Morph-specific life-history correlations in a wing-dimorphic water strider.

Life-history theory predicts a negative correlation between reproduction and survival because individuals differ in their investment in early reproduction at the expense of survival. However, life-history trade-offs can be masked when individual differences in resource allocation are smaller than those in resource acquisition. In polymorphic species, as distinct morphs exhibit differences in intrinsic physiology, the relative effects of resource acquisition and allocation on life-history traits will differ between morphs, contributing to morph-specific life-history correlations. Here, in the wing-dimorphic water strider Aquarius paludum, we found that wing morphs differed in within-morph individual-level life-history correlations. Longer-lived flight-capable long-winged females produced fewer eggs per day and matured later, whereas life-history trade-offs were not observed in short-winged flightless females. The survival-reproduction trade-off observed in long-winged females may be a result of individual differences in the timing of wing muscle histolysis. Individuals that underwent wing histolysis early would have increased reproduction at the expense of a shorter life, whereas individuals with late wing histolysis would have reduced reproduction but a longer life. Short-winged females, who never develop wings, effectively have more resources to allocate to both survival and reproduction, masking any life-history trade-offs. Thus, we suggest that morph-specific effects of resource allocation trade-offs can shape the morph-specific extent of individual variation in life-history strategies, which may contribute to the evolution and maintenance of within-species polymorphism.

Condition-Dependent Mutual Mate Preference and Intersexual Genetic Correlations for Mating Activity.

Although mating represents a mutual interaction, the study of mate preferences has long focused on choice in one sex and preferred traits in the other. This has certainly been the case in the study of the costs and condition-dependent expression of mating preferences, with the majority of studies concerning female preference. The condition dependence and genetic architecture of mutual mate preferences remain largely unstudied, despite their likely relevance for the evolution of preferences and of mating behavior more generally. Here we measured (a) male and female mate preferences and (b) intersexual genetic correlations for the mating activity in pedigreed populations of southern field crickets (Gryllus bimaculatus) raised on a favorable (free-choice) or a stressful (protein-deprived) diet. In the favorable dietary environment, mutual mate preferences were strong, and the intersexual genetic covariance for mating activity was not different from one. However, in the stressful dietary environment, mutual mate preferences were weak, and the intersexual genetic covariance for mating activity was significantly smaller than one. Altogether, our results show that diet environments affect the expression of genetic variation in mating behaviors: when the environment is stressful, both (a) the strength of mutual mate preference and (b) intersexual genetic covariance for mating activity tend to be weaker. This implies that mating dynamics strongly vary across environments.

Multiple biological mechanisms result in correlations between pre- and post-mating traits that differ among versus within individuals and genotypes.

Reproductive traits involved in mate acquisition (pre-mating traits) are predicted to covary with those involved in fertilization success (post-mating traits). Variation in male quality may give rise to positive, and resource allocation trade-offs to negative, covariances between pre- and post-mating traits. Empirical studies have yielded mixed results. Progress is hampered as researchers often fail to appreciate that mentioned biological mechanisms can act simultaneously but at different hierarchical levels of biological variation: genetic correlations may, for example, be negative due to genetic trade-offs but environmental correlations may instead be positive due to individual variation in resource acquisition. We measured pre-mating (aggression, body weight) and post-mating (ejaculate size) reproductive traits in a pedigreed population of southern field crickets (Gryllus bimaculatus). To create environmental variation, crickets were raised on either a low or a high nymphal density treatment. We estimated genetic and environmental sources of correlations between pre- and post-mating traits. We found positive genetic correlations between pre- and post-mating traits, implying the existence of genetic variation in male quality. Over repeated trials of the same individual (testing order), positive changes in one trait were matched with negative changes in other traits, suggesting energy allocating trade-offs within individuals among days. These findings demonstrate the need for research on pre- and post-mating traits to consider the hierarchical structure of trait correlations. Only by doing so was our study able to conclude that multiple mechanisms jointly shape phenotypic associations between pre- and post-mating traits in crickets.

You are what you eat: diet shapes body composition, personality and behavioural stability.

