Too big for his boots: Are social costs keeping condition‐dependent status signalling honest in an Australian lizard?

Australian painted dragon lizards Ctenophorus pictus occur in three head colours (red, orange and yellow) that differ in their level of aggression (reds being most aggressive), hormone profile (reds having higher testosterone levels) and in their frequency in our study population over time. They are also polymorphic in bib colour; some males have a bright yellow area under the chin, while others lack this coloured area entirely. We show that red males with a bib are in better body condition than red males that lack a bib. This contrasts sharply to yellow males, in which males with a bib are in poorer condition than yellow males that lack a bib. Our analysis also shows that following exposure to a high percentage of red (more aggressive) neighbours, all males suffer a reduction in body condition, and importantly, males with a bib (regardless of their head colour) suffer a more severe loss of body condition than males that lack a bib. Finally, this condition loss is significantly higher for yellow bibbed males than for red bibbed males, suggesting that the cost of sporting a bib may be higher for them. Orange males showed a non‐significant difference in condition between bib morphs. Our analysis also shows that bibbed yellow males (the morph with lower body condition), but no other morph category, declined significantly in their frequency between 2 years.     

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.     

Aggression and preputial gland of male mice affected by the presence of other males

The level of aggressiveness and the weight of preputial gland and testis in male mice (Mus musculus) were influenced by housing condition, especially by the presence of cohabitant males. In this study, the relation between aggressiveness and the preputial gland and testis weight was studied for various housing conditions. The mouse individually housed in a cage that was linked to another cage containing another male separated by wire net was more aggressive than isolated or paired mice. The preputial gland weight also showed the same tendency, suggesting that the odor from other males promotes pituitary-gonadal activity in males, and that long-term cohabitance inhibits it.     

Male sexual attractiveness and aggressiveness in rodents having different mating systems

Male aggressiveness can affect male reproductive success both directly by increasing competitiveness and indirectly through female preference. Assuming that significance of male aggressiveness in species having different mating systems can be different, we studied how male aggressiveness relates to sexual attractiveness in polygynous rodents, the water vole (Arvicola terrestris) and the house mouse (Mus musculus), and in a monogamous species, the steppe lemming (Lagurus lagurus). Our analysis revealed that the relation between odor attractiveness and aggressiveness is nonlinear. In polygynous species, males are more aggressive, so females opt for aggressive, albeit not too aggressive, males. In the monogamous steppe lemming, males show low level of intermale aggressiveness, and the most attractive are slightly aggressive males who have greater reproductive potential.     

Testosterone supplementation in subordinate, small male lizards: consequences for aggressiveness, color development, and parasite load

According to the immunocompetence hypothesis, testosterone stimulatesthe expression of male sexually selected traits while decreasingimmunocompetence. This proposed trade-off was studied by experimentalsupplementation of testosterone to small, subordinate, dull-coloredmale lizards, Psammodromus algirus. Experimental males showeda tendency to overlap their home range with fewer small malesthan did control males and tended to be more aggressive. However,control males were observed more frequently attending femalesthan experimental males. The area of patches of breeding coloration,the number of ticks, and the frequency of recoveries of testosterone-supplementedand control males did not differ significantly. The resultssuggest that small adult males with high levels of testosteronebehave more aggressively, which may be advantageous to securinga breeding territory in the next season. However, the hormonedid not apparently affect ornamentation or parasite load. Weargue that, whatever the mechanisms involved, blocking effectsof testosterone may be adaptive because being cryptic facilitatesa sneaking strategy, and low ectoparasite load may improve survival     

Are Androgens Related to Aggression in House Wrens?

Elevated circulating testosterone levels are hypothesized to allow male animals to direct resources into territorial and mating behaviors at the expense of reducing paternal care of offspring. For this hypothesis to apply, testosterone must facilitate territorial/mating behaviors and have antagonistic effects on paternal care, but this pattern has only been supported in some, not all, species. I tested whether androgens correlate with aggressive behaviors in male house wrens ( Troglodytes aedon), a double‐brooded species where paternal and aggressive behaviors overlap temporally. House wrens may therefore benefit from having a hormonal mechanism that allows males to rapidly change behavioral states. However, I found no evidence that androgens (testosterone and 5α‐dihydrotestosterone) relate to aggression in house wrens: Androgens did not increase in response to playback, and endogenous‐circulating androgens were not correlated with how aggressively males responded to those playbacks. Moreover, androgen levels were low during the pre‐breeding stage of the second brood, when many males establish new territories and attract new mates. This study adds to a growing body of the literature suggesting that the relationship between circulating androgens and aggressive behavior is more complex than originally thought.     

