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.     

Allometric relations in three species of finches (Aves: Fringillidae)

Static nestling, adult and ontogenetic allometry were analysed in three species of finches. Static nestling allometry was very similar across age in early ontogeny and among species and could be approximated by a single matrix of phenotypic variances and covariances. The first eigenvector of this matrix showed negative allometry of bill and tarsus to mass, but positive for wing length to mass. Adult static allometry was also very similar among species, but differed from nestling pattern. In adults the bill had a positive allometry in relation to tarsus and wing, but negative to mass, while tarsus and wing were unrelated to mass. The ontogenetic allometry in each species was very similar to nestling static allometry. Viewed in relation to final size, bill characters grew more slowly than body characters, but for a longer time, which created the difference between adult and nestling allometric patterns. There were differences among species both with regard to elevation and slope of allometric coefficients, suggesting that the differences among species came about by changes in the three fundamental ontogenetic parameters namely growth rate, onset of growth and offset of growth.     

JOINT ALLELIC EFFECTS ON FITNESS AND METRIC TRAITS

Theoretical explanations of empirically observed standing genetic variation, mutation, and selection suggest that many alleles must jointly affect fitness and metric traits. However, there are few direct demonstrations of the nature and extent of these pleiotropic associations. We implemented a mutation accumulation (MA) divergence experimental design in Drosophila serrata to segregate genetic variants for fitness and metric traits. By exploiting naturally occurring MA line extinctions as a measure of line‐level total fitness, manipulating sexual selection, and measuring productivity we were able to demonstrate genetic covariance between fitness and standard metric traits, wing size, and shape. Larger size was associated with lower total fitness and male sexual fitness, but higher productivity. Multivariate wing shape traits, capturing major axes of wing shape variation among MA lines, evolved only in the absence of sexual selection, and to the greatest extent in lines that went extinct, indicating that mutations contributing wing shape variation also typically had deleterious effects on both total fitness and male sexual fitness. This pleiotropic covariance of metric traits with fitness will drive their evolution, and generate the appearance of selection on the metric traits even in the absence of a direct contribution to fitness.     

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.     

The effect of directed and stabilizing selection on the population size of Drosophila melanogaster

Population size as a measure of population fitness was assayed in laboratory lines of Drosophila melanogaster subjected to directional selection for positive photoactivity and stabilizing selection for a complex of metric wing characters. Three experimental designs were used: directional and stabilizing selection (DS); directional selection (D); unselected controls (C). Population size increased under all three experimental designs. The population size of DS and C lines as well as the rate of increase of the DS lines were higher as compared to the D lines. The results suggest that stabilizing selection maintains population fitness at the higher level.     

Predicting evolutionary responses to selection on polyandry in the wild: additive genetic covariances with female extra-pair reproduction

The evolutionary forces that underlie polyandry, including extra-pair reproduction (EPR) by socially monogamous females, remain unclear. Selection on EPR and resulting evolution have rarely been explicitly estimated or predicted in wild populations, and evolutionary predictions are vulnerable to bias due to environmental covariances and correlated selection through unmeasured traits. However, evolutionary responses to (correlated) selection on any trait can be directly predicted as additive genetic covariances (cov_A) with appropriate components of relative fitness. I used comprehensive life-history, paternity and pedigree data from song sparrows (Melospiza melodia) to estimate cov_A between a female''s liability to produce extra-pair offspring and two specific fitness components: relative annual reproductive success (ARS) and survival to recruitment. All three traits showed non-zero additive genetic variance. Estimates of cov_A were positive, predicting evolution towards increased EPR, but 95% credible intervals overlapped zero. There was therefore no conclusive prediction of evolutionary change in EPR due to (correlated) selection through female ARS or recruitment. Negative environmental covariance between EPR and ARS would have impeded evolutionary prediction from phenotypic selection differentials. These analyses demonstrate an explicit quantitative genetic approach to predicting evolutionary responses to components of (correlated) selection on EPR that should be unbiased by environmental covariances and unmeasured traits.     

