitness; an indication that important internal or external traits are missing can thus be obtained. Such an analysis was indeed found in the literature; for selection on fledging weight in Great Tits it yielded valuable extra information.     

An evolutionary quantitative genetics model for phenotypic (co)variances under limited dispersal,with an application to socially synergistic traits

Darwinian evolution consists of the gradual transformation of heritable traits due to natural selection and the input of random variation by mutation. Here, we use a quantitative genetics approach to investigate the coevolution of multiple quantitative traits under selection, mutation, and limited dispersal. We track the dynamics of trait means and of variance–covariances between traits that experience frequency‐dependent selection. Assuming a multivariate‐normal trait distribution, we recover classical dynamics of quantitative genetics, as well as stability and evolutionary branching conditions of invasion analyses, except that due to limited dispersal, selection depends on indirect fitness effects and relatedness. In particular, correlational selection that associates different traits within‐individuals depends on the fitness effects of such associations between‐individuals. We find that these kin selection effects can be as relevant as pleiotropy for the evolution of correlation between traits. We illustrate this with an example of the coevolution of two social traits whose association within‐individuals is costly but synergistically beneficial between‐individuals. As dispersal becomes limited and relatedness increases, associations between‐traits between‐individuals become increasingly targeted by correlational selection. Consequently, the trait distribution goes from being bimodal with a negative correlation under panmixia to unimodal with a positive correlation under limited dispersal.     

Genotype-environment interaction for total fitness in <Emphasis Type="Italic">Drosophila</Emphasis>

A fundamental assumption of models for the maintenance of genetic variation by environmental heterogeneity is that selection favours different genotypes in different environments. Here, I use a method for measuring total fitness of chromosomal heterozygotes in Drosophila melanogaster to assess genotype-environment interaction for fitness across two ecologically relevant environments, medium with and without added ethanol. Two-third chromosomes are compared, one from a population selected for ethanol tolerance, and the other from a control population. The results show strong crossing of reaction norms for outbred, total fitness, with the chromosome from the ethanol-adapted population increasing fitness on ethanol-supplemented food, but decreasing fitness on regular food, relative to the chromosome from the control population. Although I did not map the fitness effects below the chromosome level, the method could be adapted for quantitative trait locus mapping, to determine whether a substantial proportion of fitness variation is contributed by loci at which different alleles are favoured in different environments.     

Personality‐Dependent Survival in the Marine Isopod Idotea balthica

We studied the fitness effects of animal personality by measuring activity and its relation to survival in the marine isopod Idotea balthica. We asked (1) whether activity could be considered to be a personality trait, (2) whether this trait is connected to survival, and (3) whether personality and survival exhibit sex differences. We found that activity fulfilled the criteria of personality as individuals had consistent between‐individual differences over time and across situations. Consistent individual differences in activity were associated with fitness as the survival probability of active individuals was lower, but this did not depend on sex. Our results demonstrate that personality exists in I. balthica and support recent suggestions that the association between personality and life‐history traits is a central component in mediating animal personality.     

Social phenotype extended to communities: Expanded multilevel social selection analysis reveals fitness consequences of interspecific interactions

In social species, fitness consequences are associated with both individual and social phenotypes. Social selection analysis has quantified the contribution of conspecific social traits to individual fitness. There has been no attempt, however, to apply a social selection approach to quantify the fitness implications of heterospecific social phenotypes. Here, we propose a novel social selection based approach integrating the role of all social interactions at the community level. We extended multilevel selection analysis by including a term accounting for the group phenotype of heterospecifics. We analyzed nest activity as a model social trait common to two species, the lesser kestrel (Falco naumanni) and jackdaw (Corvus monedula), nesting in either single‐ or mixed‐species colonies. By recording reproductive outcome as a measure of relative fitness, our results reveal an asymmetric system wherein only jackdaw breeding performance was affected by the activity phenotypes of both conspecific and heterospecific neighbors. Our model incorporating heterospecific social phenotypes is applicable to animal communities where interacting species share a common social trait, thus allowing an assessment of the selection pressure imposed by interspecific interactions in nature. Finally, we discuss the potential role of ecological limitations accounting for random or preferential assortments among interspecific social phenotypes, and the implications of such processes to community evolution.     

Chromosome polymorphisms and natural selection inLeptysma argentina (Orthoptera): external phenotype affected by a centric fusion predicts adult survival

The relationship between fitness variation associated with a quantitative trait and a Mendelian factor affecting that trait was examined in a natural population of the South American grasshopperLeptysma argentina. Previous studies have shown that a centric fusion between chromosomes 3 and 6 (fusion 3/6) increases adult survival and body size in this grasshopper. Here we examined the possible relationships among fusion 3/6, a size-related trait (prothorax height) and adult survival in a natural population. The study was based on two generations, comparing samples taken at the beginning and at the end of the adult life span. All individuals were karyotyped and scored for prothorax height (PH). A nonparametric regression analysis revealed that adult survival monotonically increased with PH in both generations. Moreover, fusion 3/6 was found to have an additive effect on this trait. Within generations, fusion frequency increased with adult survival in males (but not significantly so), as expected if phenotypic selection on PH influences the fusion polymorphism. Using regression analyses, we show that the correlation between PH and adult survival is not a purely environmental correlation genetically independent from the fusion polymorphism. A simple model is proposed for testing similar hypotheses in studies of selection on a trait influenced by a known genetic polymorphism.     

Wing morphology of the butterfly Coenonympha arcania in Europe: Traces of both historical isolation in glacial refugia and current adaptation

In this study, we examined the evolutionary outcome of and interplay between historic isolation and current selection pressures on traits more or less closely connected to fitness in the Pearly Heath butterfly (Coenonympha arcania) across its range in Europe. We hypothesized that a trait mean is more related to historic events if it has low connection to fitness, while a trait more closely connected with fitness is expected to have a mean that relates more to current selection pressures. In order to test this, we collected 322 butterflies from across the species range in Europe and measured five wing traits relating to size and color patterns. To infer a phylogeographic history for each individual, we sequenced a 594 bp fragment of the COI gene. The morphological data were then analyzed in relation to selected climatic variables and the history of individuals to disentangle which factors best correlated with morphological variation. The results supported our hypothesis in that wing sizes correlated with summer precipitation but not with its inferred location during the last glaciation. Eyespot position, on the other hand, correlated with the history of individuals but not with the analyzed climatic indicators. The sizes of the black spot and the white band, two traits that were expected to have intermediate selection pressure, were associated with both history and current conditions. Thus, this study illustrates the fascinating interplay between events and processes that lead to a specific evolutionary outcome.