Status-dependent selection in the dimorphic beetle Onthophagus taurus.

The occurrence of alternative reproductive phenotypes is widespread in most animal taxa. The majority of known examples best fit the notion of alternative tactics within a conditional strategy where the fitness pay-offs depend on an individual's competitive ability or status. Individuals are proposed as "choosing" the tactic that maximizes their fitness, given their status relative to others in the population. Theoretically, status-dependent selection should determine when an animal should switch between alternative tactics. While a number of studies have demonstrated unequal fitness pay-offs associated with alternative tactics, none, to our knowledge, have examined the fitness functions necessary for predicting when individuals should switch between tactics. Here, we use a dimorphic male beetle in order to provide the first empirically derived fitness function across alternative reproductive phenotypes. Our data provide empirical support for a game-theoretic conditional strategy that has evolved under status-dependent selection.     

A Syringe-Like Love Dart Injects Male Accessory Gland Products in a Tropical Hermaphrodite

Sexual conflict shapes the evolution of many behaviours and processes involved in reproduction. Nearly all evidence supporting this comes from species where the sexes are separated. However, a substantial proportion of animals and most plants are hermaphroditic, and theoretical work predicts that sexual conflict plays an important role even when the sexes are joined within one individual. This seems to have resulted in bizarre mating systems, sophisticated sperm packaging and complex reproductive morphologies. By far the best-known example of such a strategy in hermaphrodites is the shooting of so-called love-darts in land snails. All known love darts carry a gland product on their outside and enter this into the partner’s hemolymph by stabbing. Here, we show that species of the snail genus Everettia possess a syringe-like dart that serves as a real injection needle. Their dart is round in cross-section, contains numerous channels, and has perforations along its side. Histology and electron microscopy show that these holes connect to the channels inside the dart and run all the way up to the elaborate mucus glands that are attached to the dart sac. This is the first report on a love dart that is used as a syringe to directly inject the gland product into the partner’s hemolymph. Although the exact use and function of this dart remains to be demonstrated, this clearly adds to the complexity of the evolution of reproductive strategies in hermaphrodites in general. Moreover, the perforations on the outside of the love dart resemble features of other injection devices, thus uncovering common design and repeated evolution of such features in animals.     

Do alternative reproductive strategies in the Wellington tree weta represent different behavioural types?

In many animal species, variation in reproductive success among individuals has led to the evolution of alternative mating strategies, which in the case of insects can often be correlated with developmental trajectories. In the Wellington tree weta, Hemideina crassidens, males can mature at the 8th, 9th or 10th instar, while females mature at the 10th instar only. A number of morphological attributes including male head and mandible size correlate with final instar number, and as these attributes represent a form of weaponry, they are often used in mate/site guarding and male–male competition. Tenth instar males have larger head/mandible/body sizes and show a conventional (guarder) reproductive strategy, whereas smaller 8th instar males typically show an unconventional (sneaker) strategy. In contrast, 9th instar males are predicted to adopt a “jack‐of‐all‐trades” strategy whereby they can fight or sneak depending context. Here, we tested whether alternative reproductive morphs exhibit strategy‐specific differences in risk‐taking associated with refuge emergence, activity and antipredator behaviour and further, whether these traits correlate to form a behavioural syndrome. We found that tree weta show consistent and repeatable differences in activity and refuge use at the individual level; however, behavioural covariances suggest that only 8th instar males exhibit a behavioural syndrome. That 9th instar males show high plasticity and variance in their gallery‐related behaviours supports the hypothesis that these males are a “jack‐of‐all‐trades.” Contrary to our predictions, antipredator behaviour was not correlated with other traits, and differences in behaviour overall were consistently more pronounced between individuals rather than between male morphs or sexes.     

The status of the conditional evolutionarily stable strategy

The conditional evolutionarily stable strategy (ESS) has proven to be a versatile tool for understanding the production of alternative phenotypes in response to environmental cues. Hence, we would expect the theoretical basis of the conditional strategy to be robust. However, Shuster and Wade have recently criticized the conditional ESS based on Gross's 1996 proposal that most alternative reproductive tactics are conditional and have evolved by 'status-dependent selection.' We critically assess Gross's status-dependent selection model and Shuster and Wade's critique. We find shortcomings and misconceptions in both. We return to the findings of the strategic models behind the conditional ESS and demonstrate how environmental threshold models use a reaction norm approach and quantitative genetic theory to understand the evolution of conditional strategies.     