BACKGROUND: Behavioural phenotypes vary within and among individuals. While early-life experiences have repeatedly been proposed to underpin interactions between these two hierarchical levels, the environmental factors causing such effects remain under-studied. We tested whether an individual's diet affected both its body composition, average behaviour (thereby causing among-individual variation or 'personality') and within-individual variability in behaviour and body weight (thereby causing among-individual differences in residual within-individual variance or 'stability'), using the Southern field cricket Gryllus bimaculatus as a model. We further asked whether effects of diet on the expression of these variance components were sex-specific. METHODS: Manipulating both juvenile and adult diet in a full factorial design, individuals were put, in each life-stage, on a diet that was either relatively high in carbohydrates or relatively high in protein. We subsequently measured the expression of multiple behavioural (exploration, aggression and mating activity) and morphological traits (body weight and lipid mass) during adulthood. RESULTS: Dietary history affected both average phenotype and level of within-individual variability: males raised as juveniles on high-protein diets were heavier, more aggressive, more active during mating, and behaviourally less stable, than conspecifics raised on high-carbohydrate diets. Females preferred more protein in their diet compared to males, and dietary history affected average phenotype and within-individual variability in a sex-specific manner: individuals raised on high-protein diets were behaviourally less stable in their aggressiveness but this effect was only present in males. Diet also influenced individual differences in male body weight, but within-individual variance in female body weight. DISCUSSION: This study thereby provides experimental evidence that dietary history explains both heterogeneous residual within-individual variance (i.e., individual variation in 'behavioural stability') and individual differences in average behaviour (i.e., 'personality'), though dietary effects were notably trait-specific. These findings call for future studies integrating proximate and ultimate perspectives on the role of diet in the evolution of repeatedly expressed traits, such as behaviour and body weight.

Sex-dependent expression of behavioural genetic architectures and the evolution of sexual dimorphism.

Empirical studies imply that sex-specific genetic architectures can resolve evolutionary conflicts between males and females, and thereby facilitate the evolution of sexual dimorphism. Sex-specificity of behavioural genetic architectures has, however, rarely been considered. Moreover, as the expression of genetic (co)variances is often environment-dependent, general inferences on sex-specific genetic architectures require estimates of quantitative genetics parameters under multiple conditions. We measured exploration and aggression in pedigreed populations of southern field crickets (Gryllus bimaculatus) raised on either naturally balanced (free-choice) or imbalanced (protein-deprived) diets. For each dietary condition, we measured for each behavioural trait (i) level of sexual dimorphism, (ii) level of sex-specificity of survival selection gradients, (iii) level of sex-specificity of additive genetic variance, and (iv) strength of the cross-sex genetic correlation. We report here evidence for sexual dimorphism in behaviour as well as sex-specificity in the expression of genetic (co)variances as predicted by theory. The additive genetic variances of exploration and aggression were significantly greater in males compared with females. Cross-sex genetic correlations were highly positive for exploration but deviating (significantly) from one for aggression; findings were consistent across dietary treatments. This suggests that genetic architectures characterize the sexually dimorphic focal behaviours across various key environmental conditions in the wild. Our finding also highlights that sexual conflict can be resolved by evolving sexually independent genetic architectures.

Effect of diet on the structure of animal personality.

There is increasing interest in the proximate factors that underpin individual variation in suites of correlated behaviours. In this paper, we propose that dietary macronutrient composition, an underexplored environmental factor, might play a key role. Variation in macronutrient composition can lead to among-individual differentiation in single behaviours ('personality' ) as well as among-individual covariation between behaviours ('behavioural syndromes' ). Here, we argue that the nutritional balance during any life stage might affect the development of syndrome structure and the expression of genes with pleiotropic effects that influence development of multiple behaviours, hence genetic syndrome structure. We further suggest that males and females should typically differ in diet-dependent genetic syndrome structure despite a shared genetic basis. We detail how such diet-dependent multivariate gene-environment interactions can have major repercussions for the evolution of behavioural syndromes.

Long-term effect of social interactions on behavioral plasticity and lifetime mating success.