Phenotypic selection in a natural population of Impatiens pallida Nutt. (Balsaminaceae)

In the annual plant Impatiens pallida, individuals exhibit a floral heteromorphism consisting of autogamously selfing, cleistogamous (CL) flowers and partially outcrossing, chasmogamous (CH) flowers. As part of an investigation into natural selection and mating system evolution in I. pallida, we measured the magnitude and direction of phenotypic selection on nine life history characters (two traits measured on three dates, one measured on two dates and one measured once). Three of these characters were positively correlated with the ratio of CH/CL flowers produced per plant, which is an important determinant of the mating system. Values for the nine characters and three different measures of fitness (viability, fecundity, lifetime) were estimated for 500 plants in five locations over a single growing season. Based on lifetime fitness, linear selection differentials were significant for all nine characters, indicating a selective advantage to tall, leafy, highly branched plants that flowered early. However, only two of these characters had a direct effect on fitness. Selection was significant on all nine characters when based on fecundity as well as lifetime fitness; however, only three of five characters examined had significant selection based on viability fitness. For all fitness components, the frequency of significant linear and nonlinear selection coefficients was comparable (23% vs 17% of all cases, respectively), but nonlinear coefficients were generally larger. Finally, the magnitude and direction of direct linear selection was heterogeneous among locations, for all characters and all fitness components. Collectively these results suggest that selection is strong, favouring large size, high allocation to reproduction and high CH/CL flower ratios. However, any directional evolutionary changes in vegetative or reproductive characters may be constrained by strong non-linear and correlational selection.     

EVOLUTION OF VARIATION AND VARIABILITY UNDER FLUCTUATING,STABILIZING, AND DISRUPTIVE SELECTION

How variation and variability (the capacity to vary) may respond to selection remain open questions. Indeed, effects of different selection regimes on variational properties, such as canalization and developmental stability are under debate. We analyzed the patterns of among‐ and within‐individual variation in two wing‐shape characters in populations of Drosophila melanogaster maintained under fluctuating, disruptive, and stabilizing selection for more than 20 generations. Patterns of variation in wing size, which was not a direct target of selection, were also analyzed. Disruptive selection dramatically increased phenotypic variation in the two shape characters, but left phenotypic variation in wing size unaltered. Fluctuating and stabilizing selection consistently decreased phenotypic variation in all traits. In contrast, within‐individual variation, measured by the level of fluctuating asymmetry, increased for all traits under all selection regimes. These results suggest that canalization and developmental stability are evolvable and presumably controlled by different underlying genetic mechanisms, but the evolutionary responses are not consistent with an adaptive response to selection on variation. Selection also affected patterns of directional asymmetry, although inconsistently across traits and treatments.     

Components of phenotypic variation in avian ornamental and non-ornamental feathers

Phenotypic variation, measured as the coefficient of variation (CV), is usually larger in secondary sexual characters than in ordinary morphological traits. We tested if intraspecific differences in the CV between ornamental and non-ornamental feather traits in 67 evolutionary events of feather ornamentation in birds were due to differences in (1) the allometric pattern (slope of the regression line when regressing trait size on an indicator of body size), or (2) the dispersion of observations around the regression line. We found that only dispersion of observations around the regression line contributed significantly to total variation. A large dispersion of observations around the regression line for ornamental feathers is consistent with these characters showing condition-dependence, supporting indicator models of sexual selection more strongly than a pure Fisher process. Ornamental feathers in males demonstrated negative allometry when regressed on tarsus length, which is a measure of skeletal body size. This finding is consistent with ornamental feather traits being subject to directional selection due to female mate preferences, where large body size is less important than in male–male competition. This pattern of phenotypic variation for avian secondary sexual characters contrasts with patterns of variation for insect genitalia, supposedly subject to sexual selection, since the latter traits only differ from ordinary morphology traits in allometry coefficient. The prevailing regime of selection (directional or stabilizing) and the effects of environmental factors are proposed to account for these differences among traits.     

Variation in pleiotropy and the mutational underpinnings of the G-matrix

The pattern and extent of pleiotropic gene action can contribute substantially to the internal structure and shape of the additive genetic variance-covariance matrix (G)--a key determinant of evolutionary trajectories. We use data from our study (Estes et al. 2004) on the univariate effects of mutation in a mismatch-repair-defective strain, msh-2, of Caenorhabditis elegans to address the impact of increasing levels of selection on the magnitude and pattern of genetic covariance due to new mutations. Mutational covariances between three life-history traits are shown to exhibit a weak pattern of decline with increasing population size (increasing selection), while the orientation of mutational matrices remains reasonably constant. This suggests that mutations with smaller effects on fitness may tend to be slightly more confined in their influence than large-effect mutations (i.e., small-effect mutations reduce the magnitude of covariation between characters), but do not change the direction of this covariation.     

THE MEASUREMENT OF SELECTION ON QUANTITATIVE TRAITS: BIASES DUE TO ENVIRONMENTAL COVARIANCES BETWEEN TRAITS AND FITNESS

The use of regression techniques for estimating the direction and magnitude of selection from measurements on phenotypes has become widespread in field studies. A potential problem with these techniques is that environmental correlations between fitness and the traits examined may produce biased estimates of selection gradients. This report demonstrates that the phenotypic covariance between fitness and a trait, used as an estimate of the selection differential in estimating selection gradients, has two components: a component induced by selection itself and a component due to the effect of environmental factors on fitness. The second component is shown to be responsible for biases in estimates of selection gradients. The use of regressions involving genotypic and breeding values instead of phenotypic values can yield estimates of selection gradients that are not biased by environmental covariances. Statistical methods for estimating the coefficients of such regressions, and for testing for biases in regressions involving phenotypic values, are described.     