The evolution of alternative reproductive strategies: fitness differential, heritability, and genetic correlation between the sexes

Paternity analyses using molecular markers have become standard in studies of mating systems, parentage, and kinship. In systems where individuals exhibit alternative mating strategies, molecular analyses have been productively used to estimate the reproductive success of each behavioral type and hence the fitness consequences to each individual. Here we review the fitness results in a system of five alternative mating strategies present in one population of side-blotched lizards (Uta stansburiana). Males in this population adopt one of three behavioral strategies that differ in their degree of territoriality and mate guarding. In contrast, females adopt one of two strategies that differ in offspring quantity and quality. We use paternity analyses to estimate the fitness of each morph, the heritability of reproductive strategy, and the correlation in strategy between the sexes and discuss the implications of our findings for the evolution and maintenance of reproductive polymorphism in this and other systems.     

The Evolution and Consequences of Sex-Specific Reproductive Variance

Natural selection favors alleles that increase the number of offspring produced by their carriers. But in a world that is inherently uncertain within generations, selection also favors alleles that reduce the variance in the number of offspring produced. If previous studies have established this principle, they have largely ignored fundamental aspects of sexual reproduction and therefore how selection on sex-specific reproductive variance operates. To study the evolution and consequences of sex-specific reproductive variance, we present a population-genetic model of phenotypic evolution in a dioecious population that incorporates previously neglected components of reproductive variance. First, we derive the probability of fixation for mutations that affect male and/or female reproductive phenotypes under sex-specific selection. We find that even in the simplest scenarios, the direction of selection is altered when reproductive variance is taken into account. In particular, previously unaccounted for covariances between the reproductive outputs of different individuals are expected to play a significant role in determining the direction of selection. Then, the probability of fixation is used to develop a stochastic model of joint male and female phenotypic evolution. We find that sex-specific reproductive variance can be responsible for changes in the course of long-term evolution. Finally, the model is applied to an example of parental-care evolution. Overall, our model allows for the evolutionary analysis of social traits in finite and dioecious populations, where interactions can occur within and between sexes under a realistic scenario of reproduction.     

SEASONALITY MAINTAINS ALTERNATIVE LIFE‐HISTORY PHENOTYPES

Many organisms express discrete alternative phenotypes (polyphenisms) in relation to predictable environmental variation. However, the evolution of alternative life‐history phenotypes remains poorly understood. Here, we analyze the evolution of alternative life histories in seasonal environments by using temperate insects as a model system. Temperate insects express alternative developmental pathways of diapause and direct development, the induction of a certain pathway affecting fitness through its life‐history correlates. We develop a methodologically novel and holistic simulation model and optimize development time, growth rate, body size, reproductive effort, and adult life span simultaneously in both developmental pathways. The model predicts that direct development should be associated with shorter development time (duration of growth) and adult life span, higher growth rate and reproductive effort, smaller body size as well as lower fecundity compared to the diapause pathway, because the two generations divide the available time unequally. These predictions are consistent with many empirical data. Our analysis shows that seasonality alone can explain the evolution of alternative life histories.     

Endocrine correlates of alternative phenotypes in the white-throated sparrow (Zonotrichia albicollis)

Many vertebrate species exhibit alternative phenotypes (or morphs), in which one sex displays phenotypic variation equal to or greater than the variation between the sexes. Males in such species typically display differences in reproductive strategies and morphology. Steroid hormones such as testosterone are known modulators of reproductive behavior and morphology and therefore are obvious candidates for the mediation of phenotypic differences between morphs. We conducted a year-round study in the white-throated sparrow (Zonotrichia albicollis) that exhibits alternative phenotypes in plumage coloration and behavior in both sexes: during the breeding season, white-striped males and females are more aggressive and have higher song rates than tan-striped individuals. At the beginning of the breeding season, free-living white-striped males had higher plasma testosterone concentrations than tan-striped males. However, this finding might have been due to different social experiences because captive male morphs sampled at similar times of year did not differ in testosterone concentrations. Captive white-striped males had larger testis and cloacal protuberance sizes than tan-striped males, which might be related to the divergent mating strategies of the morphs. Male morphs showed similar increases in luteinizing hormone following injections of gonadotropin-releasing hormone, but white-striped males showed larger increases in testosterone, indicating differences between morphs in gonadal testosterone production. Females had low concentrations of testosterone, and morphs did not differ. Plasma dehydroepiandrosterone (DHEA) concentrations were elevated in both sexes and morphs during the breeding and non-breeding seasons. These data do not support the hypothesis that testosterone activates behavioral differences between alternative phenotypes in the white-throated sparrow. Alternative testable hypotheses include hormonal effects during early development and direct genetic effects.     