Behavioral traits often change over an individual's lifetime. Experience, physiological senescence, and age-dependent differences in optimal behavior can, in theory, all cause longitudinal behavioral changes. Yet most studies of behavioral plasticity and selection on behavior focus on short-term population-level responses to social factors such as conspecific density or sex ratio. Longer-term effects of social interactions on individual behavior have rarely been tested. Here we tested these effects by exposing male water striders (Hemiptera: Gerridae) to two different social conditions throughout their lifetime; we call these the nonsocial and social treatments. We then measured each male's lifetime mating success and individual behavioral plasticity by observing four different behaviors (exploring a novel environment, dispersal ability, sex-recognition sensitivity, and tendency to remount a resistant female after being dislodged) every 2 weeks. The social environment influenced individual variation in behavioral plasticity as well as population-level behavioral plasticity. Moreover, when we calculated linear selection gradients of individual behavioral traits and their plasticities on lifetime mating success, male remounting tendency and individual plasticity in exploration ability were likely to be the most important factors explaining variation in male lifetime mating success. In conclusion, the variation in social interactions throughout an individual's lifetime contributes to the individual variation in behavioral plasticity, which can significantly affect a male's lifetime fitness.

Activity-aggression behavioural syndromes exist in males but not in females of the field cricket Teleogryllus emma.

Previous studies on sex differences in behaviour have largely focused on differences in average behaviours between sexes. However, males and females can diverge not only in average behaviours but also in the direction of behavioural correlations at the individual level (i.e. behavioural syndromes). Behavioural syndromes, with their potential to constrain the independent evolution of behaviours, may play a role in shaping sex-specific responses to selection and contributing to the development of sex differences in behaviour. Despite the pivotal role of behavioural syndromes in the evolution of sexual dimorphism in behaviour, robust empirical evidence of sex differences in behavioural syndromes based on repeated measurements of behaviours is scarce. In this study, we conducted repeated measurements of activity and aggression in male and female field crickets Teleogryllus emma, providing evidence of sex differences in the existence of behavioural syndromes. Males exhibited a significantly positive behavioural syndrome between activity and aggression, whereas females, in contrast, did not show any aggressive behaviour, resulting in the absence of such a syndrome. The sex differences in the existence of the activity-aggression behavioural syndromes in this species could be attributed to differences in selection. Selection favouring more active and aggressive males may have shaped a positive activity-aggression behavioural syndrome in males, whereas the absence of selection favouring female aggression may have resulted in the absence of aggression and the related behavioural syndrome in females. However, given the plasticity of behaviour with changes in age or the environment, further research is needed to explore how sex differences in the existence of activity-aggression behavioural syndromes change across contexts. Furthermore, understanding the genetic underpinning of sex differences in a behavioural syndrome would be pivotal to assess the role of behavioural syndromes in the evolution of sexual dimorphism in behaviours.

Polyandrous females but not monogamous females vary in reproductive ageing patterns in the bean bug Riptortus pedestris.

BACKGROUND: In general, reproductive performance exhibits nonlinear changes with age. Specifically, reproductive performance increases early in life, reaches a peak, and then declines later in life. Reproductive ageing patterns can also differ among individuals if they are influenced by individual-specific strategies of resource allocation between early-life reproduction and maintenance. In addition, the social environment, such as the number of available mates, can influence individual-specific resource allocation strategies and consequently alter the extent of individual differences in reproductive ageing patterns. That is, females that interact with more partners are expected to vary their copulation frequency, adopt a more flexible reproductive strategy and exhibit greater individual differences in reproductive ageing patterns. METHODS: In this study, we evaluated the effect of mating with multiple males on both group- and individual-level reproductive ageing patterns in females of the bean bug Riptortus pedestris by ensuring that females experienced monogamous (one female with one male) or polyandrous conditions (one female with two males). RESULTS: We found that group-level reproductive ageing patterns did not differ between monogamy-treatment and polyandry-treatment females. However, polyandry-treatment females exhibited among-individual variation in reproductive ageing patterns, while monogamy-treatment females did not. CONCLUSION: Our findings provide the first empirical evidence regarding the influence of the social environment on individual variation in reproductive ageing patterns. We further suggest that the number of potential mates influences group- and individual-level reproductive ageing patterns, depending on which sex controls mating. We encourage future studies to consider interactions between species-specific mating systems and the social environment when evaluating group- and individual-level reproductive ageing patterns.

