The maintenance of heritable variation through social competition

The paradoxical persistence of heritable variation for fitness-related traits is an evolutionary conundrum that remains a preeminent problem in evolutionary biology. Here we describe a simple mechanism in which social competition results in the evolutionary maintenance of heritable variation for fitness related traits. We demonstrate this mechanism using a genetic model with two primary assumptions: the expression of a trait depends upon success in social competition for limited resources; and competitive success of a genotype depends on the genotypes that it competes against. We find that such social competition generates heritable (additive) genetic variation for "competition-dependent" traits. This heritable variation is not eroded by continuous directional selection because, rather than leading to fixation of favored alleles, selection leads instead to allele frequency cycling due to the concerted coevolution of the social environment with the effects of alleles. Our results provide a mechanism for the maintenance of heritable variation in natural populations and suggest an area for research into the importance of competition in the genetic architecture of fitness related traits.     

Colour variation and alternative reproductive strategies in females of the common lizard Lacerta vivipara

Within-sex colour variation is a widespread phenomenon in animals that often plays a role in social selection. In males, colour variation is typically associated with the existence of alternative reproductive strategies. Despite ecological conditions theoretically favourable to the emergence of such alternative strategies in females, the social significance of colour variation in females has less commonly been addressed, relative to the attention given to male strategies. In a population of the common lizard, females display three classes of ventral colouration: pale yellow, orange and mixed. These ventral colours are stable through individual's life and maternally heritable. Females of different ventral colourations displayed different responses of clutch size, clutch hatching success and clutch sex-ratio to several individual and environmental parameters. Such reaction patterns might reflect alternative reproductive strategies in females. Spatial heterogeneity and presence of density- and frequency-dependent feedbacks in the environment could allow for the emergence of such alternative strategies in this population and the maintenance of colour variation in females.     

The capture of heritable variation for genetic quality through social competition

In theory, females of many species choose mates based on traits that are indicators of male genetic quality. A fundamental question in evolutionary biology is why genetic variation for such indicator traits persists despite strong persistent selection imposed by female preference, which is known as the lek paradox. One potential solution to the lek paradox suggests that the traits that are targets of mate choice should evolve condition-dependent expression and that condition should have a large genetic variance. Condition is expected to exhibit high genetic variance because it is affected by a large number of physiological processes and hence, condition-dependent traits should 'capture' variation contributed by a large number of loci. We suggest that a potentially important cause of variation in condition is competition for limited resources. Here, we discuss a pair of models to analyze the evolutionary genetics of traits affected by success in social competition for resources. We show that competition can contribute to genetic variation of 'competition-dependent' traits that have fundamentally different evolutionary properties than other sources of variation. Competition dependence can make traits honest indicators of genetic quality by revealing the relative competitive ability of males, can provide a component of heritable variation that does not contribute to trait evolution, and can help maintain heritable variation under directional selection. Here we provide a general introduction to the concept of competition dependence and briefly introduce two models to demonstrate the potential evolutionary consequences of competition-dependent trait expression.     

Early determinants of lifetime reproductive success differ between the sexes in red deer.

In polygynous, sexually dimorphic species, sexual selection should be stronger in males than in females. Although this prediction extends to the effects of early development on fitness, few studies have documented early determinants of lifetime reproductive success in a natural mammal population. In this paper, we describe factors affecting the reproductive success of male and female red deer (Cervus elaphus) on the island of Rum, Scotland. Birthweight was a significant determinant of total lifetime reproductive success in males, with heavier-born males being more successful than lighter ones. In contrast, birthweight did not affect female reproductive success. High population density and cold spring temperatures in the year of birth decreased several components of fitness in females, but did not affect the breeding success of males. The results confirm the prediction that selection on a sexually dimorphic trait should be greater in males than in females, and explain the differential maternal expenditure between sons and daughters observed in red deer. Differences between the sexes in the effects of environmental and phenotypic variation on fitness may generate differences in the amount of heritable genetic variation underlying traits such as birthweight.     