Sexual selection and alternative mating behaviours generate demographic stochasticity in small populations.

Recent theory predicts that environmental variation and small population size facilitate the coexistence of alternative phenotypes despite unequal mean fitness. However, traditional studies of reproductive strategies often assume that the stability of alternative mating behaviours relies on equal male fitness. We present results from field observations and experimental manipulations of thermal resources on territories demonstrating the coexistence of alternative reproductive behaviours with unequal fitness. The side-blotched lizard Uta stansburiana exhibits two alternative strategies for territoriality: "usurp" and "defend". Paternity analysis revealed significantly greater mean fitness for "usurpers" than "defenders" in our study of natural variation. Moreover, variance in fitness was significantly higher for usurpers on both experimental and natural plots, implying that "usurp" is a risky strategy with potentially large pay-offs or none at all. We show theoretically that significantly higher variance in usurper fitness can allow for coexistence with defenders despite higher mean fitness of usurpers. This coexistence is facilitated by small population size. Our results have general implications for the evolution of alternative strategies and the maintenance of genetic diversity in small populations.     

A role for ecology in the evolution of colour variation and sexual dimorphism in Hawaiian damselflies

Variation in traits that are sexually dimorphic is usually attributed to sexual selection, in part because the influence of ecological differences between sexes can be difficult to identify. Sex‐limited dimorphisms, however, provide an opportunity to test ecological selection disentangled from reproductive differences between the sexes. Here, we test the hypothesis that ecological differences play a role in the evolution of body colour variation within and between sexes in a radiation of endemic Hawaiian damselflies. We analysed 17 Megalagrion damselflies species in a phylogenetic linear regression, including three newly discovered cases of species with female‐limited dimorphism. We find that rapid colour evolution during the radiation has resulted in no phylogenetic signal for most colour and habitat traits. However, a single ecological variable, exposure to solar radiation (as measured by canopy cover) significantly predicts body colour variation within sexes (female‐limited dimorphism), between sexes (sexual dimorphism), and among populations and species. Surprisingly, the degree of sexual dimorphism in body colour is also positively correlated with the degree of habitat differences between sexes. Specifically, redder colouration is associated with more exposure to solar radiation, both within and between species. We discuss potential functions of the pigmentation, including antioxidant properties that would explain the association with light (specifically UV) exposure, and consider alternative mechanisms that may drive these patterns of sexual dimorphism and colour variation.     

Intralocus tactical conflict: genetic correlations between fighters and sneakers of the dung beetle Onthophagus taurus

Males and females differ in their phenotypic optima for many traits, and as the majority of genes are expressed in both sexes, some alleles can be beneficial to one sex but harmful to the other (intralocus sexual conflict; ISC). ISC theory has recently been extended to intrasexual dimorphisms, where certain alleles may have opposite effects on the fitness of males of different morphs that employ alternative reproductive tactics (intralocus tactical conflict; ITC). Here, we use a half‐sib breeding design to investigate the genetic basis for ISC and ITC in the dung beetle Onthophagus taurus. We found positive heritabilities and intersexual genetic correlations for almost all traits investigated. Next, we calculated the intrasexual genetic correlation between males of different morphs for horn length, a sexually selected trait, and compared it to intrasexual correlations for naturally selected traits in both sexes. Intrasexual genetic correlations did not differ significantly between the sexes or between naturally and sexually selected traits, failing to support the hypothesis that horns present a reduction of intrasexual genetic correlations due to ITC. We discuss the implications for the idea of developmental reprogramming between male morphs and emphasize the importance of genetic correlations as constraints for the evolution of dimorphisms.     