Size-assortative mating and sexual size dimorphism are predictable from simple mechanics of mate-grasping behavior.

BACKGROUND: A major challenge in evolutionary biology is to understand the typically complex interactions between diverse counter-balancing factors of Darwinian selection for size assortative mating and sexual size dimorphism. It appears that rarely a simple mechanism could provide a major explanation of these phenomena. Mechanics of behaviors can predict animal morphology, such like adaptations to locomotion in animals from various of taxa, but its potential to predict size-assortative mating and its evolutionary consequences has been less explored. Mate-grasping by males, using specialized adaptive morphologies of their forelegs, midlegs or even antennae wrapped around female body at specific locations, is a general mating strategy of many animals, but the contribution of the mechanics of this wide-spread behavior to the evolution of mating behavior and sexual size dimorphism has been largely ignored. RESULTS: Here, we explore the consequences of a simple, and previously ignored, fact that in a grasping posture the position of the male's grasping appendages relative to the female's body is often a function of body size difference between the sexes. Using an approach taken from robot mechanics we model coercive grasping of females by water strider Gerris gracilicornis males during mating initiation struggles. We determine that the male optimal size (relative to the female size), which gives the males the highest grasping force, properly predicts the experimentally measured highest mating success. Through field sampling and simulation modeling of a natural population we determine that the simple mechanical model, which ignores most of the other hypothetical counter-balancing selection pressures on body size, is sufficient to account for size-assortative mating pattern as well as species-specific sexual dimorphism in body size of G. gracilicornis. CONCLUSION: The results indicate how a simple and previously overlooked physical mechanism common in many taxa is sufficient to account for, or importantly contribute to, size-assortative mating and its consequences for the evolution of sexual size dimorphism.

Density-dependent sex-biased development of macroptery in a water strider.

In wing-polymorphic insects, wing morphs differ not only in dispersal capability but also in life history traits because of trade-offs between flight capability and reproduction. When the fitness benefits and costs of producing wings differ between males and females, sex-specific trade-offs can result in sex differences in the frequency of long-winged individuals. Furthermore, the social environment during development affects sex differences in wing development, but few empirical tests of this phenomenon have been performed to date. Here, I used the wing-dimorphic water strider Tenagogerris euphrosyne to test how rearing density and sex ratio affect the sex-specific development of long-winged dispersing morphs (i.e., sex-specific macroptery). I also used a full-sib, split-family breeding design to assess genetic effects on density-dependent, sex-specific macroptery. I reared water strider nymphs at either high or low densities and measured their wing development. I found that long-winged morphs developed more frequently in males than in females when individuals were reared in a high-density environment. However, the frequency of long-winged morphs was not biased according to sex when individuals were reared in a low-density environment. In addition, full-sib males and females showed similar macroptery incidence rates at low nymphal density, whereas the macroptery incidence rates differed between full-sib males and females at high nymphal density. Thus complex gene-by-environment-by-sex interactions may explain the density-specific levels of sex bias in macroptery, although this interpretation should be treated with some caution. Overall, my study provides empirical evidence for density-specific, sex-biased wing development. My findings suggest that social factors as well as abiotic factors can be important in determining sex-biased wing development in insects.

Measurement of the thermal conductivity of a water-based single-wall carbon nanotube colloidal suspension with a modified 3- omega method.

A modified 3-omega method applied to a suspended platinum microwire was employed to measure the thermal conductivity and convective heat transfer coefficient of a water-based single-walled carbon nanotube (CNT) solution (metallic single-wall nanotubes with 1.33 nm diameter and 1.14 wt% concentration), and an expression for calculating the convective heat transfer coefficient in such a free convective fluid was introduced. The measurement technique was validated for three model systems including vacuum, air and deionized water. It is found that there is excellent agreement between these three model systems with theoretical predictions. In addition, the frequency dependence on the third harmonic response measured in deionized water reveals the existence of a very low working frequency below 60 mHz. The thermal conductivity and convective heat transfer coefficient of the nanofluid (water-based single-wall CNT solution) were determined to be 0.73 +/- 0.013 W m(-1) K(-1) and 14 900 +/- 260 W m(-2) K(-1), respectively, which correspond to an enhancement of 19.4% in thermal conductivity and 18.9% in convective heat transfer as compared to water.

