A behavioural syndrome in the field cricket Gryllus integer: intrasexual aggression is correlated with activity in a novel environment

Behavioural syndromes, or suites of correlated behaviours across different contexts and situations, have recently drawn attention from evolutionary biologists. In the field cricket Gryllus integer , males are aggressive with one another and fight vigorously over females and territories. We examined whether aggressiveness with other males was correlated with activity in a potentially dangerous context (a novel environment) in laboratory-raised virgin males. Aggressiveness was measured as fighting ability against a weight-matched opponent. First, we measured each cricket's latency to become active in a novel environment and latency to emerge from a refuge within a novel environment. Next, we determined which of two weight-matched males was more aggressive, by pitting the males together in an agonistic contest and counting the number of fights won by each male. More aggressive males, who won more fights, had shorter latencies to become active when placed in a novel environment and shorter latencies to emerge from a safe refuge. These results suggest that a behavioural syndrome exists in G. integer , in which more aggressive males are also more active in general, and possibly less cautious towards predation risk.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 475–482.     

Why do females find ornaments attractive? The coercion‐avoidance hypothesis

Vertebrates show two major classes of sexually dimorphic traits: weaponry and ornaments. However, Darwin could not explain why their expression varies so much across lineages. We argue that coercion-avoidance can explain both the existence and taxonomic distribution of ornaments. Females maximize their fitness when they can freely choose their mates, but males are expected to use sexually dimorphic weaponry not only to displace other males, but also to overcome female preferences and thus acquire matings by force whenever they can. Females should therefore avoid coercive males and avoid using weaponry as a criterion for male quality wherever possible, and rely on male viability indicators that cannot be used to coerce females (i.e. ornaments). Ornaments predominate in birds and weaponry in mammals because female choice is less costly in birds, due to higher intrinsic female behavioural freedom and lower male monopolization potential. We also predict that specialized coercive organs occur where females have low behavioural freedom but males benefit little from weaponry in male–male contests. A review of the empirical evidence supports the basic predictions of this coercion-avoidance hypothesis. We also present a simple mathematical model that confirms the logic of this hypothesis.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 372–382.     

No evidence for sexual dimorphism of facial width-to-height ratio in four large adult samples

Sexual dimorphism in physical appearance may be an important cue in both intra- and intersex competition. Recently, the facial width-to-height ratio (fWHR) has been proposed as a novel sexually dimorphic morphologic measure, with men suggested to have a higher fWHR than women. Currently, however, the status of fWHR as a sexually dimorphic trait is unclear. Here we tested for sexual dimorphism in fWHR, as well as in three additional, previously reported facial measures, in four (three Caucasian and one African) independent samples. In three of the four samples, no significant sex differences in fWHR were observed. In one sample, males showed a significantly lower (rather than higher) fWHR than females (this effect was no longer significant after controlling for body mass index). By contrast, significant and large sex differences were observed in all four samples for each of the three previously validated facial metrics, namely, (a) lower face/face height, (b) cheekbone prominence, and (c) face width/lower face height. These results provide strong evidence against the claim that fWHR, at least as measured from the surface of the face, is sexually dimorphic.     

Analysis of variance tables based on experimental structure

A stepwise procedure for obtaining the experimental structure for a particular experiment is presented together with rules for deriving the analysis-of-variance table from that structure. The procedure involves the division of the factors into groups and is essentially a generalization of the method of Nelder (1965, Proceedings of the Royal Society, Series A 283, 147-162; 1965, Proceedings of the Royal Society, Series A 283, 163-178), to what are termed 'multi-tiered' experiments. The proposed method is illustrated for a wine-tasting experiment.     

Nature Needs Nurture: The Interaction of Hormonal and Social Influences on the Development of Behavioral Sex Differences in Rhesus Monkeys

Thirty years of research on early social and hormonal environments and their relationship to the expression of behavioral sex differences in rhesus monkeys are reviewed. These studies demonstrate that whether aggressive and submissive behaviors are sexually dimorphic depends primarily on the social and not the hormonal environment. Early rearing environments without mothers or allowing brief periods of peer interaction produced higher levels of male aggression and female submission. Presenting behavior was expressed more by females than males in environments with high male aggressivity and female submissiveness. No sex differences in presenting occurred in low aggressivity environments, unless monkeys were reared isosexually, when males presented more than females. Rough and tumble play and foot-clasp mounting were consistently exhibited more by males than females across all rearing environments studied, but rearing environment affected the degree of the sex difference. When reared isosexually males displayed less, and females more, foot-clasp mounting than when heterosexually reared. No social environment increased the low frequency of female rough and tumble play. Suppressing neonatal androgen in males did not effect any sexually dimorphic behavior. Prenatal androgen administration to genetic females masculinized many aspects of their juvenile behavior, consistently increasing rough and tumble play and foot-clasp mounting across different social environments. Thus the sexually dimorphic behaviors which showed the smallest variability across social contexts were the most profoundly affected by the prenatal hormonal environment. These studies demonstrate that the expression of consistent juvenile behavioral sex differences results from hormonally induced predispositions to engage in specific patterns of juvenile behavior whose expression is shaped by the specific social environment experienced by the developing monkey.     

