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.     

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.     

PLASTICITY, CANALIZATION, AND DEVELOPMENTAL STABILITY OF THE DROSOPHILA WING: JOINT EFFECTS OF MUTATIONS AND DEVELOPMENTAL TEMPERATURE

The phenotypic effects of genetic and environmental manipulations have been rarely investigated simultaneously. In addition to phenotypic plasticity, their effect on the amount and directions of genetic and phenotypic variation is of particular evolutionary importance because these constitute the material for natural selection. Here, we used heterozygous insertional mutations of 16 genes involved in the formation of the Drosophila wing. The flies were raised at two developmental temperatures (18°C and 28°C). Landmark-based geometric morphometrics was used to analyze the variation of the wing size and shape at different hierarchical levels: among genotypes and temperatures; among individuals within group; and fluctuating asymmetry (FA). Our results show that (1) the phenotypic effects of the mutations depend on temperature; (2) reciprocally, most mutations affect wing plasticity; (3) both temperature and mutations modify the levels of FA and of among individuals variation within lines. Remarkably, the patterns of shape FA seem unaffected by temperature whereas those associated with individual variation are systematically altered. By modifying the direction of available phenotypic variation, temperature might thus directly affect the potential for further evolution. It suggests as well that the developmental processes responsible for developmental stability and environmental canalization might be partially distinct.     

ON THE LOW HERITABILITY OF LIFE-HISTORY TRAITS

Life-history traits such as longevity and fecundity often show low heritability. This is usually interpreted in terms of Fisher's fundamental theorem to mean that populations are near evolutionary equilibrium and genetic variance in total fitness is low. We develop the causal relationship between metric traits and life-history traits to show that a life-history trait is expected to have a low heritability whether or not the population is at equilibrium. This is because it is subject to all the environmental variation in the metric traits that affect it plus additional environmental variation. There is no simple prediction regarding levels of additive genetic variance in life-history traits, which may be high at equilibrium. Several other patterns in the inheritance of life-history traits are readily predicted from the causal model. These include the strength of genetic correlations between life-history traits, levels of nonadditive genetic variance, and the inevitability of genotype-environment interaction.     

THE EVOLUTION OF CANALIZATION AND THE BREAKING OF VON BAER'S LAWS: MODELING THE EVOLUTION OF DEVELOPMENT WITH EPISTASIS

Evolution can change the developmental processes underlying a character without changing the average expression of the character itself. This sort of change must occur in both the evolution of canalization, in which a character becomes increasingly buffered against genetic or developmental variation, and in the phenomenon of closely related species that show similar adult phenotypes but different underlying developmental patterns. To study such phenomena, I develop a model that follows evolution on a surface representing adult phenotype as a function of underlying developmental characters. A contour on such a “phenotype landscape” is a set of states of developmental characters that produce the same adult phenotype. Epistasis induces curvature of this surface, and degree of canalization is represented by the slope along a contour. I first discuss the geometric properties of phenotype landscapes, relating epistasis to canalization. I then impose a fitness function on the phenotype and model evolution of developmental characters as a function of the fitness function and the local geometry of the surface. This model shows how canalization evolves as a population approaches an optimum phenotype. It further shows that under some circumstances, “decanalization” can occur, in which the expression of adult phenotype becomes increasingly sensitive to developmental variation. This process can cause very similar populations to diverge from one another developmentally even when their adult phenotypes experience identical selection regimes.     

HYBRID FITNESS IN THE LOUISIANA IRISES: ANALYSIS OF PARENTAL AND F1 PERFORMANCE

The assumption of hybrid inferiority is central to the two models most widely applied to the prediction of hybrid zone evolution. Both the tension zone and mosaic models assume that natural selection acts against hybrids regardless of the environment in which they occur. To test this assumption, we investigated components of fitness in Iris fulva, I. hexagona and their reciprocal F₁ hybrids under greenhouse conditions. The four cross types were compared on the basis of seed germination, vegetative and clonal growth, and sexual reproduction. In all cases, the hybrids performed as well as, or significantly better than, both of their parents. These results suggest that F₁ hybrids between I. fulva and I. hexagona are at least as fit as their parents. The results of this study are therefore inconsistent with the assumptions of both the tension zone and mosaic models of hybrid zone evolution.     

