Runaway sexual selection when female preferences are directly selected

We introduce models for the runaway coevolution of female mating preferences and male display traits. The models generalize earlier results by allowing for direct natural selection on the preference, arbitrary forms of mate choice, and fairly general assumptions about the underlying genetics. Results show that a runaway is less likely when there is direct selection on the preference, but that it is still possible if there is a sufficiently large phenotypic correlation between the female's preference and the male's trait among mated pairs. Comparison of three preference functions introduced by Lande (1981) shows that open-ended preferences are particularly prone to a runaway, and that absolute preferences require very large differences between females in their preferences. We analyze the causes of the runaway seen in a model developed by Iwasa and Pomiankowski (1995).     

The role of genetic constraints and social environment in explaining female extra-pair mating

Why do females of socially monogamous species engage in extra-pair copulations? This long-standing question remains a puzzle, because the benefits of female promiscuous behavior often do not seem to outweigh the costs. Genetic constraint models offer an answer by proposing that female promiscuity emerges through selection favoring alleles that are either beneficial for male reproductive success (intersexual pleiotropy hypothesis) or beneficial for female fecundity (intrasexual pleiotropy hypothesis). A previous quantitative genetic study on captive zebra finches, Taeniopygia guttata, reported support for the first, but not for the second hypothesis. Here, we re-examine both hypotheses based on data from lines selected for high and low male courtship rate. In contrast to previous conclusions, our new analyses clearly reject the hypothesis that male and female promiscuity are genetically homologous traits. We find some support for a positive genetic correlation between female promiscuity and fecundity. This study also shows that the behavioral outcome of extra-pair courtships primarily depends on individual-specific female preferences and not on the “attractiveness” of the social mate. In contrast, patterns of paternity are strongly influenced by the social partner and the pair bond, presumably reflecting variation in copulation behavior, fertility, or sperm competitiveness.     

Sexual selection of multiple handicaps in the red-collared widowbird: female choice of tail length but not carotenoid display

Although sexual selection through female choice explains exaggerated male ornaments in many species, the evolution of the multicomponent nature of most sexual displays remains poorly understood. Theoretical models suggest that handicap signaling should converge on a single most informative quality indicator, whereas additional signals are more likely to be arbitrary Fisherian traits, amplifiers, or exploitations of receiver psychology. Male nuptial plumage in the highly polygynous red-collared widowbird (Euplectes ardens) comprises two of the commonly advocated quality advertisements (handicaps) in birds: a long graduated tail and red carotenoid coloration. Here we use multivariate selection analysis to investigate female choice in relation to male tail length, color (reflectance) of the collar, other aspects of morphology, ectoparasite load, display rate, and territory quality. The order and total number of active nests obtained are used as measures of male reproductive success. We demonstrate a strong female preference and net sexual selection for long tails, but marginal or no effects of color, morphology, or territory quality. Tail length explained 47% of male reproductive success, an unusually strong fitness effect of natural ornament variation. Fluctuating tail asymmetry was unrelated to tail length, and had no impact on mating success. For the red collar, there was negative net selection on collar area, presumably via its negative relationship with tail length. None of the color variables (hue, chroma, and brightness) had significant selection differentials, but a partial effect (selection gradient) of chroma might represent a color preference when tail length is controlled for. We suggest that the red collar functions in male agonistic interactions, which has been strongly supported by subsequent work. Thus, female choice targets only one handicap, extreme tail elongation, disregarding or even selecting against the carotenoid display. We discuss whether long tails might be better indicators of genetic quality than carotenoid pigmentation. As regards the evolution of multiple ornaments, we propose that multiple handicap signaling is stable not because of multiple messages but because of multiple receivers, in this case females and males.     

Estimating evolutionary parameters when viability selection is operating

Some individuals die before a trait is measured or expressed (the invisible fraction), and some relevant traits are not measured in any individual (missing traits). This paper discusses how these concepts can be cast in terms of missing data problems from statistics. Using missing data theory, I show formally the conditions under which a valid evolutionary inference is possible when the invisible fraction and/or missing traits are ignored. These conditions are restrictive and unlikely to be met in even the most comprehensive long-term studies. When these conditions are not met, many selection and quantitative genetic parameters cannot be estimated accurately unless the missing data process is explicitly modelled. Surprisingly, this does not seem to have been attempted in evolutionary biology. In the case of the invisible fraction, viability selection and the missing data process are often intimately linked. In such cases, models used in survival analysis can be extended to provide a flexible and justified model of the missing data mechanism. Although missing traits pose a more difficult problem, important biological parameters can still be estimated without bias when appropriate techniques are used. This is in contrast to current methods which have large biases and poor precision. Generally, the quantitative genetic approach is shown to be superior to phenotypic studies of selection when invisible fractions or missing traits exist because part of the missing information can be recovered from relatives.     