The Role of Lateral Blue Spots in Intrasexual Relationships Between Male Iberian Rock-Lizards, Lacerta monticola

Vertebrate males often show breeding colours that may function as reliable signals of status in intrasexual competition. In many lacertid lizards, males show a conspicuous row of small but distinctive blue spots that runs along their body side on the outer margin of the belly. However, no study has examined the role of these blue spots. We first analysed in a field population of the Iberian rock lizard, Lacerta monticola, the relationships between number of blue spots and some morphological traits, which are known to be related to males’ fighting ability. The number of spots seems to be an character showing ontogenetic change as large (generally older) males showed more blue spots than small (generally younger) males. Males with a higher body condition also showed a higher number of blue spots. Thus, a higher number of blue spots may be used to signal size, age or body condition. Many contiguous blue spots would result in a visual artefact consisting of a continuous blue band, which might be a reliable size‐ or condition‐dependent signal in some social contexts. We further examined in the laboratory whether male characteristics are related to dominance status. In males with similar body size or age, those with relatively larger heads were more dominant, whereas the number of blue spots was not important. Moreover, the number of blue spots in nature was not related to relative head size. Finally, we experimentally manipulated the presence and the number of blue spots of intruding males, and examined the aggressive response of resident males. Intruder individuals manipulated to cover all their blue spots received a lower amount of aggression. However, males with different numbers of manipulated blue spots received a similar number of aggressive responses. These results suggest that, during agonistic encounters, the presence of blue spots, but not their number, may elicit aggressiveness. Thus, blue spots may serve to identify an individual as an adult male, and to enhance body size of larger males.     

Female aggressiveness towards female decoys decreases with mate T level in the pied flycatcher

Social selection is expected to favour the evolution of female aggressive defence of nesting resources in cavity-nesting birds, which may be also mediated by testosterone (T) levels. Male T levels could express male dominance and thereby territorial safety for female partners and thereby reduce their need for aggressive defence. Here, we explored the role of T levels in female-female competition in a songbird, the pied flycatcher Ficedula hypoleuca. In an experiment with female decoys placed close to the nestbox at the end of laying, we explored if female aggressiveness is related to their own T level or to mate T level. T levels of males and females were measured in the middle of the nestling period. Mean female aggressiveness towards decoys in three presentations was estimated through proximity to the decoy and number of attacks by females, two variables which were positively associated. Aggressiveness by female nest owners to female decoys was negatively related to male T level but unrelated to own T level. There was no assortative mating with respect to T level. Female aggressiveness is more strongly related to the hormonal status of mates than to their own.     

The role of parasite-induced immunodepression,rank and social environment in the modulation of behaviour and hormone concentration in male laboratory mice (Mus musculus).

Peripheral immune responsiveness in male laboratory mice was reduced by infection with the trichostrongyloid nematode Heligmosomoides polygyrus. Responsiveness was also lower among high-ranking (aggressive) males regardless of infection status. Reduced responsiveness in both infected animals and high rankers was associated with elevated serum corticosterone concentration (a potential immunodepressant) and was compounded among high-ranking males by subsequent high aggressiveness. As in previous experiments, only low rankers modulated testosterone secretion in relation to current immunocompetence and corticosterone concentration. The lack of any downregulation of aggression in response to parasite-induced immunodepression contrasted with previous results using antithymocyte serum and may be due to the more localized nature of immunodepression during H. polygyrus infection. However, the additional increase in corticosterone concentration resulting from exposure to female odour and destabilized aggressive social relationships did result in downregulation of aggression among high rankers and of testosterone among mice generally, suggesting that modulation rules of thumb are at least partly dependent on the proximate cues associated with immunodepression.     

Does Female Personality Determine Mate Choice Through Sexual Cannibalism?

