Internal and external constraints in the evolution of morphological allometries in a butterfly

Much diversity in animal morphology results from variation in the relative size of morphological traits. The scaling relationships, or allometries, that describe relative trait size can vary greatly in both intercept and slope among species or other animal groups. Yet within such groups, individuals typically exhibit low variation in relative trait size. This pattern of high intra- and low intergroup variation may result from natural selection for particular allometries, from developmental constraints restricting differential growth among traits, or both. Here we explore the relative roles of short-term developmental constraints and natural selection in the evolution of the intercept of the allometry between the forewing and hindwing of a butterfly. First, despite a strong genetic correlation between these two traits, we show that artificial selection perpendicular to the forewing-hindwing scaling relationship results in rapid evolution of the allometry intercept. This demonstrates an absence of developmental constraints limiting intercept evolution for this scaling relationship. Mating experiments in a natural environment revealed strong stabilizing selection favoring males with the wild-type allometry intercept over those with derived intercepts. Our results demonstrate that evolution of this component of the forewing-hindwing allometry is not limited by developmental constraints in the short term and that natural selection on allometry intercepts can be powerful.     

The evolution of trade‐offs: where are we?

Trade-offs are a core component of many evolutionary models, particularly those dealing with the evolution of life histories. In the present paper, we identify four topics of key importance for studies of the evolutionary biology of trade-offs. First, we consider the underlying concept of 'constraint'. We conclude that this term is typically used too vaguely and suggest that 'constraint' in the sense of a bias should be clearly distinguished from 'constraint' in the sense of proscribed combinations of traits or evolutionary trajectories. Secondly, we address the utility of the acquisition-allocation model (the 'Y-model'). We find that, whereas this model and its derivatives have provided new insights, a misunderstanding of the pivotal equation has led to incorrect predictions and faulty tests. Thirdly, we ask how trade-offs are expected to evolve under directional selection. A quantitative genetic model predicts that, under weak or short-term selection, the intercept will change but the slope will remain constant. Two empirical tests support this prediction but these are based on comparisons of geographic populations: more direct tests will come from artificial selection experiments. Finally, we discuss what maintains variation in trade-offs noting that at present little attention has been given to this question. We distinguish between phenotypic and genetic variation and suggest that the latter is most in need of explanation. We suggest that four factors deserving investigation are mutation-selection balance, antagonistic pleiotropy, correlational selection and spatio-temporal variation, but as in the other areas of research on trade-offs, empirical generalizations are impeded by lack of data. Although this lack is discouraging, we suggest that it provides a rich ground for further study and the integration of many disciplines, including the emerging field of genomics.     

A test of the hypothesis that correlational selection generates genetic correlations

Theory predicts that correlational selection on two traits will cause the major axis of the bivariate G matrix to orient itself in the same direction as the correlational selection gradient. Two testable predictions follow from this: for a given pair of traits, (1) the sign of correlational selection gradient should be the same as that of the genetic correlation, and (2) the correlational selection gradient should be positively correlated with the value of the genetic correlation. We test this hypothesis with a meta-analysis utilizing empirical estimates of correlational selection gradients and measures of the correlation between the two focal traits. Our results are consistent with both predictions and hence support the underlying hypothesis that correlational selection generates a genetic correlation between the two traits and hence orients the bivariate G matrix.     

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.     

Laboratory evolution of the migratory polymorphism in the sand cricket: combining physiology with quantitative genetics

Predicting evolutionary change is the central goal of evolutionary biology because it is the primary means by which we can test evolutionary hypotheses. In this article, we analyze the pattern of evolutionary change in a laboratory population of the wing-dimorphic sand cricket Gryllus firmus resulting from relaxation of selection favoring the migratory (long-winged) morph. Based on a well-characterized trade-off between fecundity and flight capability, we predict that evolution in the laboratory environment should result in a reduction in the proportion of long-winged morphs. We also predict increased fecundity and reduced functionality and weight of the major flight muscles in long-winged females but little change in short-winged (flightless) females. Based on quantitative genetic theory, we predict that the regression equation describing the trade-off between ovary weight and weight of the major flight muscles will show a change in its intercept but not in its slope. Comparisons across generations verify all of these predictions. Further, using values of genetic parameters estimated from previous studies, we show that a quantitative genetic simulation model can account for not only the qualitative changes but also the evolutionary trajectory. These results demonstrate the power of combining quantitative genetic and physiological approaches for understanding the evolution of complex traits.     