Androgens, aggressive behaviour and social relationships in higher mammals

This paper reviews the relationships between androgen levels, aggressive behaviour and social relationships in ungulates and primates. In these and most other mammalian species, aggressive behaviour is sexually dimorphic with males being generally more aggressive than females. This difference is evident very early in play behaviour. In males, and sometimes also in females, aggressive behaviour varies in relation with reproductive cycles and the hormonal changes which are involved in these cycles. The experimental manipulation of hormonal levels by castration or administration of exogenous hormones gives results that vary according to the species, sex, type of hormone (e.g. aromatizable or non-aromatizable androgens), and other factors (e.g. antlers state in stags). Nevertheless, it has generally been shown that aggressive behaviour in male ungulates depends largely on androgens and that in female ungulates androgen treatment consistently raises social rank, with or without modification in aggressiveness. Primates, on the other hand, seem to be less dependent on androgens for the expression of aggressive behaviour and social status.     

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.     

Social isolation increases male aggression toward females in the field cricket Gryllus bimaculatus

Social isolation has often been reported to facilitate male aggressiveness in various animal species. If social isolation also escalates male aggressive behavior towards females, the mating success of the aggressive males will be low. This study evaluated the effect of social isolation on mating behavior in the field cricket Gryllus bimaculatus, which has traditionally been considered to be an asocial species. The results showed that social isolation from same-sex individuals enhanced male aggressiveness to females, and the mating success of aggressive males was reduced under the experimental conditions. More aggressive males exhibited a longer latency to court than less aggressive males. These results suggest that because male aggressiveness causes a delay in courtship, aggressive males may have reduced mating success. This demonstrated that social relationships are a critical factor affecting male mating success, even if the species is normally considered solitary.     

Androgenic control of male-typical behavior,morphology and sex recognition is independent of the mode of sex determination: A case study on Lichtenfelder's gecko (Eublepharidae: Goniurosaurus lichtenfelderi)

Previous work on lizards has shown that many sexually dimorphic traits depend on testosterone (T), but the details of this control can vary among species. Here, we tested the role of T on the expression of morphological, physiological, and behavioral traits in Lichtenfelder's gecko (Goniurosaurus lichtenfelderi), from the lizard family Eublepharidae notable for interspecific variation in sexually dimorphic traits and the mode of sex determination. Experiments included three groups of males (intact control, surgically castrated, castrated with T replacement) and two groups of females (intact control, T supplemented). In males, castration caused reductions in 1) the size of hemipenes, 2) offensive aggression, 3) male sexual behavior in a neutral arena, 4) activity of precloacal glands, and 5) loss of male chemical cues for sex recognition. These reductions were not observed in castrated males with T replacement. Interestingly, castrated males performed sexual behavior in their home cages, which shows that the effect of T depends on the environmental context. Notably, tail vibration, previously reported as a courtship behavior in other eublepharids, is displayed by males of G. lichtenfelderi during interactions with conspecifics of both sexes, suggesting an evolutionary shift in the meaning of this signal. In females, T induced growth of hemipenes and male-typical courtship but did not induce precloacal pore activity, aggression, or mounting. In comparison to previous reports on Eublepharis macularius, our results indicate that effects of T do not depend on the mode of sex determination. Further, our results extend our understanding of the complexity of control of male traits and illustrate how lability in the effects of T can be a general mechanism causing evolutionary changes in the components of suites of functionally correlated traits.     

On the threshold of dispersal: hitchhiking on a giant fly favours exaggerated male traits in a male‐dimorphic pseudoscorpion