INTERACTIVE EFFECTS OF OFFSPRING SIZE AND TIMING OF REPRODUCTION ON OFFSPRING REPRODUCTION: EXPERIMENTAL,MATERNAL, AND QUANTITATIVE GENETIC ASPECTS

We demonstrate that egg size in side-blotched lizards is heritable (parent-offspring regressions) and thus will respond to natural selection. Because our estimate of heritability is derived from free-ranging lizards, it is useful for predicting evolutionary response to selection in wild populations. Moreover, our estimate for the heritability of egg size is not likely to be confounded by nongenetic maternal effects that might arise from egg size per se because we estimate a significant parent-offspring correlation for egg size in the face of dramatic experimental manipulation of yolk volume of the egg. Furthermore, we also demonstrate a significant correlation between egg size of the female parent and clutch size of her offspring. Because this correlation is not related to experimentally induced maternal effects, we suggest that it is indicative of a genetic correlation between egg size and clutch size. We synthesize our results from genetic analyses of the trade-off between egg size and clutch size with previously published experiments that document the mechanistic basis of this trade-off. Experimental manipulation of yolk volume has no effect on offspring reproductive traits such as egg size, clutch size, size at maturity, or oviposition date. However, egg size was related to offspring survival during adult phases of the life history. We partitioned survival of offspring during the adult phase of the life history into (1) survival of offspring from winter emergence to the production of the first clutch (i.e., the vitellogenic phase of the first clutch), and (2) survival of the offspring from the production of the first clutch to the end of the reproductive season. Offspring from the first clutch of the reproductive season in the previous year had higher survival during vitellogenesis of their first clutch if these offspring came from small eggs. We did not observe selection during these prelaying phases of adulthood for offspring from later clutches. However, we did find that later clutch offspring from large eggs had the highest survival over the first season of reproduction. The differences in selection on adult survival arising from maternal effects would reinforce previously documented selection that favors the production of small offspring early in the season and large offspring later in the season—a seasonal shift in maternal provisioning. We also report on a significant parent-offspring correlation in lay date and thus significant heritable variation in lay date. We can rule out the possibility of yolk volume as a confounding maternal effect—experimental manipulation of yolk volume has no effect on lay date of offspring. However, we cannot distinguish between genetic effects (i.e., heritable) and nongenetic maternal effects acting on lay date that arise from the maternal trait lay date per se (or other unidentified maternal traits). Nevertheless, we demonstrate how the timing of female reproduction (e.g., date of oviposition and date of hatching) affect reproductive attributes of offspring. Notably, we find that date of hatching has effects on body size at maturity and fecundity of offspring from later clutches. We did not detect comparable effects of lay date on offspring from the first clutch.     

Exploring the relationship between parental relatedness and male reproductive success in the Antarctic fur seal Arctocephalus gazella

Recent genetic studies of natural populations have shown that heterozygosity and other genetic estimates of parental relatedness correlate with a wide variety of fitness traits, from juvenile survival and parasite resistance to male reproductive success. Many of these traits involve health and survival, where the underlying mechanism may involve changes in the effectiveness of the immune system. However, for traits such as reproductive success, the likely mechanisms remain less obvious. In this paper, we examine the relationship between heterozygosity and a range of traits that contribute to male reproductive success, including time spent on territories and competitiveness. Our analysis is based on observational and genetic data from eight consecutive breeding seasons at a colony of the Antarctic fur seal, Arctocephalus gazella. Overall, male reproductive success was found to correlate strongly with internal relatedness (IR, a form of heterozygosity). When different components of success were analyzed, we found that IR correlates independently with reproductive longevity, time spent ashore, and competitive ability per unit mating opportunity on the study beach, with more heterozygous males being more successful. Behavioral observations were sufficiently detailed to allow examination of how daily mean IR values for males present on the beach varied within seasons and from year to year. Again, significant variation was found both among and within seasons, with more homozygous males appearing less able to hold territories in poor seasons when pup production is low and, within a season, at both the start of the season and to some extent around the peak of female estrus. Finally, we tested whether the benefits of high heterozygosity are due mainly to a genomewide effect (e.g. inbreeding depression) or to single locus heterosis by asking whether the relationship between IR and male success was robust to the removal of any single locus or to any pair of loci. Since the relationship remained significant in all cases, we favor a multilocus explanation for the effects we report.     