Protein deprivation facilitates the independent evolution of behavior and morphology.

Ecological conditions such as nutrition can change genetic covariances between traits and accelerate or slow down trait evolution. As adaptive trait correlations can become maladaptive following rapid environmental change, poor or stressful environments are expected to weaken genetic covariances, thereby increasing the opportunity for independent evolution of traits. Here, we demonstrate the differences in genetic covariance among multiple behavioral and morphological traits (exploration, aggression, and body weight) between southern field crickets (Gryllus bimaculatus) raised in favorable (free-choice) versus stressful (protein-deprived) nutritional environments. We also quantify the extent to which differences in genetic covariance structures contribute to the potential for the independent evolution of these traits. We demonstrate that protein-deprived environments tend to increase the potential for traits to evolve independently, which is caused by genetic covariances that are significantly weaker for crickets raised on protein-deprived versus free-choice diets. The weakening effects of stressful environments on genetic covariances tended to be stronger in males than in females. The weakening of the genetic covariance between traits under stressful nutritional environments was expected to facilitate the opportunity for adaptive evolution across generations. Therefore, the multivariate gene-by-environment interactions revealed here may facilitate behavioral and morphological adaptations to rapid environmental change.

Increased female resistance to mating promotes the effect of mechanical constraints on latency to pair.

Size-assortative mating, defined as a positive linear association of body size between members of mating pairs, can arise from mechanical constraints on pairing efficiency, particularly when mating success is affected by males' mate-grasping force. In this context, female resistance is predicted to have an important role in changing the threshold force necessary for males to hold females, thereby contributing to the effect of mechanical constraints. Thus, increased female resistance is expected to increase the paring success of an optimally sized male relative to the female body size (sexual size ratio = male body size/female body size = 0.86), which leads to positive size-assortative mating. However, very little is known about the extent to which female resistance affects mechanical constraints on mate grasping. Here, using the water strider Gerris gracilicornis (Hemiptera: Gerridae), we tested whether the level of female resistance affected the relationship between the sexual size ratio and latency to pair. We found that optimally sized males mated sooner than other males when females resisted a male's mating attempts. When females did not resist, an effect of sexual size ratio on latency to pair was not found. Our results thus imply that increased female resistance to male mating attempts may strengthen the pattern of size-assortative mating. We provide clear empirical evidence that female resistance to mating influences the effect of mechanical constraints on size-assortative mating under sexual conflict. This result further suggests that patterns of size-assortative mating can be altered by a variety of ecological circumstances that change female resistance to mating in many other animal species under sexual conflict.

Increased developmental density decreases the magnitude of indirect genetic effects expressed during agonistic interactions in an insect.

The expression of aggression depends not only on the direct genetic effects (DGEs) of an individual's genes on its own behavior, but also on indirect genetic effects (IGEs) caused by heritable phenotypes expressed by social partners. IGEs can affect the amount of heritable variance on which selection can act. Despite the important roles of IGEs in the evolutionary process, it remains largely unknown whether the strength of IGEs varies across life stages or competitive regimes. Based on manipulations of nymphal densities and > 3000 pair-wise aggression tests across multiple life stages, we experimentally demonstrate that IGEs on aggression are stronger in field crickets (Gryllus bimaculatus) that develop at lower densities than in those that develop at higher densities, and that these effects persist with age. The existence of density-dependent IGEs implies that social interactions strongly determine the plastic expression of aggression when competition for resources is relaxed. A more competitive (higher density) rearing environment may fail to provide crickets with sufficient resources to develop social cognition required for strong IGEs. The contribution of IGEs to evolutionary responses was greater at lower densities. Our study thereby demonstrates the importance of considering IGEs in density-dependent ecological and evolutionary processes.

