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.     

SELECTION, PREDICTION AND RESPONSE

1. The biometric approach to selection experiments has been outlined, and found to be rather deficient because it is based on excessively restrictive models which cannot take into account the complex architectures of quantitative traits as are being revealed today. 2. The nature of polygenes is discussed in detail from the theoretical point of view. In out breeding species, some form of the balanced polygenic complex is likely, showing polymorphism for the constituent genes. Although polymorphism is implicit in the argument, definitive evidence for poiymorphisms has only just appeared. 3. There is no evidence that polygenes differ from any other gene. 4. Several artificial selection experiments are described, in particular in Drosophila. By means of appropriate breeding techniques after obtaining responses to selection, genetic activity controlling quantitative traits can be located to chromosomes, and even specific loci found. Such few studies as have been carried out reveal, in general, the types of genetic architecture predicted on theoretical grounds. 5. Selection for behavioural traits is considered briefly and it appears that no new principles are needed, except that careful environmental control and objective measurement present problems. 6. The results of selection for quantitative traits in micro-organisms reveal similarities to results in higher organisms in the few cases where definitive work has been carried out. 7. Work on the simulation of models by computers has not greatly advanced selection experiment theory, mainly because, with few exceptions, linkage has been ignored. 8. The existing theory on which selection experiments are based is inadequate for several reasons. It cannot predict the rate of response to selection nor the ultimate limits to selection, the nature of correlated responses to selection, nor the nature of gene segregation underlying the observed variability. 9. Strains set up from single inseminated founder females from the same population of Drosophila have been shown to differ genetically for several quantitative traits. Therefore the base population is polymorphic for genes controlling these traits. This was exploited by carrying out directional selection on lines derived from those strains showing a high incidence of scutellar chaetae. This led to far more rapid responses to selection than lines derived from strains where the incidence of scutellar chaetae was lower. 10. Ultimately, one can envisage the selection experiment as it is known today being partly replaced by the manipulation of located genes controlling quantitative traits into certain combinations.     

RESPONSE TO SELECTION IN PARTIALLY SELF-FERTILIZING POPULATIONS. II. SELECTION ON MULTIPLE TRAITS

The structured linear model (SLM) is generalized to treat selection on multiple, correlated characters. Four different causes of phenotypic correlations are distinguished by the SLM: environmental covariance, identity disequilibrium, pleiotropy, and linkage disequilibrium. Each is characterized by distinct variables because they have different implications for character evolution. Correlations due to identity disequilibrium and linkage disequilibrium depend on both the mating system and the selection regime. As a consequence, they will evolve rapidly under selection. Correlations due to pleiotropy or environmental factors will evolve more slowly and are characterized by parameters that can be estimated from comparisons among relatives. These parameters include several novel “inbreeding covariance components” that emerge from the interaction of inbreeding and genetic dominance. Although data are limited, current estimates suggest that the expression of these components may substantially alter the pattern of multitrait evolution in self-fertilizing populations.     

RELATIVE ROLE OF GENETIC DETERMINATION AND PLASTIC RESPONSE DURING ONTOGENY FOR SHELL-SHAPE TRAITS SUBJECTED TO DIVERSIFYING SELECTION

We studied the relative role of genetic determination versus plastic response for traits involved in ecological adaptation of two ecotypes of Littorina saxatilis living at different shore levels. To investigate the magnitude of the plastic response across ontogeny, we compared morphological data from individuals grown in the laboratory and taken from the wild at three developmental stages: shelled embryos, juveniles, and adults. The results indicate that most shell shape variation (72–99%) in adaptive traits (globosity and aperture of the shell) is explained by the ecotype irrespective of the growth environment, suggesting that direct genetic determination is the main factor responsible for the process of adaptation in the wild. There was a tendency for the contribution of plasticity to increase over ontogeny but, in general, the direction of the plastic response did not suggest that this was adaptive.     

THE RESPONSE TO DIFFERING SELECTION ON PLANT PHYSIOLOGICAL TRAITS: EVIDENCE FOR LOCAL ADAPTATION

Understanding adaptive evolution to differing environments requires studies of genetic variances, of natural selection, and of the genetic differentiation between populations. Plant physiological traits such as leaf size and water-use efficiency (the ratio of carbon gained per water lost) have been suggested by physiological plant ecologists to be important in local adaptation to environments differing in water availability. In this study, I raised families of Cakile edentula var lacustris derived from a wet-site population and a dry-site population in a common greenhouse environment to determine the degree of genetic differentiation between the two populations and the genetic architecture of the traits. The dry-site population had significantly smaller leaf size and significantly greater water-use efficiency than the wet-site population. I used a retrospective selection analysis to compare long-term selection inferred from these results to measures of phenotypic selection from a field experiment. Both direct measures in the field and the retrospective selection gradients were consistent with the hypothesis that greater water-use efficiency and smaller leaves were adaptive in drier environments. Though the correlation between population means for water-use efficiency and leaf size was negative, the genetic correlation within populations between water-use efficiency and leaf size was positive and thus would be expected to constrain the evolutionary response to 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.     

