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.     

VARIATION IN GENETIC ARCHITECTURE OF CALLING SONG AMONG POPULATIONS OF ALLONEMOBIUS SOCIUS,A. FASCIATUS,AND A HYBRID POPULATION: DRIFT OR SELECTION?

Predictions using quantitative genetic models generally assume that the variance-covariance matrices remain constant over time. This assumption is based on the supposition that selection is generally weak and hence variation lost through selection can be replaced by new mutations. Whether this is generally true can only be ascertained from empirical studies. Ideally for such a study we should be able to make a prediction concerning the relative strength of selection versus genetic drift. If the latter force is prevalent then the variance-covariances matrices should be proportional to each other. Previous studies have indicated that females in the two sibling cricket species Allonemobius socius and A. fasciatus do not discriminate between males of the two species by their calling song. Therefore, differences between the calling song of the two males most likely result from drift rather than sexual selection. We test this hypothesis by comparing the genetic architecture of calling song of three populations of A. fasciatus with two populations of A. socius. We found no differences among populations within species, but significant differences in the G (genetic) and P (phenotypic) matrices between species, with the matrices being proportional as predicted under the hypothesis of genetic drift. Because of the proportional change in the (co)variances no differences between species are evident in the heritabilities or genetic correlations. Comparison of the two species with a hybrid population from a zone of overlap showed highly significant nonproportional variation in genetic architecture. This variation is consistent with a general mixture of two separate genomes or selection. Qualitative conclusions reached using the phenotypic matrices are the same as those reached using the genetic matrices supporting the hypothesis that the former may be used as surrogate measures of the latter.     

EVOLUTION IN FLUCTUATING ENVIRONMENTS: DECOMPOSING SELECTION INTO ADDITIVE COMPONENTS OF THE ROBERTSON–PRICE EQUATION

We analyze the stochastic components of the Robertson–Price equation for the evolution of quantitative characters that enables decomposition of the selection differential into components due to demographic and environmental stochasticity. We show how these two types of stochasticity affect the evolution of multivariate quantitative characters by defining demographic and environmental variances as components of individual fitness. The exact covariance formula for selection is decomposed into three components, the deterministic mean value, as well as stochastic demographic and environmental components. We show that demographic and environmental stochasticity generate random genetic drift and fluctuating selection, respectively. This provides a common theoretical framework for linking ecological and evolutionary processes. Demographic stochasticity can cause random variation in selection differentials independent of fluctuating selection caused by environmental variation. We use this model of selection to illustrate that the effect on the expected selection differential of random variation in individual fitness is dependent on population size, and that the strength of fluctuating selection is affected by how environmental variation affects the covariance in Malthusian fitness between individuals with different phenotypes. Thus, our approach enables us to partition out the effects of fluctuating selection from the effects of selection due to random variation in individual fitness caused by demographic stochasticity.     

SEXUAL SELECTION AFFECTS THE EVOLUTION OF LIFESPAN AND AGEING IN THE DECORATED CRICKET GRYLLODES SIGILLATUS

Recent work suggests that sexual selection can influence the evolution of ageing and lifespan by shaping the optimal timing and relative costliness of reproductive effort in the sexes. We used inbred lines of the decorated cricket, Gryllodes sigillatus, to estimate the genetic (co)variance between age‐dependent reproductive effort, lifespan, and ageing within and between the sexes. Sexual selection theory predicts that males should die sooner and age more rapidly than females. However, a reversal of this pattern may be favored if reproductive effort increases with age in males but not in females. We found that male calling effort increased with age, whereas female fecundity decreased, and that males lived longer and aged more slowly than females. These divergent life‐history strategies were underpinned by a positive genetic correlation between early‐life reproductive effort and ageing rate in both sexes, although this relationship was stronger in females. Despite these sex differences in life‐history schedules, age‐dependent reproductive effort, lifespan, and ageing exhibited strong positive intersexual genetic correlations. This should, in theory, constrain the independent evolution of these traits in the sexes and may promote intralocus sexual conflict. Our study highlights the importance of sexual selection to the evolution of sex differences in ageing and lifespan in G. sigillatus.     