Maintenance of sperm variation in a highly promiscuous wild bird

Postcopulatory sexual selection is an important force in the evolution of reproductive traits, including sperm morphology. In birds, sperm morphology is known to be highly heritable and largely condition-independent. Theory predicts, and recent comparative work corroborates, that strong selection in such traits reduces intraspecific phenotypic variation. Here we show that some variation can be maintained despite extreme promiscuity, as a result of opposing, copulation-role-specific selection forces. After controlling for known correlates of siring success in the superb fairy-wren (Malurus cyaneus), we found that (a) lifetime extra-pair paternity success was associated with sperm with a shorter flagellum and relatively large head, and (b) males whose sperm had a longer flagellum and a relatively smaller head achieved higher within-pair paternity. In this species extrapair copulations occur in the same morning, but preceding, pair copulations during a female's fertile period, suggesting that shorter and relatively larger-headed sperm are most successful in securing storage (defense), whereas the opposite phenotype might be better at outcompeting stored sperm (offense). Furthermore, since cuckolding ability is a major contributor to differential male reproductive output, stronger selection on defense sperm competition traits might explain the short sperm of malurids relative to other promiscuous passerines.     

Does segregating variation in sexual or microhabitat preferences lead to non-random mating within a population of Drosophila melanogaster?

Variation in female choice for mates has implications for the maintenance of genetic variation and the evolution of male traits. Yet, estimates of population-level variation in male mating success owing to female genotype are rare. Here, we used a panel of recombinant inbred lines to estimate the strength of selection at many genetic loci in a single generation and attempt to assess differences between females with respect to the males they mated with. We performed selection assays in a complex environment to allow differences in habitat or social group preference to be expressed. We detected directional selection at loci across the genome, but are unable to provide support for differential male success because of variation in female genotype.     

Factors affecting the reproductive success of dominant male meerkats

Identifying traits that affect the reproductive success of individuals is fundamental for our understanding of evolutionary processes. In cooperative breeders, a dominant male typically restricts mating access to the dominant female for extended periods, resulting in pronounced variation in reproductive success among males. This may result in strong selection for traits that increase the likelihood of dominance acquisition, dominance retention and reproductive rates while dominant. However, despite considerable research on reproductive skew, few studies have explored the factors that influence these three processes among males in cooperative species. Here we use genetic, behavioural and demographic data to investigate the factors affecting reproductive success in dominant male meerkats (Suricata suricatta). Our data show that dominant males sire the majority of all offspring surviving to 1 year. A male's likelihood of becoming dominant is strongly influenced by age, but not by weight. Tenure length and reproductive rate, both important components of dominant male reproductive success, are largely affected by group size and composition, rather than individual traits. Dominant males in large groups have longer tenures, but after this effect is controlled, male tenure length also correlates negatively to the number of adult females in the group. Male reproductive rate also declines as the number of intra- and extra-group competitors increases. As the time spent in the dominant position and reproductive rate while dominant explain > 80% of the total variance in reproductive success, group composition thus has major implications for male reproductive success.     

Selection and inheritance of sexually dimorphic juvenile plumage coloration

Sexually dimorphic plumage coloration is widespread in birds and is generally thought to be a result of sexual selection for more ornamented males. Although many studies find an association between coloration and fitness related traits, few of these simultaneously examine selection and inheritance. Theory predicts that sex‐linked genetic variation can facilitate the evolution of dimorphism, and some empirical work supports this, but we still know very little about the extent of sex linkage of sexually dimorphic traits. We used a longitudinal study on juvenile Florida scrub‐jays (Aphelocoma coerulescens) to estimate strength of selection and autosomal and Z‐linked heritability of mean brightness, UV chroma, and hue. Although plumage coloration signals dominance in juveniles, there was no indication that plumage coloration was related to whether or not an individual bred or its lifetime reproductive success. While mean brightness and UV chroma are moderately heritable, hue is not. There was no evidence for sex‐linked inheritance of any trait with most of the variation explained by maternal effects. The genetic correlation between the sexes was high and not significantly different from unity. These results indicate that evolution of sexual dimorphism in this species is constrained by low sex‐linked heritability and high intersexual genetic correlation.     

