Male Water Striders Research Articles

Hot males: thermal biology of males and females during coercive mating in water striders Gerris lacustris

Sexual conflict theory predicts that males that adopt coercive mating strategies impose costs to females during copulation. Nevertheless, conflicting mating strategies may also affect males, although such effects on males are often neglected in the literature. Here, we seek to understand whether male water striders (Gerris lacustris) experience higher body temperatures than females during coercive mating behavior. We we explored whether the water temperature affected male and female body temperature differently, considering that water contact by females might serve as a thermal regulator. We built generalized linear mixed models considering the male and female temperature as the dependent variables. Air temperature (as a proxy for solar radiation), water temperature, and sex were used as predictor variables. Our results suggest that males are warmer than females, and despite females coming into contact with water during skimming, this contact does not significantly contribute to lowering their body temperature or improving thermoregulation under the observed conditions. These findings provide novel insights into the thermal biology of water striders. Future studies should focus on addressing whether warmer temperatures confer some advantages to males, such as increased mobility and better ability to hold onto females or impose physiological constraints and fitness costs.

Plasticity of Mating Duration in Response to Slightly Biased Operational Sex Ratios in the Water Strider (Aquarius remigis): The Effect of Cohabitation Under Standard Laboratory Conditions

In polygynandrous species, males face the trade-off between the pursuit of increased mating opportunities and securing paternity. Within such systems, males need to accurately assess the social composition of the local environment to maximize fitness. Here, we investigated this capability in the water strider (Aquarius remigis), a semi-aquatic insect known to exhibit a broad spectrum of mating behaviors and inhabit a socially diverse and changing environment. Using a combination of methodological designs to track both within- and between-subject effects, individuals remained in same-sex housing prior to being exposed to slightly biased operational sex ratios (2:1 vs. 1:2) with or without prior cohabitation to determine the effects on mating duration. Results show that males were sensitive to these subtle differences in social conditions, mating for longer periods within male-biased environments, but this was true only under conditions with prior cohabitation. In particular, when individuals could acclimate to the testing environment, mating duration dropped precipitously in female-biased conditions. These findings do not support the view that male water striders have consistent behavioral syndromes, and instead show that individuals are able to differentiate between, and adaptively respond to, small changes in the local sex ratio. In addition to improving our understanding of the plasticity of male mating behavior in this species, this study offers new insights for future laboratory research studying reproductive competition across a diverse range of polygynandrous animals.

Correlational selection on personality and social plasticity: morphology and social context determine behavioural effects on mating success.

Despite a central line of research aimed at quantifying relationships between mating success and sexually dimorphic traits (e.g., ornaments), individual variation in sexually selected traits often explains only a modest portion of the variation in mating success. Another line of research suggests that a significant portion of the variation in mating success observed in animal populations could be explained by correlational selection, where the fitness advantage of a given trait depends on other components of an individual's phenotype and/or its environment. We tested the hypothesis that interactions between multiple traits within an individual (phenotype dependence) or between an individual's phenotype and its social environment (context dependence) can select for individual differences in behaviour (i.e., personality) and social plasticity. To quantify the importance of phenotype- and context-dependent selection on mating success, we repeatedly measured the behaviour, social environment and mating success of about 300 male stream water striders, Aquarius remigis. Rather than explaining individual differences in long-term mating success, we instead quantified how the combination of a male's phenotype interacted with the immediate social context to explain variation in hour-by-hour mating decisions. We suggest that this analysis captures more of the mechanisms leading to differences in mating success. Males differed consistently in activity, aggressiveness and social plasticity. The mating advantage of these behavioural traits depended on male morphology and varied with the number of rival males in the pool, suggesting mechanisms selecting for consistent differences in behaviour and social plasticity. Accounting for phenotype and context dependence improved the amount of variation in male mating success we explained statistically by 30-274%. Our analysis of the determinants of male mating success provides important insights into the evolutionary forces that shape phenotypic variation. In particular, our results suggest that sexual selection is likely to favour individual differences in behaviour, social plasticity (i.e., individuals adjusting their behaviour), niche preference (i.e., individuals dispersing to particular social conditions) or social niche construction (i.e., individuals modifying the social environment). The true effect of sexual traits can only be understood in interaction with the individual's phenotype and environment.