SENSITIVITY OF THE DISTRIBUTION OF MUTATIONAL FITNESS EFFECTS TO ENVIRONMENT,GENETIC BACKGROUND,AND ADAPTEDNESS: A CASE STUDY WITH DROSOPHILA

Heterogeneity in the fitness effects of individual mutations has been found across different environmental and genetic contexts. Going beyond effects on individual mutations, how is the distribution of selective effects, f(s), altered by changes in genetic and environmental context? In this study, we examined changes in the major features of f(s) by estimating viability selection on 36 individual mutations in Drosophila melanogaster across two different environments in two different genetic backgrounds that were either adapted or nonadapted to the two test environments. Both environment and genetic background affected selection on individual mutations. However, the overall distribution f(s) appeared robust to changes in genetic background but both the mean, E(s), and the variance, V(s) were dependent on the environment. Between these two properties, V(s) was more sensitive to environmental change. Contrary to predictions of fitness landscape theory, the match between genetic background and assay environment (i.e., adaptedness) had little effect on f(s).     

THE EVOLUTION OF FITNESS

In every generation, the mean fitness of populations increases because of natural selection and decreases because of mutations and changes in the environment. The magnitudes of these effects can be measured in two ways: either directly, by comparing the fitnesses of selected and unselected populations, or indirectly, by measuring the additive variance of fitness and making use of the fundamental theorem of natural selection. The available data suggest that the amount by which natural selection increases mean fitness each generation (or degradation decreases mean fitness) will usually be between 0.1% and 30%; more tentatively, it is suggested that values will typically fall between 1% and 10%. These values can be used to set an upper limit of 5%–10% on the genetic advantage of mate choice.     

MEASUREMENTS OF NATURAL SELECTION ON FLORAL TRAITS IN WILD RADISH (RAPHANUS RAPHANISTRUM). I. SELECTION THROUGH LIFETIME FEMALE FITNESS

Although the role of natural selection in the evolution of floral traits has been of great interest to biologists since Darwin, studies of selection on floral traits through differences in lifetime fitness have been rare. We measured selection acting on flower number, flower size, stigma exsertion, and ovule number per flower using field data on lifetime female fitness (seed production) in wild radish, Raphanus raphanistrum. The patterns of selection were reasonably consistent across three field seasons, with strong directional selection for increased flower production in all three years, weaker selection for increased ovule number per flower in two years, and selection for increased flower size in one year. The causes of the selection were investigated using path analysis combined with multiplicative fitness components. Increased flower production increased fruit production directly, and increased numbers of ovules per flower increased the number of seeds per fruit in all three years; pollinator visitation did not influence either of these fitness components. Increased flower size was associated with increases in both the number of fruit and the number of seeds per fruit in one year, with the latter relationship being stronger. Total lifetime seed production was affected more strongly by differences in fruit production than by differences in either the number of seeds per fruit or the proportion of fertilized seeds that were viable, but all three fitness components were positively correlated with total seed production.     

RAPID LABORATORY EVOLUTION OF ADULT LIFE-HISTORY TRAITS IN DROSOPHILA MELANOGASTER IN RESPONSE TO TEMPERATURE

Three replicate lines of Drosophila melanogaster were cultured at each of two temperatures (16.5°C and 25°C) in population cages for 4 yr. The lifespans of both sexes and the fecundity and fertility of the females were then measured at both experimental temperatures. The characters showed evidence of adaptation; flies of both sexes from each selection regime showed higher longevity, and females showed higher fecundity and fertility, than flies from the other selection regime when they were tested at the experimental temperature at which they had evolved. Calculation of intrinsic rates of increase under different assumptions about the rate of population increase showed that the difference between the lines from the two selection regimes became less the higher the rate of population increase, because the lines were more similar in early adulthood than they were later. Despite the increased adaptation of the low-temperature lines to the low temperature, like the high temperature lines they produced progeny at a higher rate at the higher temperature. The lines may have independently evolved adaptations to their respective thermal regimes during the experiment, or there may have been a trade-off between adaptation to the two temperatures, or mutation pressure may have lowered adaptation to the temperature that the flies no longer encountered.     