Animal personalities (e.g. consistent across‐context behavioural differences between individuals) can lead to differences in mate choice. However, evidence for this link remains limited. Pre‐mating sexual cannibalism can be a behavioural syndrome (i.e. a suboptimal personality) in which adaptive female aggression towards heterospecific prey spills over on non‐adaptive aggression towards courting males, independently of the female mating or feeding status (i.e. the ‘aggressive spillover hypothesis’, ASH). On the other hand, sexual cannibalism can also be a form of mate choice by which females selectively kill or mate with males depending on the male phenotype. We introduce the hypothesis that the most aggressive females in the population will not only attack males more frequently, but will be less likely to impose sexual selection on males through sexual cannibalism. Assuming that in a field common garden experiment in which females were fed ad libitum the rate of weight gain by a female may reflect her voracity or aggressiveness, we show that in the cannibalistic burrowing wolf spider Lycosa hispanica (formerly L. tarantula), voracity towards heterospecific prey predicts a female's tendency towards sexual cannibalism. Unmated females with higher weight gains were more cannibalistic and attacked males regardless of the male phenotype. On the other hand, females that were less voracious tended to be less cannibalistic, and when they did kill a male, they were selective, killing males in poorer condition and mating with those in better condition. Our results demonstrate that females with different phenotypes (growth rates) differently imposed selection on male condition, tentatively supporting the hypothesis that female aggression levels can spill over on sexual selection through sexual cannibalism.     

Social environment affects testosterone level in captive male blue-black grassquits

The challenge hypothesis proposes that testosterone (T) elevation above what is needed for breeding is associated with social factors, and males possibly modulate their hormonal response to variations in population density and sex ratio. We investigated the role of social environment in altering testosterone levels and aggression in a tropical, seasonally breeding grassquit (Volatinia jacarina). We exposed males to three social conditions during 1 year: all-males treatment (six males), mixed treatment (three males-three females), and paired treatment (one male-one female). We quantified aggressiveness among males and T plasma concentration for each individual in each treatment monthly. We found that more aggressive interactions occurred in the all-males treatment than in the mixed treatment. The data also revealed that, coincident with these behavioral changes, the patterns of T variation through time in each treatment were markedly different. The all-males treatment exhibited an early increase in T concentration, which was sustained for a lengthy period with two distinctive peaks, and subsequently declined sharply. The mixed treatment presented an intermediate pattern, with more gradual increase and decrease in T levels. At the other extreme, the paired treatment presented a later rise in T concentration. We conclude that the more competitive environment, with higher density of males, caused the early and higher elevation in T level, thus the presence of competitors may influence the decision of how much a male should invest in reproduction. We suggest that the male's perception of his social environment ultimately mediates hormonal production and alters his reproductive strategy.     

Effects of Exogenous Testosterone on Parental Care Behaviours in Male Bluegill Sunfish (Lepomis macrochirus)

Androgens are known to mediate aggressive and defensive behaviour in many vertebrate species. However, high concentrations of androgens might also conflict with the expression of nurturing behaviours and therefore a trade‐off can exist between aggressive and nurturing behaviours during parental care. We explored the role of testosterone in paternal care in bluegill sunfish (Lepomis macrochirus), where males provide both sole defence of the young from predators and sole nurturing behaviour such as fanning of the eggs. At the onset of parental care, we manipulated testosterone levels in males using testosterone propionate implants. We then observed the frequency of nurturing and aggressive behaviours displayed by the males over 6 d of parental care. Testosterone‐implanted fish were more aggressive when presented with a brood predator, performing more bites, opercular flares and lateral displays than control males. Testosterone‐implanted males, however, were not less nurturing than control fish, performing similar levels of fanning and nest‐cleaning behaviours. Thus, our results support a positive relationship between testosterone and paternal aggression but no testosterone‐mediated trade‐off between paternal nurturing and aggression.     

The meek inherit the earth: less aggressive wild mice are more successful in challenging situations

Numerous studies have shown an association between aggressiveness and several other behavioural traits. For example, more aggressive animals were bold and active explorers tending to form persistent routines whereas less aggressive animals were shy, careful but more flexible. While the former are thought to be more successful under stable conditions the latter should have advantages in more dynamic situations. These differences can apply not only to individuals but also to populations, species or groups of species with important implications to species distributions and speciation rates. Here we utilized the Morris water task (MWT) to investigate how two subspecies, Mus musculus musculus and M. m. domesticus, known to differ in aggressiveness, cope with stressful situations. We found that less aggressive musculus males performed significantly better in solving the MWT than more aggressive domesticus males. This suggests that M. m. musculus is more flexible and could be more successful under stressful and/or dynamic situations typical of dispersal bouts. It seems plausible that this difference may have had an influence on the secondary contact between musculus and domesticus populations in the past and perhaps still can affect the dynamics of the European hybrid zone between the subspecies. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 310–319.     