Do social partners affect same-sex sexual behaviour in male water striders?

Same-sex sexual behaviour (SSB) represents an emergent trait of two interacting same-sex individuals. Although empirical studies have investigated how social environments can influence SSB, little is known about the effect of the interacting partner and its associated phenotype on SSB. In species where females are larger than males or males express male-specific behaviour, a male's morphology or behaviour can serve as a way for other males to recognize its sex and express SSBs. Here we used both a trait-based and variance-partitioning approach to test for the effect of the interacting male's identity and his multivariate phenotype on SSB, using water striders, Gerris lacustris, as a model. We repeatedly subjected males to dyadic interactions with the same and different partners and measured their SSBs. We used the variance-partitioning approach to estimate the partner's identity effect, and the trait-based approach to assess which trait of the partner explains changes in SSB. We found that the partner's SSB reduced the tendency of males to show SSB. SSB was affected by their interacting partner's identity, but the partner effect was not due to the repeatable components ('personality') of the partner's SSB. Males also did not differ in their responses to variation in the partner's SSB at different levels (between-partner, or partner 'personality', and within-partner levels, or partner 'plasticity'). Taken together, these findings provide the first empirical evidence that SSB can be plastically expressed in response to traits in social partners. We also highlight the usefulness of combining the trait-based and variance-partitioning approach to test whether partners represent a component of the social environment affecting the expression of labile traits. (C) 2016 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

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.

Mate disruption in the water strider Aquaris remigis Say, 1832 (Hemiptera: Gerridae)

This report describes the behaviour of a previously uncharacterised mating tactic amongst male water striders (Aquarius remigis Say, 1832), involving the physical break up of existing mating pairs. Using data from four separate laboratory observations on the water strider mating system, we show that this behaviour represents roughly 12.6% of all mating attempts by males. Furthermore, we demonstrate that males are successful in breaking up the existing mating pair in 15.6% of the cases, resulting in secure matings with the disrupted female 6.2% of time. We suspect that mate disruption may serve as an alternative means for acquiring mates by males with low mating success using conventional behaviours. Further research should be performed to determine the prevalence of this behaviour in various natural populations and the specific contexts in which this behaviour occurs.

Correlational selection does not explain the evolution of a behavioural syndrome

Correlated suites of behaviours, or behavioural syndromes, appear to be widespread, and yet few studies have explored how they arise and are maintained. One possibility holds that correlational selection can generate and maintain behavioural syndrome if certain behavioural combinations enjoy greater fitness than other combinations. Here we test this correlational selection hypothesis by comparing behavioural syndrome structure with a multivariate fitness surface based on reproductive success of male water striders. We measured the structure of a behavioural syndrome including dispersal ability, exploration behaviour, latency to remount and sex recognition sensitivity in males. We then measured the relationship between these behaviours and mating success in a range of sex ratio environments. Despite the presence of some significant correlational selection, behavioural syndrome structure was not associated with correlational selection on behaviours. Although we cannot conclusively reject the correlational selection hypothesis, our evidence suggests that correlational selection and resulting linkage disequilibrium might not be responsible for maintaining the strong correlations between behaviours. Instead, we suggest alternative ways in which this behavioural syndrome may have arisen and outline the need for physiological and quantitative genetic tests of these suggestions.

Evolution of individual variation in behaviour and behavioural plasticity under scramble competition

In scramble competition mating systems, individual behaviours related to male–male competition are expected to be plastic across sociosexual environments. However, the evolutionary forces that shape individual differences in behavioural plasticity remain poorly understood. We measured behaviour associated with scramble competition in male water striders, Tenagogerris euphrosyne, in two social contexts. Male T. euphrosyne tend to mount other individuals or pairs indiscriminately and then dismount if their target is either another male or a mating pair. We measured the speed with which a focal male dismounted (i.e. his sensitivity to having made an inappropriate mounting) in each of these contexts. We quantified temporal consistency of dismount speed within each context, as well as individual variation in behavioural plasticity across contexts. We then estimated the effect of the behaviour and of plasticity on individual fitness in different sex ratio conditions. We found that individuals differed in their recognition sensitivity traits, and also in how plastic their sensitivity (i.e. dismount speed) was to context (mating status or sex). When we measured the mating success of each male within experimental groups kept at four different sex ratios, recognition sensitivity traits in both contexts interacted to influence mating success, and there were significant differences in linear selection on sensitivity traits between sex ratio treatments. We discuss how insensitive males evolve, and how individual variation in behavioural plasticity could be maintained by selection or environmental variability.