The proximate determinants of sex ratio in C. elegans populations

The soil nematode Caenorhabditis elegans is an example of a species in which self-fertilizing hermaphrodites predominate, but functional males continue to persist--allowing outcrossing to persevere at low levels. Hermaphrodites can produce male progeny as a consequence of sex chromosome non-disjunction or via outcrossing with males. Consequently, the genetics of sex determination coupled with the efficiency by which males find, inseminate and obtain fertilizations with hermaphrodites will influence the frequency at which males and outcrossing occurs in such populations. Behavioural and physiological traits with a heritable basis, as well as ecological characters, may influence male reproductive success and therefore sex ratio. Because sex ratio is tied to male reproductive success, sex ratio greatly affects outcrossing rates, patterns of genetic variation, and the ability of natural selection to act within populations. In this paper we explore the determinants of male frequency in C. elegans with a mathematical model and experimental data. We address the role of the genetic machinery of sex determination via sex chromosome non-disjunction on sex ratio and the influence of physiological components of C. elegans' life history that contribute to variation in sex ratio by way of male reproductive success. Finally, we discuss the short-term and long-term factors that are likely to affect sex ratio and breeding system evolution in species like C. elegans.     

QUANTITATIVE GENETICS OF SIZE AND PHENOLOGY OF LIFE-HISTORY TRAITS IN CHAMAECRISTA FASCICULATA

Despite numerous adaptive scenarios concerning the evolution of plant life-history phenologies few studies have examined the heritable basis for and genetic correlations among these phenologies. Documentation of genetic variation for and covariation among reproductive phenologies is important because it is this variation/covariation that will determine the potential for response to evolutionary forces. To address this problem, I conducted a breeding experiment to determine narrow-sense heritabilities for and genetic correlations among the phenologies of life-history events and plant size in Chamaecristafasciculata, a temperate summer annual plant species. Paternal families showed no evidence of heritable variation for two estimates of plant size, six measures of reproductive phenology or two fitness components. Similarly, paternal estimates of genetic correlations among these traits were low or zero. In contrast, maternal estimates of heritability suggested the influence of maternal parent on one estimate of plant size and four phenological traits. Likewise, maternal effects influenced maternal estimates of genetic correlations. These maternal effects can arise from three sources: endosperm nuclear, cytoplasmic genetic and/or maternal phenotypic. The degree to which the phenology of one life-history trait acts as a constraint on the evolution of other phenological traits depends on the source of the maternal influence in this species.     

CONDITION, GENOTYPE-BY-ENVIRONMENT INTERACTION, AND CORRELATIONAL SELECTION IN LIZARD LIFE-HISTORY MORPHS

Abstract We compared reproductive allocation and variation in condition and survivorship of two heritable female throat color morphs (orange and yellow) in a free‐living population of side‐blotched lizards (Uta stansburiana). Using path analysis and structural equation modeling, we investigated how variation in the social environment affected clutch size and egg mass and two condition traits (postlaying mass, immunological condition) and how these traits in turn affected female field survival. In the presence of many neighbors, both morphs increased their clutch sizes, although these effects were only significant in yellow females. In addition, yellow females increased their egg mass in the presence of many orange neighbors. Orange females surrounded by many orange neighbors showed sign of stress in the form of immunosuppression, whereas this effect was less pronounced in yellow females. The morphs also differed in the impact of variation in clutch size and egg mass on both condition traits. Finally, female morphotype and immune responsiveness affected fitness interactively, and hence these two traits showed signs of fitness epistasis: Selection gradients on this trait were opposite in sign in the two morphs. The correlational selection gradient (_{γthroatxantibody response}) between female throat color and antibody responsiveness was ‐0.365. Our data thus reveal important interactive effects such as genotype‐by‐environment interaction toward the social environment and morph‐specific trade‐offs as well as the occurrence of correlational selection. We discuss the use of naturally occurring and conspicuous genetic polymorphisms in field studies of selection and life‐history allocation.     