THE ACTION OF STABILIZING SELECTION,MUTATION, AND DRIFT ON EPISTATIC QUANTITATIVE TRAITS

For a quantitative trait under stabilizing selection, the effect of epistasis on its genetic architecture and on the changes of genetic variance caused by bottlenecking were investigated using theory and simulation. Assuming empirical estimates of the rate and effects of mutations and the intensity of selection, we assessed the impact of two‐locus epistasis (synergistic/antagonistic) among linked or unlinked loci on the distribution of effects and frequencies of segregating loci in populations at the mutation‐selection‐drift balance. Strong pervasive epistasis did not modify substantially the genetic properties of the trait and, therefore, the most likely explanation for the low amount of variation usually accounted by the loci detected in genome‐wide association analyses is that many causal loci will pass undetected. We investigated the impact of epistasis on the changes in genetic variance components when large populations were subjected to successive bottlenecks of different sizes, considering the action of genetic drift, operating singly (D), or jointly with mutation (MD) and selection (MSD). An initial increase of the different components of the genetic variance, as well as a dramatic acceleration of the between‐line divergence, were always associated with synergistic epistasis but were strongly constrained by selection.     

EVOLUTION OF DIVERGENT FEMALE MATING PREFERENCE IN RESPONSE TO EXPERIMENTAL SEXUAL SELECTION

Sexual selection is predicted to drive the coevolution of mating signals and preferences (mating traits) within populations, and could play a role in speciation if sexual isolation arises due to mating trait divergence between populations. However, few studies have demonstrated that differences in mating traits between populations result from sexual selection alone. Experimental evolution is a promising approach to directly examine the action of sexual selection on mating trait divergence among populations. We manipulated the opportunity for sexual selection (low vs. high) in populations of Drosophila pseudoobscura. Previous studies on these experimental populations have shown that sexual selection manipulation resulted in the divergence between sexual selection treatments of several courtship song parameters, including interpulse interval (IPI) which markedly influences male mating success. Here, we measure female preference for IPI using a playback design to test for preference divergence between the sexual selection treatments after 130 generations of experimental sexual selection. The results suggest that female preference has coevolved with male signal, in opposite directions between the sexual selection treatments, providing direct evidence of the ability of sexual selection to drive the divergent coevolution of mating traits between populations. We discuss the implications in the context sexual selection and speciation.     

PHAGE-MEDIATED SELECTION AND THE EVOLUTION AND MAINTENANCE OF RESTRICTION-MODIFICATION

Restriction-modification (R-M) was discovered because it provides bacteria with immunity to phage infection. But, is phage-mediated selection the sole mechanism responsible for the evolution and maintenance of these ubiquitous and multiply evolved systems? In an effort to answer this question, we have performed experiments with laboratory populations of E. coli and phage and computer simulations. We consider two ecological situations whereby phage-mediated selection could favor R-M immunity; i) when bacteria with a novel R-M system invade communities of phage-sensitive bacteria in which there are one or more species of phage, and ii) when bacteria colonize bacterial-free habitats in which phage are present. The results of our experiments indicate that in established communities of bacteria and phage, the advantage R-M provides an invading population of bacteria is ephemeral. Within short order, mutants resistant (refractory) to the phage evolve in the dominant population and subsequently in the invading population. The outcome of competition then depends on the relative fitness of the resistant states of these bacterial clones, rather than R-M. As a consequence of sequential selection for independent mutants, this rapid evolution of resistance occurs even when two and three species of phage are present. While in our experiments resistance also evolved when bacteria colonized new habitats in which phage were present, a novel R-M system greatly augmented the likelihood of their becoming established. We interpret the results of this study as support for the hypothesis that the latter, colonization selection, may play an important role in the evolution and maintenance of restriction-modification. However, we also see these results and other observations we discuss as questioning whether protection against phage is the unique biological role of restriction-modification.     

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.     