Sexual dimorphism in lizard body shape: the roles of sexual selection and fecundity selection

Sexual dimorphism is widespread in lizards, with the most consistently dimorphic traits being head size (males have larger heads) and trunk length (the distance between the front and hind legs is greater in females). These dimorphisms have generally been interpreted as follows: (1) large heads in males evolve through male-male rivalry (sexual selection); and (2) larger interlimb lengths in females provide space for more eggs (fecundity selection). In an Australian lizard (the snow skink, Niveoscincus microlepidotus), we found no evidence for ongoing selection on head size. Trunk length, however, was under positive fecundity selection in females and under negative sexual selection in males. Thus, fecundity selection and sexual selection work in concert to drive the evolution of sexual dimorphism in trunk length in snow skinks.     

Sexual selection and its evolutionary consequences in female animals

For sexual selection to act on a given sex, there must exist variation in the reproductive success of that sex as a result of differential access to mates or fertilisations. The mechanisms and consequences of sexual selection acting on male animals are well documented, but research on sexual selection acting on females has only recently received attention. Controversy still exists over whether sexual selection acts on females in the traditional sense, and over whether to modify the existing definition of sexual selection (to include resource competition) or to invoke alternative mechanisms (usually social selection) to explain selection acting on females in connection with reproduction. However, substantial evidence exists of females bearing characters or exhibiting behaviours that result in differential reproductive success that are analogous to those attributed to sexual selection in males. Here we summarise the literature and provide substantial evidence of female intrasexual competition for access to mates, female intersexual signalling to potential mates, and postcopulatory mechanisms such as competition between eggs for access to sperm and cryptic male allocation. Our review makes clear that sexual selection acts on females and males in similar ways but sometimes to differing extents: the ceiling for the elaboration of costly traits may be lower in females than in males. We predict that current and future research on female sexual selection will provide increasing support for the parsimony and utility of the existing definition of sexual selection.     

A simple completion of Fisher’s fundamental theorem of natural selection

Fisher''s fundamental theorem of natural selection shows that the part of the rate of change of mean fitness that is due to natural selection equals the additive genetic variance in fitness. Fisher embedded this result in a model of total fitness, adding terms for deterioration of the environment and density dependence. Here, a quantitative genetic version of this neglected model is derived that relaxes its assumptions that the additive genetic variance in fitness and the rate of deterioration of the environment do not change over time, allows population size to vary, and includes an input of mutational variance. The resulting formula for total rate of change in mean fitness contains two terms more than Fisher''s original, representing the effects of stabilizing selection, on the one hand, and of mutational variance, on the other, making clear for the first time that the fundamental theorem deals only with natural selection that is directional (as opposed to stabilizing) on the underlying traits. In this model, the total (rather than just the additive) genetic variance increases mean fitness. The unstructured population allows an explanation of Fisher''s concept of fitness as simply birth rate minus mortality rate, and building up to the definition in structured populations.     

Evolution in response to social selection: the importance of interactive effects of traits on fitness

Social interactions have a powerful effect on the evolutionary process. Recent attempts to synthesize models of social selection with equations for indirect genetic effects (McGlothlin et al. 2010) provide a broad theoretical base from which to study selection and evolutionary response in the context of social interactions. However, this framework concludes that social selection will lead to evolution only if the traits carried by social partners are nonrandomly associated. I suggest this conclusion is incomplete, and that traits that do not covary between social partners can nevertheless lead to evolution via interactive effects on fitness. Such effects occur when there are functional interactions between traits, and as an example I use the interplay in water striders (Gerridae) between grasping appendages carried by males and spines by females. Functional interactive effects between traits can be incorporated into both the equations for social selection and the general model of social evolution proposed by McGlothlin et al. These expanded equations would accommodate adaptive coevolution in social interactions, integrate the quantitative genetic approach to social evolution with game theoretical approaches, and stimulate some new questions about the process of social evolution.     

Male parental care, female reproductive success, and extrapair paternity

Birds differ considerably in the degree of male parental care,and it has been suggested that interspecific variation in extrapairpaternity is determined by the relative importance of benefitsto females from male parental care and good genes from extrapairsires. I estimated the relationship between extrapair paternityand the importance of male parental care for female reproductivesuccess mainly based on male removal studies, using a comparativeapproach. The reduction in female reproductive success causedby the absence of a male mate was positively correlated withthe male contribution to feeding offspring. The frequency ofextrapair paternity was negatively related to the reductionin female reproductive success caused by the absence of a mate.This was also the case when potentially confounding variablessuch as developmental mode of offspring and sexual dichromatismwere considered. A high frequency of extrapair paternity occursparticularly in bird species in which males play a minor rolein offspring provisioning and in which attractive males providerelatively little parental care. Bird species with frequentextrapair paternity thus appear to be those in which direct fitness benefits from male care are small, females can readilycompensate for the absence of male care, and indirect fitnessbenefits from extrapair sires are important.     