Sex differences in the genetic architecture of aggressiveness in a sexually dimorphic spider

Sex differences in the genetic architecture of behavioral traits can offer critical insight into the processes of sex‐specific selection and sexual conflict dynamics. Here, we assess genetic variances and cross‐sex genetic correlations of two personality traits, aggression and activity, in a sexually size‐dimorphic spider, Nuctenea umbratica. Using a quantitative genetic approach, we show that both traits are heritable. Males have higher heritability estimates for aggressiveness compared to females, whereas the coefficient of additive genetic variation and evolvability did not differ between the sexes. Furthermore, we found sex differences in the coefficient of residual variance in aggressiveness with females exhibiting higher estimates. In contrast, the quantitative genetic estimates for activity suggest no significant differentiation between males and females. We interpret these results with caution as the estimates of additive genetic variances may be inflated by nonadditive genetic effects. The mean cross‐sex genetic correlations for aggression and activity were 0.5 and 0.6, respectively. Nonetheless, credible intervals of both estimates were broad, implying high uncertainty for these estimates. Future work using larger sample sizes would be needed to draw firmer conclusions on how sexual selection shapes sex differences in the genetic architecture of behavioral traits.     

Behavioral plasticity and G × E of reproductive tactics in Nicrophorus vespilloides burying beetles

Phenotypic plasticity is important in the evolution of traits and facilitates adaptation to rapid environmental changes. However, variation in plasticity at the individual level, and the heritable basis underlying this plasticity is rarely quantified for behavioral traits. Alternative behavioral reproductive tactics are key components of mating systems but are not often considered within a phenotypic plasticity framework (i.e., as reaction norms). Here, using lines artificially selected for repeated mating rate, we test for genetic (G × E) sources of variation in reproductive behavior of male Nicrophorus vespilloides burying beetles (including signaling behavior), as well as the role of individual body size, in responsiveness to changes in social environment. The results show that body size influences the response of individuals’ signaling behavior to changes in the social environment. Moreover, there was G × E underlying the responses of males to variation in the quality of social environment experienced (relative size of focal male compared to his rival). This shows that individual variation in plasticity and social sensitivity of signaling behavior can evolve in response to selection on investment in mating behavior, with males selected for high mating investment having greater social sensitivity.     

宁波滑蜥两性异形和雌性繁殖

蜥蜴的雌性繁殖特征对理解两性异形的进化原因起着重要作用。于2011年4月在安徽滁州采集宁波滑蜥(Scincella modesta),定量研究该种形态特征的两性异形和雌性繁殖特征,检验成体形态特征两性异形与雌性繁殖的相关性。研究共采集43条(17♀♀,26♂♂)宁波滑蜥,雄性和雌性个体的最大体长分别为47.4 mm和46.6 mm。雌雄两性在体长和头宽上没有差异,而在腹长和头长上差异显著,雄性有较大的头长,雌性有较大的腹长。宁波滑蜥年产单窝卵。窝卵数和窝卵重与雌体体长及腹长呈正相关,卵重与雌体体长无相关性。窝卵数及卵重的变异系数分别为0.20和0.12。卵长径与窝卵数呈负相关,而卵短径与窝卵数无关。雌体主要通过增加窝卵数来增加繁殖输出。这些结果表明,宁波滑蜥是雌雄个体大小同形的两性异形模式,性选择使得雄性有着较大的头长,以具有较高的交配成功率,生育力选择使得雌性有着较大的腹长,以具有较大的生育力和繁殖输出。     

Melanin coloration has temperature‐dependent effects on breeding performance that may maintain phenotypic variation in a passerine bird

Fluctuating selection pressure may maintain phenotypic variation because of different types of individuals being adapted to different environmental conditions. We show that the extensive variation in the coloration of male pied flycatchers (Ficedula hypoleuca) can be maintained through differences in the reproductive success of male phenotypes under different conditions. The effects of weather conditions on the relative success of different male phenotypes varied between different phases of breeding. The reproductive output of black males was the highest when it was cold during egg‐laying but warm during the nestling period, whereas the fledgling production of brown males was highest when it was continuously warm. In addition, male forehead and wing patch sizes had context‐dependent effects on timing of breeding and nestling mortality, respectively. These results indicate that environmental heterogeneity plays a role in maintaining phenotypic variation. As melanin‐based coloration is heritable, climate change may alter phenotype frequencies depending on the patterns of warming.     