QUANTITATIVE GENETICS OF BRYOZOAN PHENOTYPIC EVOLUTION. II. ANALYSIS OF SELECTION AND RANDOM CHANGE IN FOSSIL SPECIES USING RECONSTRUCTED GENETIC PARAMETERS

The roles of natural selection and random genetic change in the punctuated phenotypic evolution of eight Miocene-Pliocene tropical American species of the cheilostome bryozoan Metrarabdotos are analyzed by quantitative genetic methods. Trait heritabilities and genetic covariances reconstructed by partitioning within- and among-colony phenotypic variance are similar to those previously obtained for living species of the cheilostome Stylopoma using breeding data. The hypothesis that differences in skeletal morphology between species of Metrarabdotos are entirely due to mutation and genetic drift cannot be rejected for reasonable rates of mutation maintained for periods brief enough to account for the geologically abrupt appearances of these species in the fossil record. Except for one pair of species, separated by the largest morphologic distance, directional selection acting alone would require unrealistically high rates of selective mortality to be maintained for these periods. Thus, directional selection is not strongly implicated in the divergence of Metrarabdotos species. Within species, rates of net phenotypic change are slow enough to require stabilizing selection, but mask large, relatively rapid fluctuations, all of which, however, can be attributed to chance departures from the mean phenotype by mutation and genetic drift, rather than to tracking environmental fluctuation by directional selection. The results are consistent with genetic models involving shifts between multiple adaptive peaks on which phenotypes remain more or less static through long-term stabilizing selection. Regardless of the degree to which directional selection may be involved in peak shifts, phenotypic differentiation is thus related to processes different than the pervasive stabilizing selection acting within species.     

THE EVOLUTIONARY GENETICS AND DEVELOPMENTAL BASIS OF WING PATTERN VARIATION IN THE BUTTERFLY BICYCLUS ANYNANA

We have studied interactions between developmental processes and genetic variation for the eyespot color pattern on the adult dorsal forewing of the nymphalid butterfly, Bicyclus anynana. Truncation selection was applied in both an upward and a downward direction to the size of a single eyespot consisting of rings with wing scales of differing color pigments. High heritabilities resulted in rapid responses to selection yielding divergent lines with very large or very small eyespots. Strong correlated responses occurred in most of the other eyespots on each wing surface. The cells at the center of a presumptive eyespot (the “focus”) act in the early pupal stage to establish the adult wing pattern. The developmental fate of the scale cells within an eyespot is specified by the “signaling” properties of the focus and the “response” thresholds of the epidermis. The individual eyespots can be envisaged as developmental homologues. Grafting experiments performed with the eyespot foci of the selected lines showed that additive genetic variance exists for both the response and, in particular, the signaling components of the developmental system. The results are discussed in the context of how constraints on the evolution of this wing pattern may be related to the developmental organization.     

DENSITY-DEPENDENT NATURAL SELECTION IN DROSOPHILA: EVOLUTION OF GROWTH RATE AND BODY SIZE

Drosophila melanogaster populations subjected to extreme larval crowding (CU lines) in our laboratory have evolved higher larval feeding rates than their corresponding controls (UU lines). It has been suggested that this genetically based behavior may involve an energetic cost, which precludes natural selection in a density-regulated population to simultaneously maximize food acquisition and food conversion into biomass. If true, this stands against some basic predictions of the general theory of density-dependent natural selection. Here we investigate the evolutionary consequences of density-dependent natural selection on growth rate and body size in D. melanogaster. The CU populations showed a higher growth rate during the postcritical period of larval life than UU populations, but the sustained differences in weight did not translate into the adult stage. The simplest explanation for these findings (that natural selection in a crowded larval environment favors a faster food acquisition for the individual to attain the same final body size in a shorter period of time) was tested and rejected by looking at the larva-to-adult development times. Larvae of CU populations starved for different periods of time develop into comparatively smaller adults, suggesting that food seeking behavior in a food depleted environment carries a higher cost to these larvae than to their UU counterparts. The results have important implications for understanding the evolution of body size in natural populations of Drosophila, and stand against some widespread beliefs that body size may represent a compromise between the conflicting effects of genetic variation in larval and adult performance.     