LONG-TERM CORRELATED RESPONSE,INTERPOPULATION COVARIATION,AND INTERSPECIFIC ALLOMETRY

A model of long-term correlated evolution of multiple quantitative characters is analyzed, which partitions selection into two components: one stabilizing and the other directional. The model assumes that the stabilizing component is less variable than the directional component among populations. The major result is that, within a population, the responses of characters to selection in the short term differ qualitatively from those in the long term. In the short term, the responses depend on genetic correlations between characters, but in the long term they are only determined by the fitness functions of stabilizing and directional selection, independent of genetic and phenotypic correlations. Treating the stabilizing component as a constant and assuming the directional component to vary among populations, I present formulas for the interpopulation covariation and interspecific allometry, which are functions of the intensity matrix of stabilizing selection. Particular attention is paid to the relationship between intra- and interpopulation correlations.     

Pitfalls in understanding the functional significance of genital allometry

The male genitalia of arthropods consistently show negative static allometry (the genitalia of small males of a species are disproportionally large, and those of large males are disproportionally small). We discuss relations between the ‘one‐size‐fits‐all’ hypothesis to explain this allometry and the regimes of selection that may be acting on genitalia. We focus on the contrasts between directional vs. stabilizing selection, and natural vs. sexual selection. In addition, we point out some common methodological problems in studies of genital allometry. One‐size‐fits‐all types of arguments for negative allometry imply net stabilizing selection, but the effects of stabilizing selection on allometry will be weaker when the correlation between body size and the trait size is weaker. One‐size‐fits‐all arguments can involve natural as well as sexual selection, and negative allometry can also result from directional selection. Several practical problems make direct tests of whether directional or stabilizing selection is acting difficult. One common methodological problem in previous studies has been concentration on absolute rather than relative values of the allometric slopes of genitalia; there are many reasons to doubt the usefulness of comparing absolute slopes with the usual reference value of 1.00. Another problem has been the failure to recognize that size and shape are independent traits of genitalia; rapid divergence in the shape of genitalia is thus not paradoxical with respect to the reduced variation in their sizes that is commonly associated with negative allometric scaling.     

The prediction of adaptive evolution: empirical application of the secondary theorem of selection and comparison to the breeder's equation

Adaptive evolution occurs when fitness covaries with genetic merit for a trait (or traits). The breeder's equation (BE), in both its univariate and multivariate forms, allows us to predict this process by combining estimates of selection on phenotype with estimates of genetic (co)variation. However, predictions are only valid if all factors causal for trait-fitness covariance are measured. Although this requirement will rarely (if ever) be met in practice, it can be avoided by applying Robertson's secondary theorem of selection (STS). The STS predicts evolution by directly estimating the genetic basis of trait-fitness covariation without any explicit model of selection. Here we apply the BE and STS to four morphological traits measured in Soay sheep (Ovis aries) from St. Kilda. Despite apparently positive selection on heritable size traits, sheep are not getting larger. However, although the BE predicts increasing size, the STS does not, which is a discrepancy that suggests unmeasured factors are upwardly biasing our estimates of selection on phenotype. We suggest this is likely to be a general issue, and that wider application of the STS could offer at least a partial resolution to the common discrepancy between naive expectations and observed trait dynamics in natural populations.     

Are wing size,wing shape and asymmetry related to field fitness of Trichogramma egg parasitoids?

The effects of wing shape, wing size, and fluctuating asymmetry in these measures on the field fitness of T. nr. brassicae and T. pretiosum were investigated. Trichogramma wasps mass-reared on eggs of the factitious host Sitotroga cerealella were released in tomato paddocks and those females ovipositing on Helicoverpa spp. eggs were recaptured. Comparisons of the recaptured group with a sample from the release population were used to assess fitness. Wing data were obtained by positioning landmarks on mounted forewings. Size was then measured as the centroid size computed from landmark distances, while Procrustes analysis followed by principal component analysis was used to assess wing shape. Similar findings were obtained for both Trichogramma species: fitness of wasps was strongly related to wing size and some shape dimensions, but not to the asymmetries of these measures. Wasps which performed well in the field had larger wings and a different wing shape compared to wasps from the mass reared population. Both size and the shape dimensions were linearly associated with fitness although there was also some evidence for non-linear selection on shape. The results suggest that wing shape and wing size are reliable predictors of field fitness for these Trichogramma wasps.     