Individuality in nutritional preferences: a multi-level approach in field crickets.

Selection may favour individuals of the same population to differ consistently in nutritional preference, for example, because optimal diets covary with morphology or personality. We provided Southern field crickets (Gryllus bimaculatus) with two synthetic food sources (carbohydrates and proteins) and quantified repeatedly how much of each macronutrient was consumed by each individual. We then quantified (i) whether individuals were repeatable in carbohydrate and protein intake rate, (ii) whether an individual's average daily intake of carbohydrates was correlated with its average daily intake of protein, and (iii) whether short-term changes in intake of carbohydrates coincided with changes in intake of protein within individuals. Intake rates were individually repeatable for both macronutrients. However, individuals differed in their relative daily intake of carbohydrates versus proteins (i.e., 'nutritional preference'). By contrast, total consumption varied plastically as a function of body weight within individuals. Body weight-but not personality (i.e., aggression, exploration behaviour)-positively predicted nutritional preference at the individual level as large crickets repeatedly consumed a higher carbohydrate to protein ratio compared to small ones. Our finding of level-specific associations between the consumption of distinct nutritional components demonstrates the merit of applying multivariate and multi-level viewpoints to the study of nutritional preference.

Insects perceive local sex ratio in the absence of tactile or visual sex-specific cues.

Numerous studies have demonstrated adaptive behavioral responses of males and females to changes in operational sex ratio (the ratio of potentially receptive males to receptive females; OSR), and theory often assumes that animals have perfect instantaneous knowledge about the OSR. However, the role of sensory mechanisms in monitoring the local sex ratio by animals and whether animals can perceive local sex ratio in a manner consistent with model assumptions have not been well addressed. Here, we show that mating water striders Gerris gracilicornis respond to local sex ratio even when visual and physical contact with other individuals were experimentally prohibited. Our study shows that insects are able to estimate local population's sex ratio and adjust their behavior based on nonvisual cues perceived at a distance or released to the habitat. Hence, the frequent theoretical assumption that individuals have knowledge about their local sex ratio regardless of their direct behavioral interactions may be an acceptable approximation of reality.

Male water striders attract predators to intimidate females into copulation.

Despite recent advances in our understanding of sexual conflict and antagonistic coevolution between sexes, the role of interspecific interactions, such as predation, in these evolutionary processes remains unclear. In this paper, we present a new male mating strategy whereby a male water strider Gerris gracilicornis intimidates a female by directly attracting predators as long as she does not accept the male's coercive copulation attempt. We argue that this male strategy is a counteradaptation to the evolution of the female morphological shield protecting her genitalia from coercive intromission by water strider males. The G. gracilicornis mating system clearly represents an effect expected from models of the coevolutionary arms race between sexes, whereby one sex causes a decrease in the fitness component of the other sex. Moreover, our study demonstrates a crucial role that interspecific interactions such as predation can have in the antagonistic coevolution between sexes.

Female genitalia concealment promotes intimate male courtship in a water strider.

Violent coercive mating initiation is typical for animals with sexual conflict over mating. In these species, the coevolutionary arms-race between female defenses against coercive mating and male counter-adaptations for increased mating success leads to coevolutionary chases of male and female traits that influence the mating. It has been controversial whether one of the sexes can evolve traits that allow them to "win" this arms race. Here, we use morphological analysis (traditional and scanning electron micrographs), laboratory experiments and comparative methods to show how females of a species characterized by typical coercive mating initiation appear to "win" a particular stage of the sexual conflict by evolving morphology to hide their genitalia from direct, forceful access by males. In an apparent response to the female morphological adaptation, males of this species added to their typically violent coercive mounting of the female new post-mounting, pre-copulatory courtship signals produced by tapping the water's surface with the mid-legs. These courtship signals are intimate in the sense that they are aimed at the female, on whom the male is already mounted. Females respond to the signals by exposing their hidden genitalia for copulatory intromission. Our results indicate that the apparent victory of coevolutionary arms race by one sex in terms of morphology may trigger evolution of a behavioral phenotype in the opposite sex.