THE EVOLVABILITY OF GROWTH FORM IN A CLONAL SEAWEED

Although modular construction is considered the key to adaptive growth or growth‐form plasticity in sessile taxa (e.g., plants, seaweeds and colonial invertebrates), the serial expression of genes in morphogenesis may compromise its evolutionary potential if growth forms emerge as integrated wholes from module iteration. To explore the evolvability of growth form in the red seaweed, Asparagopsis armata, we estimated genetic variances, covariances, and cross‐environment correlations for principal components of growth‐form variation in contrasting light environments. We compared variance–covariance matrices across environments to test environmental effects on heritable variation and examined the potential for evolutionary change in the direction of plastic responses to light. Our results suggest that growth form in Asparagopsis may constitute only a single genetic entity whose plasticity affords only limited evolutionary potential. We argue that morphological integration arising from modular construction may constrain the evolvability of growth form in Asparagopsis, emphasizing the critical distinction between genetic and morphological modularity in this and other modular taxa.     

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.     

GOOD GENES AND DIRECT SELECTION IN THE EVOLUTION OF MATING PREFERENCES

A model is used to study quantitatively the impact of a good genes process and direct natural selection on the evolution of a mating preference. The expression of a male display trait is proportional to genetic quality, which is determined by the number of deleterious mutations a male carries throughout his genome. Genetic variances and covariances, including the covariance between the preference and male trait that drives the good genes process, are allowed to evolve under an infinitesimal model. Results suggest that the good genes process generates only weak indirect selection on preferences, with an effective selection intensity of a few percent or less. If preferences are subject to direct natural selection of the intensity observed for other characters, the good genes process alone is not expected to exaggerate the male trait by more than a few phenotypic standard deviations, contrary to what is observed in highly sexually selected species. Good genes can, however, cause substantial exaggeration if preference genes are nearly selectively neutral. Alternatively, direct selection on preference genes, acting on mating behavior itself or on the genes' pleiotropic effects, can cause mating preferences and male display traits to be exaggerated by any degree. Direct selection of preference genes may therefore play an important role in species that show extreme sexual selection.     

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.     

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.     

THE MIXED-MODEL ANALYSIS OF VARIANCE APPLIED TO QUANTITATIVE GENETICS: BIOLOGICAL MEANING OF THE PARAMETERS

The mixed-model factorial analysis of variance has been used in many recent studies in evolutionary quantitative genetics. Two competing formulations of the mixed-model ANOVA are commonly used, the “Scheffe” model and the “SAS” model; these models differ in both their assumptions and in the way in which variance components due to the main effect of random factors are defined. The biological meanings of the two variance component definitions have often been unappreciated, however. A full understanding of these meanings leads to the conclusion that the mixed-model ANOVA could have been used to much greater effect by many recent authors. The variance component due to the random main effect under the two-way SAS model is the covariance in true means associated with a level of the random factor (e.g., families) across levels of the fixed factor (e.g., environments). Therefore the SAS model has a natural application for estimating the genetic correlation between a character expressed in different environments and testing whether it differs from zero. The variance component due to the random main effect under the two-way Scheffe model is the variance in marginal means (i.e., means over levels of the fixed factor) among levels of the random factor. Therefore the Scheffe model has a natural application for estimating genetic variances and heritabilities in populations using a defined mixture of environments. Procedures and assumptions necessary for these applications of the models are discussed. While exact significance tests under the SAS model require balanced data and the assumptions that family effects are normally distributed with equal variances in the different environments, the model can be useful even when these conditions are not met (e.g., for providing an unbiased estimate of the across-environment genetic covariance). Contrary to statements in a recent paper, exact significance tests regarding the variance in marginal means as well as unbiased estimates can be readily obtained from unbalanced designs with no restrictive assumptions about the distributions or variance-covariance structure of family effects.     