QUANTITATIVE GENETIC MODELS FOR DEVELOPMENT,EPIGENETIC SELECTION,AND PHENOTYPIC EVOLUTION

Herein we describe a general multivariate quantitative genetic model that incorporates two potentially important developmental phenomena, maternal effects and epigenetic effects. Maternal and epigenetic effects are defined as partial regression coefficients and phenotypic variances are derived in terms of age-specific genetic and environmental variances. As a starting point, the traditional quantitative genetic model of additive gene effects and random environmental effects is cast in a developmental time framework. From this framework, we first extend a maternal effects model to include multiple developmental ages for the occurrence of maternal effects. An example of maternal effects occurring at multiple developmental ages is prenatal and postnatal maternal effects in mammals. Subsequently, a model of intrinsic and epigenetic effects in the absence of maternal effects is described. It is shown that genetic correlations can arise through epigenetic effects, and in the absence of other developmental effects, epigenetic effects are in general confounded with age-specific intrinsic genetic effects. Finally, the two effects are incorporated into the basic quantitative genetic model. For this more biologically realistic model combining maternal and epigenetic effects, it is shown that the phenotypic regressions of offspring on mother and offspring on father can be used in some cases to estimate simultaneously maternal effects and epigenetic effects.     

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.     

CORRELATED EVOLUTION OF SEXUAL SYSTEM AND LIFE-HISTORY TRAITS IN MOSSES

In mosses, separate and combined sexes are evolutionarily labile, yet factors selecting for this variation are unknown. In this study, we investigate phylogenetic correlations between sexual system and five life-history traits (asexual reproduction, chromosome number, gametophore length, spore size, and seta length). We assigned states to species on a large-scale phylogeny of mosses and used maximum likelihood analyses to test for the correlations and investigate the sequence of trait acquisition. Mosses in lineages with separate sexes were significantly more likely to be large, whereas those in lineages with combined sexes had higher chromosome numbers. Moreover, evolutionary transitions to separate sexes were more likely to occur in lineages with small spores. There was no support for a correlation between asexual reproduction and separate sexes. These results suggest that sexual system evolution is influenced by traits affecting mate availability and the dispersal of gametes and spores, and provides evidence for the existence of syndromes of life-history traits in mosses.     

SOCIAL SELECTION AND THE EVOLUTION OF ANIMAL SIGNALS

Social selection is presented here as a parallel theory to sexual selection and is defined as a selective force that occurs when individuals change their own social behaviors, responding to signals sent by conspecifics in a way to influence the other individuals' fitness. I analyze the joint evolution of a social signal and behavioral responsiveness to the signal by a quantitative-genetic model. The equilibria of average phenotypes maintained by a balance of social selection and natural selection and their stability are examined for two alternative assumptions on behavioral responsiveness, neutral and adaptive. When behavioral responsiveness is neutral on fitness, a rapid evolution by runaway selection occurs only with enough genetic covariance between the signal and responsiveness. The condition for rapid evolution also depends on natural selection and the number of interacting individuals. When signals convey some information on signalers (e.g., fighting ability), behavioral responsiveness is adaptive such that a receiver's fitness is also influenced by the signal. Here there is a single point of equilibrium. The equilibrium point and its stability do not depend on the genetic correlation. The condition needed for evolution is that the signal is beneficial for receivers, which results from reliability of the signal. Frequency-dependent selection on responsiveness has almost no influence on the equilibrium and the rate of evolution.     

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.     

SEX DIFFERENCES, SEXUAL SELECTION, AND AGEING: AN EXPERIMENTAL EVOLUTION APPROACH

Life-history (LH) theory predicts that selection will optimize the trade-off between reproduction and somatic maintenance. Reproductive ageing and finite life span are direct consequences of such optimization. Sexual selection and conflict profoundly affect the reproductive strategies of the sexes and thus can play an important role in the evolution of life span and ageing. In theory, sexual selection can favor the evolution of either faster or slower ageing, but the evidence is equivocal. We used a novel selection experiment to investigate the potential of sexual selection to influence the adaptive evolution of age-specific LH traits. We selected replicate populations of the seed beetle Callosobruchus maculatus for age at reproduction ("Young" and "Old") either with or without sexual selection. We found that LH selection resulted in the evolution of age-specific reproduction and mortality but these changes were largely unaffected by sexual selection. Sexual selection depressed net reproductive performance and failed to promote adaptation. Nonetheless, the evolution of several traits differed between males and females. These data challenge the importance of current sexual selection in promoting rapid adaptation to environmental change but support the hypothesis that sex differences in LH—a historical signature of sexual selection—are key in shaping trait responses to novel selection.