Hormones, performance and fitness: Natural history and endocrine experiments on a lizard (Sceloporus undulatus)

We used the "morphology-performance-fitness" paradigm (Arnold, 1983) as our framework to investigate endocrine control of performance and fitness in Sceloporus undulatus (Eastern Fence Lizard). Focusing on males, we used the "natural experiments" of seasonal, sexual, and developmental variation in growth and in exercise endurance to identify testosterone and corticosterone as potential modulators of performance and related traits of interest. We followed with experimental manipulations of testosterone to investigate functional relationships, both in the laboratory and in the field. Further, we used focal observations and demographic studies, coupled with genetic determination of paternity, to test associations between performance and fitness, measured as reproductive success. We found that in males, endurance and plasma concentrations of testosterone and corticosterone are at their peaks in the spring breeding season, when lizards are most actively engaged in patrolling home ranges and in reproductive behavior. At that time, plasma concentrations of testosterone are correlated with body size; plasma concentrations of corticosterone and parameters of home range, including area and the number of overlapped females, are correlated with home-range overlap between males and females. During prereproductive development, males (but not females) experience a maturational increase in plasma testosterone. At about the same time, they become more active, expand their home ranges, and grow less quickly than do females, suggesting a trade-off in the allocation of energy, mediated by testosterone. Experimentally, testosterone has positive effects on fitness by stimulating endurance and reproductive activity and increasing home-range area, but it exacts costs in fitness by increasing ectoparasitism, decreasing growth, and decreasing survivorship. We found evidence of selection on body size, endurance, and home-range size (and thus access to potential mates). Despite having positive effects on performance traits, plasma concentrations of testosterone were not correlated with number of offspring sired by males. However, we found a strong correlation between the level of plasma corticosterone and the number of offspring sired. We also found evidence of size-assortative mating, indicating that for males, both the number and the size (and thus, fecundity) of their mates increase with body size. Our studies exemplify the power of natural history combined with experimental endocrine manipulations to identify hormonal regulators of performance and linkages to fitness. Furthermore, our results illustrate ecological and evolutionary significance of individual variation in endocrine traits.     

Testosterone and autumn territorial behavior in male red grouse Lagopus lagopus scoticus

In many bird species, males exhibit territorial aggression outside the breeding season, when testosterone concentrations are low and may not regulate territorial behaviors. The hormonal regulation of aggression at this time of year has only been studied in passerine birds. Here, we investigated the role of testosterone in the regulation of aggression in a non-passerine bird, the red grouse Lagopus lagopus scoticus. Male red grouse are aggressive in early spring when breeding starts, in autumn when they establish territories, and sporadically through much of the winter. We first describe seasonal variations in plasma testosterone concentrations and in the size of males' sexual ornaments, their red combs, which relates to aggressiveness. Testosterone concentrations and comb size were correlated. Both increased in autumn to a peak in October, and then increased again in spring, to a greater peak in early April. Secondly, we experimentally investigated the effects of testosterone, and of an anti-androgen (flutamide) used in combination with an aromatase inhibitor (ATD), on autumn territorial behavior. Males were treated with either empty implants, as controls (C-males), testosterone implants (T-males), or with flutamide and ATD implants (FA-males). One month after implanting, both T- and FA-males had higher concentrations of testosterone than C-males. Comb size, aggressive call rate, and response to playbacks of territorial call all significantly increased in T-males. However, the increase in testosterone in FA-males did not increase comb size or aggressive behavior. In the following spring, after the content of implants was used, FA-males had significantly lower testosterone than C-males, and had a reduced seasonal increase in comb size. The results suggest that testosterone plays a significant role in regulating red grouse aggressive behavior in autumn. However, the observation that flutamide and ATD treatment did not reduce territorial behavior, suggests that estradiol may also be involved in the regulation of non-breeding aggression.     

The effects of luteinizing hormone, oestrogen and ovariectomy on the agonistic behaviour of female Quelea quelea

Previous work with male Quelea showed that agonistic behaviour in relation to individual distance is controlled by luteinizing hormone (LH), rather than by testosterone, and that males are more aggressive than females. Experiments with female groups are reported which show that: (a) LH injections increase aggressive encounter frequency; (b) ovariectomy in the breeding season (but not outside it) also increases encounter frequency; and (c) oestrogen injections decrease encounter frequency. The effects of LH were shown to be specific to agonistic responses rather than mediated through changes in activity. Correlations between changes in natural hormone levels and encounter frequency support the injection findings. These results are consistent with the hypothesis that LH controls aggressive encounters over individual distance in the female as in the male and that oestrogenic inhibition of this LH-mediated aggressiveness is a cause of female subordination and the lower encounter frequency found in female groups. The annual cycle of encounter frequency is described and the significance of different systems of hormonal control is discussed.     