A POPULATION GENETIC THEORY OF CANALIZATION

Canalization is the suppression of phenotypic variation. Depending on the causes of phenotypic variation, one speaks either of genetic or environmental canalization. Genetic canalization describes insensitivity of a character to mutations, and the insensitivity to environmental factors is called environmental canalization. Genetic canalization is of interest because it influences the availability of heritable phenotypic variation to natural selection, and is thus potentially important in determining the pattern of phenotypic evolution. In this paper a number of population genetic models are considered of a quantitative character under stabilizing selection. The main purpose of this study is to define the population genetic conditions and constraints for the evolution of canalization. Environmental canalization is modeled as genotype specific environmental variance. It is shown that stabilizing selection favors genes that decrease environmental variance of quantitative characters. However, the theoretical limit of zero environmental variance has never been observed. Of the many ways to explain this fact, two are addressed by our model. It is shown that a “canalization limit” is reached if canalizing effects of mutations are correlated with direct effects on the same character. This canalization limit is predicted to be independent of the strength of stabilizing selection, which is inconsistent with recent experimental data (Sterns et al. 1995). The second model assumes that the canalizing genes have deleterious pleiotropic effects. If these deleterious effects are of the same magnitude as all the other mutations affecting fitness very strong stabilizing selection is required to allow the evolution of environmental canalization. Genetic canalization is modeled as an influence on the average effect of mutations at a locus of other genes. It is found that the selection for genetic canalization critically depends on the amount of genetic variation present in the population. The more genetic variation, the stronger the selection for canalizing effects. All factors that increase genetic variation favor the evolution of genetic canalization (large population size, high mutation rate, large number of genes). If genetic variation is maintained by mutation-selection balance, strong stabilizing selection can inhibit the evolution of genetic canalization. Strong stabilizing selection eliminates genetic variation to a level where selection for canalization does not work anymore. It is predicted that the most important characters (in terms of fitness) are not necessarily the most canalized ones, if they are under very strong stabilizing selection (k > 0.2V_e). The rate of decrease of mutational variance V_m is found to be less than 10% of the initial V_m. From this result it is concluded that characters with typical mutational variances of about 10^–3 V_e are in a metastable state where further evolution of genetic canalization is too slow to be of importance at a microevolutionary time scale. The implications for the explanation of macroevolutionary patterns are discussed.     

MEASUREMENTS OF NATURAL SELECTION ON FLORAL TRAITS IN WILD RADISH (RAPHANUS RAPHANISTRUM). II. SELECTION THROUGH LIFETIME MALE AND TOTAL FITNESS

It has often been suggested that selection on floral traits in hermaphroditic plants should occur primarily through differences in male fitness. However, measurements of selection on floral traits through differences in lifetime male fitness have been lacking. We measured selection on a variety of wild radish floral traits using lifetime male fitness measures derived from genetic paternity analysis. These male fitness estimates were then combined with estimates of lifetime female fitness of the same plants to produce measurements of selection based on lifetime total fitness. Contrary to the prediction above, there was no strong evidence for selection on floral morphology through male fitness differences in any of the three years of the study, but there was strong selection for increased flower size through female fitness differences in one year. The main determinant of both male and female fitness in all years was flower number; this lead to moderately positive correlations between male and female fitness in all three years.     