The evolution of trade-offs: testing predictions on response to selection and environmental variation

The concept of phenotypic trade-offs is a central element in evolutionary theory. In general, phenotypic models assume a fixed trade-off function, whereas quantitative genetic theory predicts that the trade-off function will change as a result of selection. For a linear trade-off function selection will readily change the intercept but will have to be relatively stronger to change the slope. We test these predictions by examining the trade-off between fecundity and flight capability, as measured by dorso-longitudinal muscle mass, in four different populations of the sand cricket, Gryllus firmus. Three populations were recently derived from the wild, and the fourth had been in the laboratory for 19 years. We hypothesized that the laboratory population had most likely undergone more and different selection from the three wild populations and therefore should differ from these in respect to both slope and intercept. Because of geographic variation in selection, we predicted a general difference in intercept among the four populations. We further tested the hypothesis that this intercept will be correlated with proportion macropterous and that this relationship will itself vary with environmental conditions experienced during both the nymphal and adult period. Observed variation in the phenotypic trade-off was consistent with the predictions of the quantitative genetic model. These results point to the importance of modeling trade-offs as dynamic rather than static relationships. We discuss how phenotypic models can incorporate such variation. The phenotypic trade-off between fecundity and dorso-longitudinal muscle mass is determined in part by variation in body size, illustrating the necessity of considering trade-offs to be multi factorial rather than simply bivariate relationships.     

Correlational selection leads to genetic integration of body size and an attractive plumage trait in dark-eyed juncos

When a trait's effect on fitness depends on its interaction with other traits, the resultant selection is correlational and may lead to the integration of functionally related traits. In relation to sexual selection, when an ornamental trait interacts with phenotypic quality to determine mating success, correlational sexual selection should generate genetic correlations between the ornament and quality, leading to the evolution of honest signals. Despite its potential importance in the evolution of signal honesty, correlational sexual selection has rarely been measured in natural populations. In the dark-eyed junco (Junco hyemalis), males with experimentally elevated values of a plumage trait (whiteness in the tail or "tail white") are more attractive to females and dominant in aggressive encounters over resources. We used restricted maximum-likelihood analysis of a long-term dataset to measure the heritability of tail white and two components of body size (wing length and tail length), as well as genetic correlations between pairs of these traits. We then used multiple regression to assess directional, quadratic, and correlational selection as they acted on tail white and body size via four components of lifetime fitness (juvenile and adult survival, mating success, and fecundity). We found a positive genetic correlation between tail white and body size (as measured by wing length), which indicates past correlational selection. Correlational selection, which was largely due to sexual selection on males, was also found to be currently acting on the same pair of traits. Larger males with whiter tails sired young with more females, most likely due to a combination of female choice, which favors males with whiter tails, and male-male competition, which favors both tail white and larger body size. To our knowledge, this is the first study to show both genetic correlations between sexually selected traits and currently acting correlational sexual selection, and we suggest that correlational sexual selection frequently may be an important mechanism for maintaining the honesty of sexual signals.     

When three traits make a line: evolution of phenotypic plasticity and genetic assimilation through linear reaction norms in stochastic environments

Genetic assimilation emerges from selection on phenotypic plasticity. Yet, commonly used quantitative genetics models of linear reaction norms considering intercept and slope as traits do not mimic the full process of genetic assimilation. We argue that intercept–slope reaction norm models are insufficient representations of genetic effects on linear reaction norms and that considering reaction norm intercept as a trait is unfortunate because the definition of this trait relates to a specific environmental value (zero) and confounds genetic effects on reaction norm elevation with genetic effects on environmental perception. Instead, we suggest a model with three traits representing genetic effects that, respectively, (i) are independent of the environment, (ii) alter the sensitivity of the phenotype to the environment and (iii) determine how the organism perceives the environment. The model predicts that, given sufficient additive genetic variation in environmental perception, the environmental value at which reaction norms tend to cross will respond rapidly to selection after an abrupt environmental change, and eventually becomes equal to the new mean environment. This readjustment of the zone of canalization becomes completed without changes in genetic correlations, genetic drift or imposing any fitness costs of maintaining plasticity. The asymptotic evolutionary outcome of this three‐trait linear reaction norm generally entails a lower degree of phenotypic plasticity than the two‐trait model, and maximum expected fitness does not occur at the mean trait values in the population.     