Pollen limitation of female reproductive success at fine spatial scale in a gynodioecious and wind-pollinated species, Beta vulgaris ssp. maritima

In sexually polymorphic plants, the spatial distribution of sexes is usually not random. Local variation in phenotype frequencies is expected to affect individual fitness of the different phenotypes. For gynodioecious species, with co-occurrence of hermaphrodites and females, if sexual phenotypes are structured in space and pollen flow is spatially restricted, local pollen availability should vary among patches. Female fitness may thus be low when hermaphrodites are locally rare. To test this hypothesis, we analysed how the reproductive output of females varied among patches within two natural study sites of the gynodioecious wind-pollinated Beta vulgaris ssp. maritima. Plants growing in female-biased areas and experiencing pollen limitation were found to have low fruit and seed sets but did not reallocate resources towards better offspring. Our results show that fine-scale processes influence individual fitness and the evolution of sex ratio in sexually polymorphic plants.     

Evolution of alternative insect life histories in stochastic seasonal environments

Deterministic seasonality can explain the evolution of alternative life history phenotypes (i.e., life history polyphenism) expressed in different generations emerging within the same year. However, the influence of stochastic variation on the expression of such life history polyphenisms in seasonal environments is insufficiently understood. Here, we use insects as a model and explore (1) the effects of stochastic variation in seasonality and (2) the life cycle on the degree of life history differentiation among the alternative developmental pathways of direct development and diapause (overwintering), and (3) the evolution of phenology. With numerical simulation, we determine the values of development (growth) time, growth rate, body size, reproductive effort, adult life span, and fecundity in both the overwintering and directly developing generations that maximize geometric mean fitness. The results suggest that natural selection favors the expression of alternative life histories in the alternative developmental pathways even when there is stochastic variation in seasonality, but that trait differentiation is affected by the developmental stage that overwinters. Increasing environmental unpredictability induced a switch to a bet‐hedging type of life history strategy, which is consistent with general life history theory. Bet‐hedging appeared in our study system as reduced expression of the direct development phenotype, with associated changes in life history phenotypes, because the fitness value of direct development is highly variable in uncertain environments. Our main result is that seasonality itself is a key factor promoting the evolution of seasonally polyphenic life histories but that environmental stochasticity may modulate the expression of life history phenotypes.     

Meek Males and Fighting Females: Sexually-Dimorphic Antipredator Behavior and Locomotor Performance Is Explained by Morphology in Bark Scorpions (Centruroides vittatus)

Sexual dimorphism can result from sexual or ecological selective pressures, but the importance of alternative reproductive roles and trait compensation in generating phenotypic differences between the sexes is poorly understood. We evaluated morphological and behavioral sexual dimorphism in striped bark scorpions (Centruroides vittatus). We propose that reproductive roles have driven sexually dimorphic body mass in this species which produces sex differences in locomotor performance. Poor locomotor performance in the females (due to the burden of being gravid) favors compensatory aggression as part of an alternative defensive strategy, while male morphology is coadapted to support a sprinting-based defensive strategy. We tested the effects of sex and morphology on stinging and sprinting performance and characterized overall differences between the sexes in aggressiveness towards simulated threats. Greater body mass was associated with higher sting rates and slower sprinting within sexes, which explained the greater aggression of females (the heavier sex) and, along with longer legs in males, the improved sprint performance in males. These findings suggest females are aggressive to compensate for locomotor costs of reproduction while males possess longer legs to enhance sprinting for predator evasion and mate finding. Sexual dimorphism in the metasoma (“tail”) was unrelated to stinging and sprinting performance and may best be explained by sexual selection.     

Ecomorphological variation in male and female wall lizards and the macroevolution of sexual dimorphism in relation to habitat use

Understanding how phenotypic diversity evolves is a major interest of evolutionary biology. Habitat use is an important factor in the evolution of phenotypic diversity of many animal species. Interestingly, male and female phenotypes have been frequently shown to respond differently to environmental variation. At the macroevolutionary level, this difference between the sexes is frequently analysed using phylogenetic comparative tools to assess variation in sexual dimorphism (SD) across taxa in relation to habitat. A shortcoming of such analyses is that they evaluate the degree of dimorphism itself and therefore they do not provide access to the evolutionary trajectories of each sex. As such, the relative contribution of male and female phenotypes on macroevolutionary patterns of sexual dimorphism cannot be directly assessed. Here, we investigate how habitat use shapes phenotypic diversity in wall lizards using phylogenetic comparative tools to simultaneously assess the tempo and mode of evolution in males, females and the degree of sexual dimorphism. We find that both sexes have globally diversified under similar, but not identical, processes, where habitat use seems to drive macroevolutionary variation in head shape, but not in body size or relative limb length. However, we also observe small differences in the evolutionary dynamics of male and female phenotypes that have a marked impact on macroevolutionary patterns of SD, with important implications for our interpretation of what drives phenotypic diversification within and between the sexes.     