SEXUAL SELECTION AND SURVIVAL SELECTION ON WING COLORATION AND BODY SIZE IN THE RUBYSPOT DAMSELFLY HETAERINA AMERICANA

I review methodological problems that can lead to false evidence for selection on secondary sexual characters and present a study of selection in rubyspot damselflies (Hetaerina americana) that avoids these pitfalls. Male rubyspots have a large red spot on each wing that grows to a terminal size after sexual maturity. Selection gradient analyses revealed evidence for positive sexual and survival selection on both terminal wing spot size and body size. Phenotype manipulations confirmed that wing spot size was subject to direct sexual selection, but showed that the positive slope of survival on wing spot size was an indirect effect of selection on unmeasured traits. This study provides the strongest evidence yet for sexual selection on coloration in Odonata, but also provides clear examples of why phenotypic selection statistics must be calculated and interpreted cautiously.     

Effects of bottlenecks on quantitative genetic variation in the butterfly Bicyclus anynana

The effects of a single population bottleneck of differing severity on heritability and additive genetic variance was investigated experimentally using a butterfly. An outbred laboratory stock was used to found replicate lines with one pair, three pairs and 10 pairs of adults, as well as control lines with approximately 75 effective pairs. Heritability and additive genetic variance of eight wing pattern characters and wing size were estimated using parent-offspring covariances in the base population and in all daughter lines. Individual morphological characters and principal components of the nine characters showed a consistent pattern of treatment effects in which average heritability and additive genetic variance was lower in one pair and three pair lines than in 10 pair and control lines. Observed losses in heritability and additive genetic variance were significantly greater than predicted by the neutral additive model when calculated with coefficients of inbreeding estimated from demographic parameters alone. However, use of molecular markers revealed substantially more inbreeding, generated by increased variance in family size and background selection. Conservative interpretation of a statistical analysis incorporating this previously undetected inbreeding led to the conclusion that the response to inbreeding of the morphological traits studied showed no significant departure from the neutral additive model. This result is consistent with the evidence for minimal directional dominance for these traits. In contrast, egg hatching rate in the same experimental lines showed strong inbreeding depression, increased phenotypic variance and rapid response to selection, highly indicative of an increase in additive genetic variance due to dominance variance conversion.     

Reducing bias in the measurement of selection

Selection on quantitative characters is commonly mesured in natural populations using regression techniques based on phenotypic covariances between traits and fitness. However, such methods do not give an accutate view of the causal relationship between the phenotype and fitness if enviornmental factors also contribute to covariances between traits and fitness. A recently developed method for estimating selection eliminates the problem of bias resulting from enviormental covariances. This underappreciated method represents a significant addition to the toolbox of evolutionary ecologist.     

Nonlinear selection and the evolution of variances and covariances for continuous characters in an anole

The pattern of genetic variances and covariances among characters, summarized in the additive genetic variance‐covariance matrix, G , determines how a population will respond to linear natural selection. However, G itself also evolves in response to selection. In particular, we expect that, over time, G will evolve correspondence with the pattern of multivariate nonlinear natural selection. In this study, we substitute the phenotypic variance‐covariance matrix ( P ) for G to determine if the pattern of multivariate nonlinear selection in a natural population of Anolis cristatellus, an arboreal lizard from Puerto Rico, has influenced the evolution of genetic variances and covariances in this species. Although results varied among our estimates of P and fitness, and among our analytic techniques, we find significant evidence for congruence between nonlinear selection and P , suggesting that natural selection may have influenced the evolution of genetic constraint in this species.     

Growth and allometry of external morphology in Darwin's finches (Geospiza) on Isla Daphne Major, Galapagos

Seven widely used avian external morphological measurements were examined, mainly in Geospiza fortis and G. scandens on Isla Daphne Major, Galapagos. Geospiza grow more slowly than other "finches", and smaller Geospiza species grow relatively more slowly than larger Geospiza . Weight, wing chord and tarsus grow quickly, while bill characters grow more slowly. This pattern of relative growth (dynamic allometry) is reversed in the static allometry of adults, where bill characters, particularly bill depth in G. fortis , display strong, positive allometry with respect to weight, wing and tarsus. Static allometric patterns help explain differences in the size, shape and relative variability of different characters in adults, as well as the results of multivariate analyses such as principal components or canonical variates. Several different multivariate techniques arrange five Geospiza populations in a consistent two-dimensional morphological space, with a major axis of overall "body-size", and a minor axi of "bill-pointedeness". An alternative analysis of dynamic and static allometry is also provided, based on multivariate techniques.