The evolution of exaggerated male traits is frequently driven by competition between males to control resources critical for female survival and/or reproductive success. For flightless arthropods specializing on patchy habitats, dispersal agents may represent one such critical resource. The Neotropical pseudoscorpion, Semeiochernes armiger, disperses to new habitats by attaching to the giant timber fly, Pantophthalmus tabaninus, as it ecloses from pupal boreholes within decaying Ficus trees. In a study that combined field observations of mating with experimental removal of individuals from a large, pre‐dispersal population, our morphometric analyses revealed that S. armiger is among the most highly sexually dimorphic pseudoscorpions known, with males possessing unusual, triangular‐shaped pedipalpal chelae (hands) and a male‐specific, dimorphic chela peg that exhibits threshold trait expression. Several lines of evidence indicate that extreme sexual dimorphism in S. armiger results from male competition to monopolize pantophthalmid bores as strategic sites for inseminating females on the verge of dispersal. Sexually dimorphic pedipalpal characters were significantly larger in males located in and around pantophthalmid boreholes, compared with males collected at the periphery of the pantophthalmid emergence zone. Removal of pseudoscorpions resulted in a significant decline in pedipalpal size of males associated with pantophthalmid bores, followed by a rebound in size after collected individuals were returned to the tree. Most significantly, field observations of mating indicate that this competition translates into intense selection for exaggerated male traits, with all traits of the sexually dimorphic chelae exhibiting highly significant sexual selection differentials in males. © 2013 The Linnean Society of London     

Evidence for extended action of gonadal hormones on the organization of sexually dimorphic behavior and morphology in gray short-tailed opossums (Monodelphis domestica)

Male and female gray short-tailed opossums were gonadectomized (GDX), or treated with the estrogen receptor antagonist tamoxifen citrate (TX), or corn oil (OIL) (control) during the 5th postnatal week, a time period equivalent to the 3rd postnatal week in rats and associated with high levels of circulating gonadal hormones and neural aromatase activity in this marsupial species. In adulthood following gonadectomy (for animals not previously gonadectomized) and replacement therapy with estradiol or testosterone, GDX males showed less male-typical scent marking and had shorter phalluses than OIL and TX males. Following replacement therapy with estradiol, GDX females were more likely to fight with and less likely to mate with stimulus males than TX females; OIL females were intermediate in these measures. Along with previous findings, these results suggest that gonadal hormones act over an extended postnatal period to organize sexually dimorphic behavior and morphology in male gray opossums and may have some effect on the organization of aggressive behavior in females of this species.     

Detection of Propensity for Aggression based on Facial Structure Irrespective of Face Race

The human face provides a wealth of information pertaining to the internal state and life-stage history of an individual. Facial width-to-height ratio is a size-independent sexually dimorphic trait, and estimates of aggression made by untrained adults judging own-race faces were positively associated with both facial width-to-height ratio and actual aggressive behavior. Given the significant adaptive value of accurately detecting aggressiveness based on facial appearance, we hypothesized that aggression estimates made by adults and 8-year-olds would be highly correlated with male facial width-to-height ratio even for a face category with which they had minimal experience-other-race faces. For each of the four race and age groups, estimates of aggression were positively correlated with facial width-to-height ratio irrespective of rating own-or other-race faces. Overall, the correlations between facial width-to-height ratio and ratings of aggression were stronger for adults than for children. Sensitivity to facial width-to-height ratio appears to be part of an evolved mechanism designed to detect threats in the external environment. This mechanism is likely broadly tuned and functions independently of experience.     

Maternal aggression and intermale social aggression: a behavioral comparison

The aggressive behavior of alpha male rats and lactating females were each examined toward an intact adult male rat, a castrated adult male rat, an anesthetized adult male rat, a nonlactating adult female rat, an adult albino guinea pig (male or female), or an albino mouse (male or female). When in their living colony, females displayed high levels of aggressiveness toward all stimulus objects except a mouse. The aggression toward the intruding males occurred whether the female's pups were present or not. Alpha males were aggressive toward the same stimuli except an intruding female rat and a mouse. When tested in an unfamiliar colony, the males but not the females (with or without pups present) were aggressive toward an adult male rat. Half of the females but none of the males displayed defensive burying toward an anesthetized intruder. It is suggested that the attack on an adult female, the absence of attack outside of the resident colony, and the tendency to display defensive burying are features of the aggressiveness of lactating females that are fundamentally different from the aggressiveness of alpha males. The form of the aggression (lateral attack vs. lunge attack) was only quantitatively different in males and females.     

Female preference for both behavior and morphology traits of the male Japanese newt <Emphasis Type="Italic">Cynops pyrrhogaster</Emphasis>

Males of the Japanese newt (Cynops pyrrhogaster) display complex courtship behaviors and are sexually dimorphic in terms of tail morphology. Pair encounter experiments were conducted to investigate which males are preferred by female newts. Male courtship behavior consisted of four stages, namely, Approach, Fan, Creep and Spermatophore deposition. The Fan behavior was classified into four sub-patterns. Males which showed a specific sub-pattern were accepted at a significantly higher probability by females than males which showed the other sub-patterns. The accepted males had a smaller snout–vent length, higher tail, and larger body mass than the rejected males, and their body weight was relatively heavier. Our results suggest that females of C. pyrrhogaster select their mates based on both behavioral patterns and morphological characters.     