The evolution of trade-offs: effects of inbreeding on fecundity relationships in the cricket Gryllus firmus

The evolution of traits is modulated by their interrelationships with each other, particularly when those relationships result in a fitness trade-off. In this paper we explore the consequences of genetic architecture on functional relationships between traits. Specifically, we address the consequences of inbreeding on these relationships. We show that the linear regression between two traits will not be affected if there is no dominance genetic variance in either trait, whereas the intercept but not the slope of the regression will change if there is dominance genetic variance in one trait only. We test the latter hypothesis using fecundity relationships in the cricket Gryllus firmus. Data from pedigree analysis and an inbreeding experiment show that there is significant dominance genetic variance in fecundity, but not head width (an index of body size) or dorsal longitudinal muscle (DLM) mass. Fecundity increases with head width, but decreases with DLM mass. As predicted, the intercepts of the regressions of fecundity on these two morphological traits decrease with inbreeding, but there is little or no change in slope. Gryllus firmus is wing dimorphic, with the macropterous (LW) morph having a lower fecundity than the micropterous (SW) morph. We hypothesize that the difference in fecundity arises primarily because of a competition for resources in the LW females between DLM maintenance (i.e., mass) and egg production. As a consequence, we predict that the fecundity within each morph should decline linearly with the inbreeding coefficient at the same rate in both morphs. The result of this will be a change in the relative fitness of the two morphs, that of the SW morph increasing with inbreeding. This prediction is supported. These results indicate that trade-offs will evolve and such changes will affect evolutionary trajectories by altering the pattern of relationships among fitness components.     

Response of fluctuating and directional asymmetry to selection on wing shape in Drosophila melanogaster

We tested whether directional selection on an index-based wing character in Drosophila melanogaster affected developmental stability and patterns of directional asymmetry. We selected for both an increase (up selection) and a decrease (down selection) of the index value on the left wing and compared patterns of fluctuating and directional asymmetry in the selection index and other wing traits across selection lines. Changes in fluctuating asymmetry across selection lines were predominantly small, but we observed a tendency for fluctuating asymmetry to decrease in the up-selected lines in both replicates. Because changes in fluctuating asymmetry depended on the direction of selection, and were not related to changes in trait size, these results fail to support existing hypotheses linking directional selection and developmental stability. Selection also produced a pattern of directional asymmetry that was similar in all selected lines whatever the direction of selection. This result may be interpreted as a release of genetic variance in directional asymmetry under selection.     

Evolution of branched regulatory genetic pathways: directional selection on pleiotropic loci accelerates developmental system drift

Developmental systems are regulated by a web of interacting loci. One common and useful approach in studying the evolution of development is to focus on classes of interacting elements within these systems. Here, we use individual-based simulations to study the evolution of traits controlled by branched developmental pathways involving three loci, where one locus regulates two different traits. We examined the system under a variety of selective regimes. In the case where one branch was under stabilizing selection and the other under directional selection, we observed "developmental system drift": the trait under stabilizing selection showed little phenotypic change even though the loci underlying that trait showed considerable evolutionary divergence. This occurs because the pleiotropic locus responds to directional selection and compensatory mutants are then favored in the pathway under stabilizing selection. Though developmental system drift may be caused by other mechanisms, it seems likely that it is accelerated by the same underlying genetic mechanism as that producing the Dobzhansky-Muller incompatibilities that lead to speciation in both linear and branched pathways. We also discuss predictions of our model for developmental system drift and how different selective regimes affect probabilities of speciation in the branched pathway system.     

Evolution in a changing environment: a case study with great tit fledging mass

Heritable phenotypic traits under significant and consistent directional selection often fail to show the expected evolutionary response. A potential explanation for this contradiction is that because environmental conditions change constantly, environmental change can mask an evolutionary response to selection. We combined an "animal model" analysis with 36 years of data from a long-term study of great tits (Parus major) to explore selection on and evolution of a morphological trait: body mass at fledging. We found significant heritability of this trait, but despite consistent positive directional selection on both the phenotypic and the additive genetic component of body mass, the population mean phenotypic value declined rather than increased over time. However, the mean breeding value for body mass at fledging increased over time, presumably in response to selection. We show that the divergence between the response to selection observed at the levels of genotype and phenotype can be explained by a change in environmental conditions over time, that is, related both to increased spring temperature before breeding and elevated population density. Our results support the suggestion that measuring phenotypes may not always give a reliable impression of evolutionary trajectories and that understanding patterns of phenotypic evolution in nature requires an understanding of how the environment has itself changed.     