Overwinter survival depends on immune defence and body length in male Aquarius najas water striders

Winter survival oforganisms has a crucial effecton theirfitness in a seasonal environment. We tested whether overwinter survival of male water striders, Aquarius najas (De Geer) (Heteroptera: Gerridae), is associated with the time of season they leave the water for winter diapause. This was performed by comparing parameters of males leaving the water at the beginning of autumn and 1 monthlater. Theresults show significantlyhigher overwintersurvivalin males ofthe early diapausinggroup.Theywere foundto be larger than late diapausing individuals. Overall, overwintersurvival was found to be associated with body length. The strength of immune defence measured as encapsulation response against nylon monofilament appeared to be stronger in the early than in the late diapausing group. Body length had an effect on the encapsulation rates of water striders, with larger males having a stronger encapsulation response. The amount oflipids was larger in males of the early diapausing group, and the relationship between body length and absolute lipid reserves was positive in both groups. However, a correlation between body reserves and body length was not found when lipid content was expressed as a proportion oftotal body weight. The results suggest that body length isthemainvariablelinkingoverwintersurvivalandresistanceagainstpathogensandparasitoids.This studyshows that differences in resistance can explain differential winter survival of larger and smaller A. najaswater striders.

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.

Population structure influences sexual conflict in wild populations of water striders

In sexual conflict, aggressive males frequently diminish the long-term reproductive success of females in efforts to gain a short-term advantage over rival males. This short-term advantage can selectively favour high-exploitation males. However, just as the over-exploitation of resources can lead to local extinction, the over-exploitation of females in the form of harassment by aggressive males can yield similar consequences resulting in reduced female fecundity, increased female mortality and overall decline in mating activity. This outcome may often be prevented by selection acting at multiple levels of biological organization. Directional selection favouring aggressive exploitation within groups can be balanced by directional selection amongst groups opposing exploitation. Such between-group selection has recently been demonstrated in laboratory studies of water striders, where the conditional dispersal of individuals increased variation amongst groups and influenced the balance of selection toward reduced male aggression. This multilevel selection (MLS) framework also provides predictive value when investigating natural populations differing in their relative strength of selection within versus among groups. For water striders, the consequences of local exploitation cause fitness differences between groups, favouring less aggressive males. Inconsistently flowing ephemeral streams consist of isolated pools that prevent aggressive male water striders from escaping the consequences of local exploitation. We, therefore, predicted that inconsistently flowing ephemeral streams would favour the evolution of less aggressive males than would perennial streams, which allow aggressive males to move more freely and to escape the group-level costs of their aggression. Comparing two neighbouring streams during the mating season, we found that males dispersed naturally between pools at much higher rates in the perennial stream than in the ephemeral stream. As predicted, we found that males from the perennial stream were significantly more aggressive than those from the ephemeral stream. We also found that dispersers were significantly more aggressive than non-dispersers within each stream. These field results illustrate the relevance of the MLS framework in our understanding of the evolution of sexual conflict.

Role of body size in dominance interactions between male water striders, Aquarius paludum

Water striders are a model system for the study of sexual size dimorphism, but the effect of body size on the dominance relationship between individuals has not been experimentally tested. In 34 staged contests between males of the water strider Aquarius paludum, we determined the effect of body size difference between contestants on the outcome of the aggressive interactions. In contests between a large and a small male, the larger individuals won the interactions significantly more often than expected by chance. This is the first experimental evidence for the importance of body size in pair-wise contests among water striders.

Aggressive mating as a tragedy of the commons in the water strider Aquarius remigis

The tragedy of the commons usually refers to the overexploitation of resources such as food or water. Here, we show in a laboratory study that competition among males for females can also result in a tragedy of the commons’ situation. Male water striders (Aquarius remigis) vary widely in their aggressiveness toward pursuing females. The most aggressive males prevent females from feeding and cause them to leave the water surface, where they are unavailable to all males. Groups of nonaggressive males are collectively three times more fit than groups of hyperaggressive males, but hyperaggressive males are more successful than nonaggressive males within mixed groups. This is the classic tragedy of the commons’ situation, and it is likely to occur in many species that exhibit sexual conflict. We have also shown that individual differences in male aggression are stable across time and are not influenced by food or light regime, although all individuals become nonaggressive in the presence of fish predators.