Sexual selection drives the coevolution of male and female reproductive traits in Peromyscus mice

When females mate with multiple partners within a single reproductive cycle, sperm from rival males may compete for fertilization of a limited number of ova, and females may bias the fertilization of their ova by particular sperm. Over evolutionary timescales, these two forms of selection shape both male and female reproductive physiology when females mate multiply, yet in monogamous systems, post-copulatory sexual selection is weak or absent. Here, we examine how divergent mating strategies within a genus of closely related mice, Peromyscus, have shaped the evolution of reproductive traits. We show that in promiscuous species, males exhibit traits associated with increased sperm production and sperm swimming performance, and females exhibit traits that are predicted to limit sperm access to their ova including increased oviduct length and a larger cumulus cell mass surrounding the ova, compared to monogamous species. Importantly, we found that across species, oviduct length and cumulus cell density are significantly correlated with sperm velocity, but not sperm count or relative testes size, suggesting that these female traits may have coevolved with increased sperm quality rather than quantity. Taken together, our results highlight how male and female traits evolve in concert and respond to changes in the level of post-copulatory sexual selection.     

Evolution of female colours in birds: The role of female cost of reproduction and paternal care

Female ornamentation is frequently observed in animal species and is sometimes found as more evolutionary labile than male ornamentation. A complex array of factors may explain its presence and variation. Here we assessed the role of female cost of reproduction and paternal care. Both factors have been pinpointed as important by theoretical studies but have not been investigated yet in details at the interspecific level. We worked on 133 species of North temperate Passeriformes bird species for which both the clutch volume – here taken as the proxy of female cost of reproduction – and amount of paternal care are relatively well known. Using spectrometry, we measured the whole-body coloured plumage patches and quantified three metrics corresponding to brightness (i.e. achromatic component), colour chromaticity (i.e. intensity) and colour volume (i.e. diversity). We found a strong association between male and female colour metrics. Controlling for this association, we found additional small but detectable effects of both cost of reproduction and paternal care. First, females of species with more paternal care were slightly brighter. Second, the interaction between the level of paternal care and egg volume was correlated with female colour intensity: females with more paternal care were more chromatic, with this association mostly present when their investment in reproduction was low. Together these results suggest that female cost of reproduction and paternal care are part of the multiple factors explaining variation of female coloration, besides the strong covariation between male and female coloration.     

Natural selection. VII. History and interpretation of kin selection theory

Kin selection theory is a kind of causal analysis. The initial form of kin selection ascribed cause to costs, benefits and genetic relatedness. The theory then slowly developed a deeper and more sophisticated approach to partitioning the causes of social evolution. Controversy followed because causal analysis inevitably attracts opposing views. It is always possible to separate total effects into different component causes. Alternative causal schemes emphasize different aspects of a problem, reflecting the distinct goals, interests and biases of different perspectives. For example, group selection is a particular causal scheme with certain advantages and significant limitations. Ultimately, to use kin selection theory to analyse natural patterns and to understand the history of debates over different approaches, one must follow the underlying history of causal analysis. This article describes the history of kin selection theory, with emphasis on how the causal perspective improved through the study of key patterns of natural history, such as dispersal and sex ratio, and through a unified approach to demographic and social processes. Independent historical developments in the multivariate analysis of quantitative traits merged with the causal analysis of social evolution by kin selection.     

Sexual selection in gallus: Effects of morphology and dominance on female spatial behavior

Sexual selection has received a great deal of attention from field and laboratory researchers for over a century, but hard evidence of female choice of mates in mixed-sex groups remains scarce. Dominant males typically mate much more often than subordinants but evidence that females “choose” such males is elusive. In $\text{Gallus}$, which includes junglefowl and their domestic fowl descendants, females stay near and mate with dominant, territorial males. We demonstrate here that $\text{Gallus}$ females in mixed-sex flocks who have no information about the social dominance status of males orient to, approach and stay near males with larger than average combs whereas females which $\text{do}$ not have information about male dominance orient toward and stay near high ranking males. We verify that comb size correlates with male social rank. Hence, $\text{Gallus}$ females do actively respond to “high quality” males; they apparently identify such males by male physical characteristics and, if available, information concerning male-male interactions.     