The coevolution of sexual imprinting by males and females

Sexual imprinting is the learning of a mate preference by direct observation of the phenotype of another member of the population. Sexual imprinting can be paternal, maternal, or oblique if individuals learn to prefer the phenotypes of their fathers, mothers, or other members of the population, respectively. Which phenotypes are learned can affect trait evolution and speciation rates. “Good genes” models of polygynous systems predict that females should evolve to imprint on their fathers, because paternal imprinting helps females to choose mates that will produce offspring that are both viable and sexy. Sexual imprinting by males has been observed in nature, but a theory for the evolution of sexual imprinting by males does not exist. We developed a good genes model to study the conditions under which sexual imprinting by males or by both sexes can evolve and to ask which sexual imprinting strategies maximize the fitness of the choosy sex. We found that when only males imprint, maternal imprinting is the most advantageous strategy. When both sexes imprint, it is most advantageous for both sexes to use paternal imprinting. Previous theory suggests that, in a given population, either males or females but not both will evolve choosiness in mating. We show how environmental change can lead to the evolution of sexual imprinting behavior by both sexes in the same population.     

Social flexibility and social evolution in mammals: a case study of the African striped mouse (Rhabdomys pumilio)

Environmental change poses challenges to many organisms. The resilience of a species to such change depends on its ability to respond adaptively. Social flexibility is such an adaptive response, whereby individuals of both sexes change their reproductive tactics facultatively in response to fluctuating environmental conditions, leading to changes in the social system. Social flexibility focuses on individual flexibility, and provides a unique opportunity to study both the ultimate and proximate causes of sociality by comparing between solitary and group-living individuals of the same population: why do animals form groups and how is group-living regulated by the environment and the neuro-endocrine system? These key questions have been studied for the past ten years in the striped mouse Rhabdomys pumilio. High population density favours philopatry and group-living, while reproductive competition favours dispersal and solitary-living. Studies of genetic parentage reveal that relative fitness of alternative reproductive tactics depends on the prevailing environment. Tactics have different fitness under constrained ecological conditions, when competitive ability is important. Under conditions with relaxed ecological constraints, alternative tactics can yield equal fitness. Both male and female striped mice display alternative reproductive tactics based on a single strategy, i.e. all individuals follow the same decision rules. These changes are regulated by endocrine mechanisms. Social flexibility is regarded as an adaptation to unpredictably changing environments, selecting for high phenotypic flexibility based on a broad reaction norm, not on genetic polymorphism for specific tactics.     

Self assessment in insects: honeybee queens know their own strength

Contests mediate access to reproductive opportunities in almost all species of animals. An important aspect of the evolution of contests is the reduction of the costs incurred during intra-specific encounters to a minimum. However, escalated fights are commonly lethal in some species like the honeybee, Apis mellifera. By experimentally reducing honeybee queens' fighting abilities, we demonstrate that they refrain from engaging in lethal contests that typically characterize their reproductive dominance behavior and coexist peacefully within a colony. This suggests that weak queens exploit an alternative reproductive strategy and provides an explanation for rare occurrences of queen cohabitation in nature. Our results further indicate that self-assessment, but not mutual assessment of fighting ability occurs prior to and during the agonistic encounters.     

Sexual Selection,Ontogenetic Acceleration,and Hypermorphosis Generates Male Trimorphism in Wellington Tree Weta

Strong sex-specific selection on traits common to both sexes typically results in sexual dimorphism. Here we find that Wellington tree weta (Hemideina crassidens) are sexually dimorphic in both head shape and size due to differential selection pressures on the sexes: males use their heads in male-male combat and feeding whereas females use theirs for feeding only. Remarkably, the sexes share a common ontogenetic trajectory with respect to head growth. Male head shape allometry is an extension of the female’s trajectory despite maturing two instars earlier, a feat achieved through ontogenetic acceleration and hypermorphosis. Strong sexual selection also favours the evolution of alternative reproductive strategies in which some males produce morphologically different weapons. Wild-caught male H. crassidens are trimorphic with regard to weapon size, a rare phenomenon in nature, and weapon shape is related to each morph’s putative mating strategy.