Bite-force performance and head shape in a sexually dimorphic crevice-dwelling lizard, the common chuckwalla [Sauromalus ater (= obesus)]

The Common Chuckwalla [ Sauromalus ater (=  obesus )] is a large, sexually dimorphic lizard with a flattened head that takes refuge from predators in rock crevices. Males use their relatively large heads to bite competing males during territorial fights and to restrain females during copulation. Flattened heads with an antipredator function (i.e. seeking refuge in crevices) and enlarged heads with intrasexual competition and reproductive functions suggest possible antagonism between selective pressures on head morphology in males. To examine this hypothesis, we performed a morphometric analysis and measured the bite-force performance of 49 adult chuckwallas. Males had disproportionately wider heads than females, but did not have deeper heads. Males bit with nearly four times the force of females, consistent with the notion of sexual selection for high bite force in males. Although constrained by crevice-wedging behaviour, head depth was a good predictor of bite force in both sexes. In males, however, osteological head width also was a good predictor of bite force. These results are consistent with the hypothesis that head shape in males is under antagonistic selective pressures, which may partly explain the pattern of head shape dimorphism. The disproportionately wide head of males may reflect anatomical modifications to enhance bite force in response to sexual selection in spite of presumed constraints on head shape for crevice-wedging behaviour  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 215–222.     

Pheromones exchanged during mating: a mechanism for mate assessment in Drosophila

Many insect species are sexually dimorphic for volatile compounds associated with the cuticle. In these species, females may acquire volatile compounds from males through direct contact with males during mating. In some cases, these compounds function as antiaphrodisiacs, which inhibit subsequent male precopulatory behaviour. During mating, males may also acquire female compounds, which normally stimulate males to court. Contact during mating thus results in a mutual exchange of compounds usually found primarily, or exclusively, on one or the other sex. Drosophila melanogaster is a sexually dimorphic dipteran species in which predominant male and female cuticular hydrocarbons are mutually exchanged during mating. Using synthetic compounds, the effect of this exchange on the post-mating sexual attractiveness of both males and females was tested. The sex-predominant hydrocarbons acquired during mating decreased the attractiveness of both males and females to members of the other sex. Mated females are courted less actively than virgins, and are usually unwilling to re-mate. Similarly, recently mated males are less attractive to females than virgin males are, and may be less fertile. Thus, cuticular hydrocarbons acquired by the other sex during mating could allow both males and females to assess the immediate reproductive potential of prospective mates.     

Sex differences in the electrocommunication signals of Sternarchogiton nattereri (Gymnotiformes: Apteronotidae)

In this study we examined electrocommunication behavior in Sternarchogiton nattereri (Apteronotidae), a weakly electric fish from South America. We focused on variation between females and males lacking external dentition and used playbacks of simulated conspecifics to elicit chirps (modulations of their electric organ discharge, EOD). Chirp responses were not affected by the frequency of the playback stimulus. EOD frequency, chirp rate, and chirp duration were not sexually dimorphic; however, the amount of chirp frequency modulation was significantly greater in toothless males than in females. These results reinforce that sex differences in chirp structure are highly diverse and widespread in the Apteronotidae.     

Androgens regulate sex differences in signaling but are not associated with male variation in morphology in the weakly electric fish Parapteronotus hasemani

Sexually dimorphic signaling is widespread among animals and can act as an honest indicator of mate quality. Additionally, differences in signaling and morphology within a sex can be associated with different strategies for acquiring mates. Weakly electric fish communicate via self-generated electrical fields that transmit information about sex, reproductive state, and social status. The weakly electric knifefish Parapteronotus hasemani exhibits sexual dimorphism in body size as well as substantial within-male variation in body size and jaw length. We asked whether P. hasemani exhibits hormonally mediated sexual dimorphism in electrocommunication behavior. We also asked whether males with short versus long jaws differed significantly from each other in morphology, behavior, hormone levels, or reproductive maturity. Males produced longer chirps than females, but other signal parameters (electric organ discharge frequency; chirp rate and frequency modulation) were sexually monomorphic. Pharmacologically blocking androgen receptors in males reduced chirp duration, suggesting that this sexually dimorphic trait is regulated at least in part by the activational effects of androgens. Males sorted into two distinct morphological categories but did not differ in circulating 11-ketotestosterone or testosterone. Short-jawed males and long-jawed males also did not differ in any aspects of signaling. Thus, chirping and high levels of 11-ketotestosterone were reliably associated with reproductively active males but do not necessarily indicate male type or quality. This contrasts with other alternative male morph systems in which males that differ in morphology also differ in androgen profiles and signaling behavior.