THE FORM OF SEXUAL SELECTION ON MALE GENITALIA CANNOT BE INFERRED FROM WITHIN-POPULATION VARIANCE AND ALLOMETRY?A CASE STUDY IN AQUARIUS REMIGIS

Male genital morphology in insects and arachnids is characterized by static hypoallometry and low intrapopulational levels of phenotypic variation relative to other male traits. The one-size-fits-all model of genital evolution attributes these patterns to stabilizing sexual selection. This model relies on the assumption that the observed patterns of variation and allometry reflect the form of sexual selection acting these traits. We test this by examining the patterns of scaling and trait variation for a set of genitalic and somatic morphological traits in male water striders (Aquarius remigis). This suite of traits is of particular interest because previous work has shown that the genitalic traits are under strong directional selection whereas the somatic traits are under either weak directional or stabilizing selection. Because the selection regime for these traits is known, we can, for the first time, test the purported relationship between trait variation, scaling, and the form of sexual selection. We show that the patterns of variation and scaling of these traits differ sharply from those predicted for traits experiencing strong directional sexual selection. Specifically, the male genital structures show static hypoallometry and low intrapopulational levels of phenotypic variation relative to other male traits, in spite of consistent, strong, directional sexual selection. These scaling relationships and levels of variation are typical of genital traits in other insect species, where they have been presumed to reflect stabilizing sexual selection. Our data clearly refute the assumption of the one-size-fits-all hypothesis that hypoallometric scaling of genitalic traits implies stabilizing selection. We discuss the implications of this finding and propose future directions for improving our current understanding of genital evolution in arthropods.

Fishing spiders, green sunfish, and a stream-dwelling water strider: male-female conflict and prey responses to single versus multiple predator environments.

Many studies have experimentally addressed the effects of a particular predator species on prey behavior. In nature, however, prey frequently face multiple species of predators that often vary in their predatory mode and in their level of predation risk. Relatively few studies have considered prey responses under these complex conditions. In Kentucky, the stream-dwelling water strider (Aquariusremigis) coexists with many potentially dangerous predators, two of which are the green sunfish (Lepomiscyanellus) and the fishing spider (Dolomedesvittatus). Green sunfish occupy stream pools and attack water striders from below. In contrast, fishing spiders hunt along stream shorelines where they perch on overhanging vegetation or rocks and attack water striders near shore. We compared how A. remigis individuals respond to these two very different predators in pools with one or both predators. The presence of sunfish in pools had strong effects on male water strider behavior, including increased use of three types of refuge from sunfish (riffles, climbing out of the water, sitting on the water but at the edges of pools), decreased activity and a decreased number of aggressive males on the water. Spiders also influenced water strider behavior; male water striders avoided spiders by shifting away from the edges of pools. Comparisons of the effects of the two predator species showed that in general, antipredator responses by male water striders were stronger in pools with fish alone than in those with spiders alone. In the presence of both predators, male water strider behavior (microhabitat use and activity) was generally similar to behavior in the presence of fish alone. In contrast, female water striders showed no significant response to the presence of sunfish, and little response to the presence of spiders. This lack of response could be because females spent much of their time in refuges even in the absence of predators (apparently hiding from harassment by males). Both spiders and fish caused decreases in water strider mating activity. The presence of fish reduced both the number of matings per pool (mating frequency), and mean mating durations. Spiders induced a decrease in mean mating duration, but not in mating frequency. The largest reductions in mating activity occurred in pools with both predators present. Pools with either spiders or fish alone suffered 15-20% water strider mortality during our experiment (versus no mortality in predator-free pools). Extant theory suggests that when prey face conflicting microhabitat responses to two predators (as in this study), the predators should have facilitative effects on predation rates (i.e., prey that avoid one predator are often killed by the other and vice versa). Mortality rates in pools with both predators present, however, were not significantly different from that predicted by a null model of multiple predator effects. The lack of predator facilitation can be explained by the compensatory reductions in water strider activity and mating activity in the presence of both predators.