INBREEDING: ITS EFFECT ON RESPONSE TO SELECTION FOR PUPAL WEIGHT AND THE HERITABLE VARIANCE IN FITNESS IN THE FLOUR BEETLE,TRIBOLIUM CASTANEUM

We report our studies of the effect of inbreeding on the response to selection for increased pupal weight in the flour beetle, Tribolium castaneum. We also report the effects of inbreeding and selection for pupal weight on the heritable variation in fitness and fitness components. We created replicate and independent inbred lines with F-values of 0.00, 0.375, and 0.672, by 0, 2, and 5 generations, respectively, of brother-sister mating of adult beetles from an outbred stock population. Subsequently, we imposed artificial within-family selection for increased pupal weight in each of 15 inbred lines for eight generations; each line had its own paired, unselected control. We compared the response to selection across the three levels of inbreeding with theoretical expectation, and investigated the effects of inbreeding and selection on fitness variation among families within all 30 selected and control lines. Among-line variation in pupal weight increased with increased inbreeding prior to selection but diminished with directional selection. Inbreeding reduced the realized heritability of pupal weight concordant with quantitative predictions of additive theory. Mean fitness, measured in several ways, declined with inbreeding and declined further with selection. In contrast, the genetic variation for fitness in the inbred and selected lines lines equalled or exceeded that of the outbred controls. Our results suggest that inbreeding and selection may affect traits in different ways depending on the relative amounts of additive and nonadditive genetic variation.     

DIRECT AND INDIRECT SEXUAL SELECTION AND QUANTITATIVE GENETICS OF MALE TRAITS IN GUPPIES (POECILIA RETICULATA)

Abstract.— The ornamentation and displays on which sexual attractiveness and thus mating success are based may be complex and comprise several traits. Predicting the outcome of sexual selection on such complex phenotypes requires an understanding of both the direct operation of selection on each trait and the indirect consequences of selection operating directly on genetically correlated traits. Here we report the results of a quantitative genetic analysis of the ornamentation, sexual attractiveness, and mating success of male guppies (Poecilia reticulata). We analyze male ornamentation both from the point of view of single ornamental traits (e.g., the area of each color) and of composite measures of the way the entire pattern is likely to be perceived by females (e.g., the mean and contrast in chroma). We demonstrate that there is substantial additive genetic variation in almost all measures of male ornamentation and that much of this variation may be Y linked. Attractiveness and mating success are positively correlated at the phenotypic and genetic level. Orange area and chroma, the area of a male's tail, and the color contrast of his pattern overall are positively correlated with attractiveness and/or mating success at the phenotypic and genetic levels. Using attractiveness and mating success as measures of fitness, we estimate gradients of linear directional sexual selection operating on each male trait and use equations of multivariate evolutionary change to predict the response of male ornamentation to this sexual selection. From these analyses, we predict that indirect selection may have important effects on the evolution of male guppy color patterns.     

ECOLOGICAL HISTORY AND EVOLUTION IN A NOVEL ENVIRONMENT: HABITAT HETEROGENEITY AND INSECT ADAPTATION TO A NEW HOST PLANT

Environmental heterogeneity has often been implicated in the maintenance of genetic variation. However, previous research has not considered how environmental heterogeneity might affect the rate of adaptation to a novel environment. In this study, I used an insect-plant system to test the hypothesis that heterogeneous environments maintain more genetic variation in fitness components in a novel environment than do uniform environments. To manipulate recent ecological history, replicate populations of the dipteran leafminer Liriomyza trifolii were maintained for 20 generations in one of three treatments: a heterogeneous environment that contained five species of host plant, and two uniform environments that contained either a susceptible chrysanthemum or tomato. The hypothesis that greater genetic variance for survivorship and developmental time on a new host plant (a leafminer-resistant chrysanthemum) would be maintained in the heterogeneous treatment relative to the uniform environments was then tested with a sib-analysis and a natural selection experiment. Populations from the heterogeneous host plant treatment had no greater genetic variance in either larval survivorship or developmental time on the new host than did populations from either of the other treatments. Moreover, the rate of adaptation to the new host did not differ between the ecological history treatments, although the populations from the uniform chrysanthemum treatment had higher mean survivorship throughout the selection experiment. The estimates of the heritability of larval survivorship from the sib-analysis and selection experiment were quite similar. These results imply that ecologically realistic levels of environmental heterogeneity will not necessarily maintain more genetic variance than uniform environments when traits expressed in a particular novel environment are considered.     