Sexual selection and the evolution of costly female preferences: spatial effects

Abstract.— Models of Fisher's runaway process show that if there is a cost to female preference, no preference or male trait exaggeration will evolve. Surprisingly, this is true no matter how small the cost, which reveals that these models of Fisher's process are structurally unstable (Bulmer 1989). Here a model of Fisher's runaway process is presented to demonstrate that costly female preference evolves very easily when space is explicitly included in the model. The only requirement is that the optimal male phenotype changes across the species' range. The model shows that the spatial average of the female preference and male trait reach an evolutionary equilibrium that is identical to those of nonspatial models, but that the preference and male trait can deviate greatly from these averages at any point in space. For example, if random mating results in the lowest cost to females, then at equilibrium the spatial average preference will be zero. Nevertheless, there will be some locations at which females prefer males with larger ornaments and others where they prefer males with smaller ornaments. Results also show that the structural instability of nonspatial models of Fisher's process is less of a problem in spatial models. In particular, many of the main qualitative features of cost-free spatial models of Fisher's process remain valid even when there are small costs of female preference. Finally, the model shows that abrupt changes in the optimal male phenotype across space can result in an amplification of this pattern when preference has a small cost, but it can also result in a pattern similar to reproductive character displacement. Which of these occurs depends on the magnitude of the cost of female preference. This suggests that some patterns of reproductive character displacement in nature might be explained simply by sexual selection rather than by hybrid dysgenesis and reinforcement.     

Quantitative genetic study of the adaptive process

The additive genetic variance with respect to absolute fitness, V_A(W), divided by mean absolute fitness, , sets the rate of ongoing adaptation. Fisher''s key insight yielding this quantitative prediction of adaptive evolution, known as the Fundamental Theorem of Natural Selection, is well appreciated by evolutionists. Nevertheless, extremely scant information about V_A(W) is available for natural populations. Consequently, the capacity for fitness increase via natural selection is unknown. Particularly in the current context of rapid environmental change, which is likely to reduce fitness directly and, consequently, the size and persistence of populations, the urgency of advancing understanding of immediate adaptive capacity is extreme. We here explore reasons for the dearth of empirical information about V_A(W), despite its theoretical renown and critical evolutionary role. Of these reasons, we suggest that expectations that V_A(W) is negligible, in general, together with severe statistical challenges of estimating it, may largely account for the limited empirical emphasis on it. To develop insight into the dynamics of V_A(W) in a changing environment, we have conducted individual-based genetically explicit simulations. We show that, as optimizing selection on a trait changes steadily over generations, V_A(W) can grow considerably, supporting more rapid adaptation than would the V_A(W) of the base population. We call for direct evaluation of V_A(W) and in support of prediction of rates adaptive evolution, and we advocate for the use of aster modeling as a rigorous basis for achieving this goal.     

Sexual selection is ineffectual or inhibits the purging of deleterious mutations in Drosophila melanogaster

The effects of sexual selection on population mean fitness are unclear and a subject of debate. Recent models propose that, because reproductive success may be condition dependent, much of the genome may be a target of sexual selection. Under this scenario, mutations that reduce health, and thus nonsexual fitness, may also be deleterious with respect to reproductive success, meaning that sexual selection may contribute to the purging of deleterious alleles. We tested this hypothesis directly by subjecting replicate Drosophila melanogaster populations to two treatments that altered the opportunity for sexual selection and then tracked changes in the frequency of six separate deleterious alleles with recessive and visible phenotypic effects. While natural selection acted to decrease the frequency of all six mutations, the addition of sexual selection did not aid in the purging of any of them, and for three of them appears to have hampered it. Courtship and mating have harmful effects in this species and mate choice assays showed that males directed more courtship and mating behavior toward wild-type over mutant females, providing a likely explanation for sexual selection's cost. Whether this cost extends to other mutations (e.g., those lacking visible phenotypic effects) is an important topic for future research.     

Sex‐linked inheritance,genetic correlations and sexual dimorphism in three melanin‐based colour traits in the barn owl

Theory states that genes on the sex chromosomes have stronger effects on sexual dimorphism than genes on the autosomes. Although empirical data are not necessarily consistent with this theory, this situation may prevail because the relative role of sex‐linked and autosomally inherited genes on sexual dimorphism has rarely been evaluated. We estimated the quantitative genetics of three sexually dimorphic melanin‐based traits in the barn owl (Tyto alba), in which females are on average darker reddish pheomelanic and display more and larger black eumelanic feather spots than males. The plumage traits with higher sex‐linked inheritance showed lower heritability and genetic correlations, but contrary to prediction, these traits showed less pronounced sexual dimorphism. Strong offspring sexual dimorphism primarily resulted from daughters not expressing malelike melanin‐based traits and from sons expressing femalelike traits to similar degrees as their sisters. We conclude that in the barn owl, polymorphism at autosomal genes rather than at sex‐linked genes generate variation in sexual dimorphism in melanin‐based traits.