The evolution of trade-offs: geographic variation in call duration and flight ability in the sand cricket, Gryllus firmus

Quantitative genetic theory assumes that trade-offs are best represented by bivariate normal distributions. This theory predicts that selection will shift the trade-off function itself and not just move the mean trait values along a fixed trade-off line, as is generally assumed in optimality models. As a consequence, quantitative genetic theory predicts that the trade-off function will vary among populations in which at least one of the component traits itself varies. This prediction is tested using the trade-off between call duration and flight capability, as indexed by the mass of the dorsolateral flight muscles, in the macropterous morph of the sand cricket. We use four different populations of crickets that vary in the proportion of macropterous males (Lab = 33%, Florida = 29%, Bermuda = 72%, South Carolina = 80%). We find, as predicted, that there is significant variation in the intercept of the trade-off function but not the slope, supporting the hypothesis that trade-off functions are better represented as bivariate normal distributions rather than single lines. We also test the prediction from a quantitative genetical model of the evolution of wing dimorphism that the mean call duration of macropterous males will increase with the percentage of macropterous males in the population. This prediction is also supported. Finally, we estimate the probability of a macropterous male attracting a female, P, as a function of the relative time spent calling (P = time spent calling by macropterous male/(total time spent calling by both micropterous and macropterous male). We find that in the Lab and Florida populations the probability of a female selecting the macropterous male is equal to P, indicating that preference is due simply to relative call duration. But in the Bermuda and South Carolina populations the probability of a female selecting a macropterous male is less than P, indicating a preference for the micropterous male even after differences in call duration are accounted for.     

MULTIYEAR STUDY OF MULTIVARIATE LINEAR AND NONLINEAR PHENOTYPIC SELECTION ON FLORAL TRAITS OF HUMMINGBIRD-POLLINATED SILENE VIRGINICA

Pollination syndromes suggest that convergent evolution of floral traits and trait combinations reflects similar selection pressures. Accordingly, a pattern of selection on floral traits is expected to be consistent with increasing the attraction and pollen transfer of the important pollinator. We measured individual variation in six floral traits and yearly and lifetime total plant seed and fruit production of 758 plants across nine years of study in natural populations of Ruby-Throated Hummingbird-pollinated Silene virginica. The type, strength, and direction of selection gradients were observed by year, and for two cohorts selection was estimated through lifetime maternal fitness. Positive directional selection was detected on floral display height in all years of study and stigma exsertion in all years but one. Significant quadratic and correlational selection gradients were rare. However, a canonical analysis of the gamma matrix indicated nonlinear selection was common; if significant curvature was detected it was convex with one exception. Our analyses demonstrated selection favored trait combinations and the integration of floral features of attraction and pollen transfer efficiency that were consistent with the hummingbird pollination syndrome.     

Evolutionary quantitative genetics of nonlinear developmental systems

In quantitative genetics, the effects of developmental relationships among traits on microevolution are generally represented by the contribution of pleiotropy to additive genetic covariances. Pleiotropic additive genetic covariances arise only from the average effects of alleles on multiple traits, and therefore the evolutionary importance of nonlinearities in development is generally neglected in quantitative genetic views on evolution. However, nonlinearities in relationships among traits at the level of whole organisms are undeniably important to biology in general, and therefore critical to understanding evolution. I outline a system for characterizing key quantitative parameters in nonlinear developmental systems, which yields expressions for quantities such as trait means and phenotypic and genetic covariance matrices. I then develop a system for quantitative prediction of evolution in nonlinear developmental systems. I apply the system to generating a new hypothesis for why direct stabilizing selection is rarely observed. Other uses will include separation of purely correlative from direct and indirect causal effects in studying mechanisms of selection, generation of predictions of medium‐term evolutionary trajectories rather than immediate predictions of evolutionary change over single generation time‐steps, and the development of efficient and biologically motivated models for separating additive from epistatic genetic variances and covariances.     

CORRELATIONAL SELECTION FOR COLOR PATTERN AND ANTIPREDATOR BEHAVIOR IN THE GARTER SNAKE THAMNOPHIS ORDINOIDES

Correlational selection favors combinations of traits and is a key element of many models of phenotypic and genetic evolution. Multiple regression techniques for measuring selection allow for the direct estimation of correlational selection gradients, yet few studies in natural populations have investigated this process. Color patterns and antipredator behaviors of snakes are thought to function interactively in predator escape and therefore may be subject to correlational selection. To investigate this hypothesis, I studied the survivorship of juvenile garter snakes, Thamnophis ordinoides, as a function of a suite of escape behaviors and color pattern. The only natural selection detected favored opposite combinations of stripedness of the color pattern and the tendency to perform during escape evasive behaviors called reversals. This selection presumably results from optical illusions created by moving patterns and their effects on visually foraging predators. Analysis of the bivariate selection surface shows that pure correlational selection can be thought of as a series of linear selection functions on one trait whose slopes depend on the value of the second trait. Alternatively, viewing the selection surface along its major axes reveals stabilizing and disruptive components of correlational selection. It is further shown that correlational selection alone can promote genetic variance and covariance within a generation. This phenomenon may be partially responsible for the extreme variation in color pattern and the genetic covariance between color pattern and behavior observed in natural populations of T. ordinoides.     