A critical review of adaptive genetic variation in Atlantic salmon: implications for conservation

Here we critically review the scale and extent of adaptive genetic variation in Atlantic salmon (Salmo salar L.), an important model system in evolutionary and conservation biology that provides fundamental insights into population persistence, adaptive response and the effects of anthropogenic change. We consider the process of adaptation as the end product of natural selection, one that can best be viewed as the degree of matching between phenotype and environment. We recognise three potential sources of adaptive variation: heritable variation in phenotypic traits related to fitness, variation at the molecular level in genes influenced by selection, and variation in the way genes interact with the environment to produce phenotypes of varying plasticity. Of all phenotypic traits examined, variation in body size (or in correlated characters such as growth rates, age of seaward migration or age at sexual maturity) generally shows the highest heritability, as well as a strong effect on fitness. Thus, body size in Atlantic salmon tends to be positively correlated with freshwater and marine survival, as well as with fecundity, egg size, reproductive success, and offspring survival. By contrast, the fitness implications of variation in behavioural traits such as aggression, sheltering behaviour, or timing of migration are largely unknown. The adaptive significance of molecular variation in salmonids is also scant and largely circumstantial, despite extensive molecular screening on these species. Adaptive variation can result in local adaptations (LA) when, among other necessary conditions, populations live in patchy environments, exchange few or no migrants, and are subjected to differential selective pressures. Evidence for LA in Atlantic salmon is indirect and comes mostly from ecological correlates in fitness-related traits, the failure of many translocations, the poor performance of domesticated stocks, results of a few common-garden experiments (where different populations were raised in a common environment in an attempt to dissociate heritable from environmentally induced phenotypic variation), and the pattern of inherited resistance to some parasites and diseases. Genotype x environment interactions occurr for many fitness traits, suggesting that LA might be important. However, the scale and extent of adaptive variation remains poorly understood and probably varies, depending on habitat heterogeneity, environmental stability and the relative roles of selection and drift. As maladaptation often results from phenotype-environment mismatch, we argue that acting as if populations are not locally adapted carries a much greater risk of mismanagement than acting under the assumption for local adaptations when there are none. As such, an evolutionary approach to salmon conservation is required, aimed at maintaining the conditions necessary for natural selection to operate most efficiently and unhindered. This may require minimising alterations to native genotypes and habitats to which populations have likely become adapted, but also allowing for population size to reach or extend beyond carrying capacity to encourage competition and other sources of natural mortality.     

Hormones and mating system affect sex and species differences in immune function among vertebrates

Males generally exhibit reduced immune responses as well as increased intensity and prevalence of infections compared to female conspecifics. Physiologically, these sex differences may reflect the immunosuppressive effects of androgens. In addition to suppressing immune function, androgens maintain several characteristics important for reproductive success. Thus, a dynamic relationship is assumed to exist among hormones, secondary sex traits, and the immune system. Ultimately, the extent to which this relationship exists may be related to the mating system. Because polygynous males generally have higher circulating testosterone concentrations and rely more heavily on testosterone-dependent traits for reproductive success than monogamous males, sex differences in immune function are hypothesised to be more pronounced among polygynous as compared to monogamous species. Additionally, if secondary sex traits are used to advertise infection status, then females should be able to use the condition of male secondary sex traits to discern the immune/infection status of males during mate selection. The purpose of this review is to survey current studies that examine both the proximate mechanisms and ultimate function of variation in immune function and susceptibility to infection and determine whether immunological variation influences mate preference and possibly reproductive success.