Aggressiveness and size: a model and two tests

Individual variation in aggressive behavior in animals might be caused by adaptive covariation with body size. We developed a model that predicts the benefits of aggressiveness as a function of body size. The model indicated that individuals of intermediate sizes would derive the greatest benefits from being aggressive. If we assume that the cost of aggression is approximately uniform with respect to body size, selection should favor higher aggression in intermediate-sized individuals than in large or small individuals. This prediction was tested by stimulating male Madagascar hissing cockroaches, Gromphadorhina portentosa, with disembodied antennae and recording the males' aggressive responses. Antennae from larger males evoked weaker responses in subjects, suggesting that males obtained information about their opponents' size from the opponents' antennae alone. After accounting for this effect, we found support for the key prediction of our model: aggressiveness peaked at intermediate sizes. Data from actual male-male interactions validated that the antenna assay accurately measured aggressiveness. Analysis of an independent data set generated by staging male-male interactions also supported the prediction that intermediate-sized males were most aggressive. We conclude that adaptive covariation between body size and aggressiveness explains some interindividual variation in aggressiveness.     

Corticosterone and time-activity budget: an experiment with Black-legged kittiwakes

In vertebrates, the well established increase in plasma corticosterone in response to food shortage is thought to mediate adjustments of foraging behavior and energy allocation to environmental conditions. However, investigating the functional role of corticosterone is often constrained by the difficulty to track time-activity budget of free-ranging animals. To examine how an experimental increase in corticosterone affects the activity budget of male Black-legged kittiwakes (Rissa tridactyla), we used miniaturized activity loggers to record flying/foraging, presence on the sea surface and nest attendance. To investigate how corticosterone affects allocation processes between self-foraging and foraging devoted to the brood, we monitored body mass change of males from capture (day 0) to recapture (day 3). Among control birds, males in poor condition at day 0 spent significantly more time flying/foraging and less time attending the nest site than did males in good condition. Corticosterone treatment affected time spent flying/foraging in interaction with body condition at day 0: corticosterone-implanted males in good condition spent more time flying/foraging than control ones; this was not observed in poor condition males. In control birds, change in body mass was negatively correlated with body condition at day 0. This was reinforced by corticosterone treatment and, on average, corticosterone-implanted males gained much more mass than controls. These results suggest that in Black-legged kittiwakes, body condition and corticosterone levels can interact to mediate foraging decisions and possibly energy allocation: when facing stressful environmental conditions, birds in good body condition may afford to increase the time spent foraging probably to maintain brood provisioning, whereas poor body condition birds seemed rather to redirect available energy from reproduction to self-maintenance.     

Absence of Mate Guarding in the Yellowhammer (Emberiza citrinella)?

The mate guarding behaviour of male yellowhammer (Emberiza citrinella) was studied with special reference to the effects of age, body size (tarsus length) and coloration of males. Measurements of intra-pair distance do at the most provide evidence for relatively lax mate guarding. On the other hand, patterns of male song activity and inter-male aggression were more in agreement with the predictions of the mate guarding hypothesis. The reasons for the comparatively low mate guarding intensity in the yellowhammer may be that males do not need to guard their mates intensely. Age differences were found in song and aggressive activity, older males singing and fighting the most. Size had no effect on guarding behaviour. Coloration was correlated with inter-male aggressiveness and conflict initiation propensity. Less colourful males fought the most in the pre-fertile period of their mates, whereas colourful and old males fought the most during the fertile period. This suggests that coloration may be an indicator of individual fighting and guarding ability.     

Song rate as a signal of male aggressiveness during territorial contests in the wood warbler

Aggressive signaling is an important component in animal communication, as it provides an efficient mechanism for settling conflicts over resources between competitors. In songbirds, a number of singing behaviors have been proposed to be aggressive signals used in territory defense, including song rate. Although aggressive signaling in songbirds has received considerable research attention, adequate evidence for most putative aggressive signals is not available. In this study, we experimentally investigated whether the song rate of male wood warblers Phylloscopus sibilatrix is a signal of their aggressive intent in male–male interactions. We found that males responded differentially to simulated territorial intrusions depending on the song rate of an intruder. Moreover, males that continued to sing during territorial contests increased their song rates, and this behavior predicted the strength of aggressive escalation by the signaler. These results suggest that song rate is an aggressive signal during male–male interactions in the wood warbler. We also found high intra‐individual repeatability in the strength of aggressive response to simulated intrusions, likely reflecting differences in personality (aggressiveness) or quality of male wood warblers. We conclude that changes in singing rate may be an efficient mechanism of signaling immediate shifts in motivation of signalers during territorial contests, especially in species that lack large repertoires or have simple songs.