Environmental heterogeneity,multivariate sexual selection and genetic constraints on cuticular hydrocarbons in Drosophila simulans

Sexual selection is responsible for the evolution of many elaborate traits, but sexual trait evolution could be influenced by opposing natural selection as well as genetic constraints. As such, the evolution of sexual traits could depend heavily on the environment if trait expression and attractiveness vary between environments. Here, male Drosophila simulans were reared across a range of diets and temperatures, and we examined differences between these environments in terms of (i) the expression of male cuticular hydrocarbons (CHCs) and (ii) which male CHC profiles were most attractive to females. Temperature had a strong effect on male CHC expression, whereas the effect of diet was weaker. Male CHCs were subject to complex patterns of directional, quadratic and correlational sexual selection, and we found differences between environments in the combination of male CHCs that were most attractive to females, with clearer differences between diets than between temperatures. We also show that genetic covariance between environments is likely to cause a constraint on independent CHC evolution between environments. Our results demonstrate that even across the narrow range of environmental variation studied here, predicting the outcome of sexual selection can be extremely complicated, suggesting that studies ignoring multiple traits or environments may provide an over‐simplified view of the evolution of sexual traits.     

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.     

Hormone-mediated suites as adaptations and evolutionary constraints

Hormones mediate the expression of suites of correlated traits and hence may act both to facilitate and constrain adaptive evolution. Selection on one trait within a hormone-mediated suite may, for example, lead to a change in the strength of the hormone signal, causing either beneficial or detrimental changes in correlated traits. Theory and empirical methods for studying correlated trait evolution have been developed by the field of evolutionary quantitative genetics, and here we suggest that their application to the study of hormone-mediated suites may prove fruitful. We present hypotheses for how selection shapes the evolution of hormone-mediated suites and argue that correlational selection, which arises when traits interact in their effects on fitness, may act to alter or conserve the composition of hormone-mediated suites. Next, we advocate using quantitative genetic methods to assess natural covariation among hormone-mediated traits and to measure the strength of natural selection acting on them. Finally, we present illustrative examples from our own work on the evolution of testosterone-mediated suites in male and female dark-eyed juncos. We conclude that future work on hormone-mediated suites, if motivated by quantitative genetic theory, may provide important insights into their dual roles as adaptations and evolutionary constraints.     

Predicted accuracy of and response to genomic selection for new traits in dairy cattle

Genomic selection relaxes the requirement of traditional selection tools to have phenotypic measurements on close relatives of all selection candidates. This opens up possibilities to select for traits that are difficult or expensive to measure. The objectives of this paper were to predict accuracy of and response to genomic selection for a new trait, considering that only a cow reference population of moderate size was available for the new trait, and that selection simultaneously targeted an index and this new trait. Accuracy for and response to selection were deterministically evaluated for three different breeding goals. Single trait selection for the new trait based only on a limited cow reference population of up to 10 000 cows, showed that maximum genetic responses of 0.20 and 0.28 genetic standard deviation (s.d.) per year can be achieved for traits with a heritability of 0.05 and 0.30, respectively. Adding information from the index based on a reference population of 5000 bulls, and assuming a genetic correlation of 0.5, increased genetic response for both heritability levels by up to 0.14 genetic s.d. per year. The scenario with simultaneous selection for the new trait and the index, yielded a substantially lower response for the new trait, especially when the genetic correlation with the index was negative. Despite the lower response for the index, whenever the new trait had considerable economic value, including the cow reference population considerably improved the genetic response for the new trait. For scenarios with a zero or negative genetic correlation with the index and equal economic value for the index and the new trait, a reference population of 2000 cows increased genetic response for the new trait with at least 0.10 and 0.20 genetic s.d. per year, for heritability levels of 0.05 and 0.30, respectively. We conclude that for new traits with a very small or positive genetic correlation with the index, and a high positive economic value, considerable genetic response can already be achieved based on a cow reference population with only 2000 records, even when the reliability of individual genomic breeding values is much lower than currently accepted in dairy cattle breeding programs. New traits may generally have a negative genetic correlation with the index and a small positive economic value. For such new traits, cow reference populations of at least 10 000 cows may be required to achieve acceptable levels of genetic response for the new trait and for the whole breeding goal.