Monopolization in a resource queue: water striders competing for food and mates

The monopolization of resources plays an important theoretical role in the literature on competition for food and mates. We used 12 groups of male water striders (Aquariusremigis) to: (1) test the general prediction that monopolization of both food and mates decreases as the temporal clumping of resources increases, (2) compare the efficiency of two indices of resource monopolization, coefficient of variation and Q (Ruzzante et al. 1996), and (3) quantitatively assess the resource queue model of Blanckenhorn and Caraco (1992). Each group of six males competed for both food items and mates released from the upstream end of a laboratory stream. The mean inter-arrival time for resource units (food or females) was 10 min, with four levels of temporal clumping (variance in inter-arrival time: 0, 25, 50 or 320 min2). As predicted, the monopolization of both food and mates decreased as the temporal clumping of resource arrival increased, although monopolization was greater for food than for mates. Q detected the difference in monopolization of food and mates, whereas the coefficient of variation did not, because Q is independent of mean resource abundance. The resource queue model successfully predicted monopolization of both resource types, explaining 89% and 76% of variation in the proportion of food and mates acquired by the six males. The success of the model suggests that the scaling of handling time to the variance in resource inter-arrival time should play an important role in any general theory of resource monopolization.

Mate choice by male water striders (Gerris lacustris): expression of a wing morph preference depends on a size difference between females

Mate choice by male water striders (<i>Gerris lacustris</i>): expression of a wing morph preference depends on a size difference between females

Predation risk, food deprivation and non-random mating by size in the stream water strider, Aquarius remigis

Non-random mating by size (NRMS) plays a central role in the study of sexual selection and the evolution of mating systems. Theory suggests that NRMS should be influenced by conflicting demands (e.g., predation risk, hunger); few experimental studies, however, have addressed these effects. We used a factorial experiment to examine the influence of predatory green sunfish and food deprivation on NRMS in male and female stream water striders, Aquarius remigis. As predicted by theory, food deprivation decreased the large-male mating advantage. The influence of predation risk, however, went against existing theory; that is, risk increased the large male mating advantage. The degree of large-male mating advantage was negatively related to a measure of the rate of male harassment of females. A behavioral mechanism that can explain these patterns emphasizes the contrasting effects of different competing demands on male harassment rates, female resistance and the role of male size in overcoming female resistance. Females usually resist male mating attempts. Successful mating occurs when males overcome female resistance. If harassment rates (of females by males) are low, larger males have a mating advantage over smaller males perhaps because females resist heavily and thus only larger males can overcome female resistance. If, however, male harassment rates are very high, female resistance might be swamped; mating should then be more random with respect to male size. Food deprivation increases gerrid activity and thus increases harassment rates which should then reduce NRMS. In contrast, risk decreases gerrid activity, thus decreasing harassment rates and increasing NRMS. Females did not show significant NRMS. Females did, however, show a pattern of change in NRMS that is consistent with male choice for larger females.

Avoidance of Male Giant Water Striders By Females

Shifts in behaviour and microhabitat preference were exhibited by female giant water striders (G. remigis) when males were experimentally introduced into and removed from wading pools containing females. In the presence of males, females became significantly less active, interacted with one another less, spent less time in open water, and spent more time out of the water away from females. Furthermore, they resumed their original behaviours once males were removed. It is potentially advantageous for females to avoid male harassment due to costs associated with such interactions.

Resource Acquisition and Alternative Mating Strategies in Water Striders

Behavioral polymorphisms occur among male and female water striders, Gems remigis , when competing for food and mates. Individuals of both sexes vie for positions in the fastest flowing portions of streams. Here prey capture rates are highest, as are those of swimming and aggression. Only the largest females, and males with the largest first appendages, can regularly maintain positions in these areas. The remaining females are arranged along the flow gradient according to their size with the smallest holding positions in pools of slow moving water. For the remaining males neither overall size, nor the size of the first appendages, appears to determine which males swim near the edge of streams, or which males swim as satellites behind those occupying the fast flowing productive areas. Preliminary data show that mating success of edge and satellite males are about equal, but significantly less than that of the centrally positioned males with the largest first appendages. Thus although it appears that morphological phenotype influences male competitive behavior, when the absolute size of the critical trait is small males adopt behavior after assessing the actions of others. For these “subordinate” males, behavioral assessment appears to produce an “ideal free” spatial distribution.