LABORATORY EVOLUTION OF LIFE-HISTORY TRAITS IN THE BEAN WEEVIL (ACANTHOSCELIDES OBTECTUS): THE EFFECTS OF DENSITY-DEPENDENT AND AGE-SPECIFIC SELECTION

Four types of laboratory populations of the bean weevil (Acanthoscelides obtectus) have been developed to study the effects of density-dependent and age-specific selection. These populations have been selected at high (K) and low larval densities (r) as well as for reproduction early (Y) and late (O) in life. The results presented here suggest that the r- and K-populations (density-dependent selection regimes) have differentiated from each other with respect to the following life-history traits: egg-to-adult viability at high larval density (K > r), preadult developmental time (r > K), body weight (r > K), late fecundity (K > r), total realized fecundity (r > K), and longevity of males (r > K). It was also found that the following traits responded in statistically significant manner in populations subjected to different age-specific selection regimes: egg-to-adult viability (O > Y), body weight (O > Y), early fecundity (Y > O), late fecundity (O > Y), and longevity of females and males (O > Y). Although several life-history traits (viability, body weight, late fecundity) responded in similar manner to both density-dependent and age-specific selection regimes, it appears that underlying genetic and physiological mechanisms responsible for differentiation of the r/K and Y/O populations are different. We have also tested quantitative genetic basis of the bean weevil life-history traits in the populations experiencing density-dependent and age-specific selection. Among the traits traded-off within age-specific selection regimes, only early fecundity showed directional dominance, whereas late fecundity and longevity data indicated additive inheritance. In contrast to age-specific selecton regimes, three life-history traits (developmental time, body size, total fecundity) in the density-sependent regimes exhibited significant dominance effects. Lastly, we have tested the congruence between short-term and long-term effects of larval densities. The comparisons of the outcomes of the r/K selection regimes and those obtained from the low- and high-larval densities revealed that there is no congruence between the selection results and phenotypic plasticity for the analyzed life-history traits in the bean weevil.     

The differential genetic and environmental canalization of fitness components in Drosophila melanogaster

Canalization describes the process by which phenotypic variation is reduced by developmental mechanisms. A trait can be canalized against environmental or genetic perturbations. Stabilizing selelction should favor improved canalization, and the degree of a trait's canalization should be positively correlated with its impact on fitness. Here we report, for Drosophila melanogaster, measurements of environmental canalization for five fitness components. We compare them with measurements of genetic canalization, and we discuss the impact of inbreeding on both. In three experiments we measured the variation of fitness components within lines nested within temperature, treatment, and experiment. Lines differed in the position of a P element insert or in genetic background. Within lines flies were genetically nearly identical. We designated trait variation within lines as environmental canalization. The canalization of the traits increased with their impact on fitness, and the pattern was similar to that found for the canalization of fitness components against genetic differences, measured as the variation among lines nested within temperature, treatment, and experiment. This suggests that developmental mechanisms buffer the phenotype against both genetic and environmental disturbance. The results also suggest, less strongly, that inbreeding weakens canalization.     

SELECTION AND EVOLUTION OF CAUSALLY COVARYING TRAITS

When traits cause variation in fitness, the distribution of phenotype, weighted by fitness, necessarily changes. The degree to which traits cause fitness variation is therefore of central importance to evolutionary biology. Multivariate selection gradients are the main quantity used to describe components of trait‐fitness covariation, but they quantify the direct effects of traits on (relative) fitness, which are not necessarily the total effects of traits on fitness. Despite considerable use in evolutionary ecology, path analytic characterizations of the total effects of traits on fitness have not been formally incorporated into quantitative genetic theory. By formally defining “extended” selection gradients, which are the total effects of traits on fitness, as opposed to the existing definition of selection gradients, a more intuitive scheme for characterizing selection is obtained. Extended selection gradients are distinct quantities, differing from the standard definition of selection gradients not only in the statistical means by which they may be assessed and the assumptions required for their estimation from observational data, but also in their fundamental biological meaning. Like direct selection gradients, extended selection gradients can be combined with genetic inference of multivariate phenotypic variation to provide quantitative prediction of microevolutionary trajectories.