THE EVOLUTION OF SOCIAL SIGNALS: MORPHOLOGICAL,FUNCTIONAL, AND GENETIC INTEGRATION OF THE SEX PHEROMONE IN NAUPHOETA CINEREA

Social signals that mediate intraspecific interactions can be complex, conveying considerable information concerning the probable behavior of individuals and minimizing overt aggression and wasted energy. In the cockroach Nauphoeta cinerea, male-male competition and female mate choice are mediated by a multicomponent male-produced sex pheromone. In this study, I examine variation in this pheromone. First I measure differences among males in both individual pheromone compounds and the overall composition of the pheromone. Principal component analysis is used to quantify and describe pheromone composition. Next, I explore some of the causes and consequences of this variation by examining the pheromone of males with different social experiences. Compared to subordinate males, dominant males have significantly less variable quantities of the individual pheromone compounds and are significantly less variable in the composition of their pheromone. Because of an association between status and mating success, male-male competition can result in stabilizing sexual selection on the sex pheromone. Finally, I test the hypothesis that the pheromone compounds evolve in a manner consistent with their function. As predicted for morphologically integrated characters, the patterns of phenotypic, genetic, and environmental correlations among my measures of pheromone compounds and composition match functional patterns suggested by this study and the developmental patterns demonstrated in my previous studies. Based on these studies of the N. cinerea sex pheromone, I argue that stabilizing sexual selection shapes the evolution of pheromonal communication involved in social interactions among male N. cinerea. Further, I argue that coordinated evolution of social signals may be possible due to the morphological integration of their multiple compounds.     

QUANTITATIVE GENETICS OF SEXUAL SELECTION IN THE FIELD CRICKET,GRYLLUS INTEGER

Major theories of sexual selection predict heritable variation in female preferences and male traits and a positive genetic correlation between preference and trait. Here we show that female Texas field crickets, Gryllus integer, have heritable genetic variation for the male calling song stimulus level that produces the greatest phonotactic response. Approximately 34% of the variation in female preferences was due to additive genetic effects. Female choosiness, that is, the strength of the female response to her most preferred stimulus relative to her average response to all stimuli, did not show significant genetic effects. The male calling song character was not related to male size or age but did show significant genetic effects. Approximately 39% of the variation in the number of pulses per trill was due to additive genetic variation. The genetic correlation estimated for the field population was 0.51 ± 0.17. The number of pulses per trill produced by males is under stabilizing sexual selection.     

EVOLUTION AND EXTINCTION IN A CHANGING ENVIRONMENT: A QUANTITATIVE-GENETIC ANALYSIS

Because of the ubiquity of genetic variation for quantitative traits, virtually all populations have some capacity to respond evolutionarily to selective challenges. However, natural selection imposes demographic costs on a population, and if these costs are sufficiently large, the likelihood of extinction will be high. We consider how the mean time to extinction depends on selective pressures (rate and stochasticity of environmental change, and strength of selection), population parameters (carrying capacity, and reproductive capacity), and genetics (rate of polygenic mutation). We assume that in a randomly mating, finite population subject to density-dependent population growth, individual fitness is determined by a single quantitative-genetic character under Gaussian stabilizing selection with the optimum phenotype exhibiting directional change, or random fluctuations, or both. The quantitative trait is determined by a finite number of freely recombining, mutationally equivalent, additive loci. The dynamics of evolution and extinction are investigated, assuming that the population is initially under mutation-selection-drift balance. Under this model, in a directionally changing environment, the mean phenotype lags behind the optimum, but on the average evolves parallel to it. The magnitude of the lag determines the vulnerability to extinction. In finite populations, stochastic variation in the genetic variance can be quite pronounced, and bottlenecks in the genetic variance temporarily can impair the population's adaptive capacity enough to cause extinction when it would otherwise be unlikely in an effectively infinite population. We find that maximum sustainable rates of evolution or, equivalently, critical rates of environmental change, may be considerably less than 10% of a phenotypic standard deviation per generation.