Adolescent social environment shapes sexual and aggressive behaviour of adult male zebra finches (Taeniopygia guttata)

Adolescence is the pivotal transitional phase during which animals become sexually and socially mature and acquire the skills to cope with a variety of environmental challenges on their own. We investigated in a bird species, the zebra finch, how the social environment experienced during this period influences their behaviour in a sexual context. Zebra finches were kept in pairs (male–female or male–male) or larger mixed-sex groups (three males and three females) during adolescence and the long-term consequences were studied on courtship behaviour, aggressiveness and attractiveness in 42 males. To investigate the stability of the observed effects over time, all behavioural tests were repeated approximately 4 months after the initial recordings. Males that grew up with a single female showed the most intense courtship and highest aggressiveness and were most attractive to females, while group-reared males had the lowest courtship and aggressiveness and were the least attractive. The observed differences in courtship and aggressiveness were stable, while the differences in attractiveness disappeared over time. These findings are very similar to earlier studies on guinea pigs, indicating that the observed effects represent a general phenomenon, not restricted to mammals with a similar function and presumably also similar underlying mechanisms.     

Social feedback and attractiveness in zebra finches

The attractiveness of an individual (i.e. its ability to arouse interest in a potential mate) has important implications for its reproductive success. However, attractiveness is not a fixed trait. Previous work has shown that male birds can adjust the intensity of their courtship display in response to variation in female behaviour, but little is known about how males adjust their behaviour during mate choice in response to social feedback about their own attractiveness independent of their intrinsic quality. Such information may help to maximize the potential mating success of males. Here, we provide experimental evidence that the amount of attention given by male zebra finches to females is dependent upon the manipulated attractiveness of males. This demonstrates that, in this socially monogamous species of bird, attractiveness of males could be considered to be a social construct, at least partially determined via social feedback from females.     

Testosterone and the allocation of reproductive effort in male house finches (Carpodacus mexicanus)

Testosterone has been proposed to serve as the mediator that controls the relative effort that an individual male bird will devote to mating effort versus parental effort. Here, we demonstrate a testosterone-influenced trade-off between parental and mating efforts in male house finches. Male house finches with experimentally elevated testosterone fed nestlings at a significantly lower rate, but sang at a higher rate than males without manipulated testosterone levels. Females mated to testosterone-implanted males fed nestlings at a significantly higher rate than females mated to males without testosterone implants, resulting in similar feeding rates for both treated and untreated pairs. The effects of testosterone on male house finches, however, were not as dramatic as the effects of testosterone observed in some other socially monogamous species of birds. Because extra-pair copulations are uncommon in house finches and males provide substantial amounts of parental care, these more modest effects may be due to differences in how the allocation of reproductive effort affects the costs and benefits of different reproductive behaviors. Received: 6 June 2000 / Accepted: 17 July 2000     

Testosterone treatment suppresses paternal care in superb fairy-wrens, Malurus cyaneus, despite their concurrent investment in courtship

Courtship displays and paternal care in male birds are generally thought to be mutually exclusive, because testosterone, necessary for stimulation of sexual behaviours, suppresses paternal behaviours. Superb fairy-wrens, Malurus cyaneus, are unusual in that males concurrently engage in courtship and paternal care. Fairy-wrens live in stable socially monogamous pairs with 0-4 subordinate male helpers. Both helper and dominant males provide care whenever it is required but continue courtship throughout the period of care as most fertilisations are extra-group and females are multi-brooded. To examine the role of testosterone in this trade-off, we compared testosterone levels in males of different social status, while they had dependent nestlings, and determined the effect of testosterone treatment on provisioning rates of pairs. Testosterone levels were lower in subordinate helpers, although these do not provide more paternal care than dominant males. Conversely, testosterone levels were similar in dominant males with or without helpers, although as the number of helpers increases males invest substantially less in nestling care and more in extra-group courtship. Although testosterone levels are high, irrespective of paternal duties, experimental testosterone treatment of males resulted in a large (65%) reduction in nestling feeding rates. Surprisingly, there was no indication that females compensated for this reduction in provisioning, suggesting that females might assume a constant male contribution to offspring care. We conclude that during nestling provisioning, male fairy-wrens maintain testosterone at an individual level that does not interfere with parental duties, while allowing high investment in extra-group courtship.     

Prenatal social conditions shape offspring adult phenotype and reproductive success

The prenatal social environment affects offspring development in most studied taxa with potentially lifelong consequences. To understand the adaptive significance of such maternal influences on offspring development, it is important to study their effects on fitness. In guinea pigs, social instability during pregnancy leads to delayed development of male offspring. This has been interpreted as an adaptation to high social densities, where young males need to queue for reproductive opportunities since they cannot out-compete older dominant males. The consequences for male reproductive success are, however, so far unknown. To study the effects of different prenatal social densities on offspring reproductive performance, we housed females individually or in small groups during late pregnancy. Offspring from both treatments were reared together in large groups until independence and thereafter housed in same-sex pairs of the same treatment. We then observed courtship, aggressive behavior, and reproductive success in a low-density context with one male from each treatment competing over access to two females. Sons born to individually housed females initiated more fights, had more social contacts, courted females more, and had a higher reproductive success than sons of group-housed females. Sons born to mothers experiencing low social densities before birth therefore perform better at low social group sizes, suggesting that male development may be adaptively adjusted to anticipated social densities, although performance under high densities still needs to be compared.     

A dynamic trait affects continuous pair assessment in the blue-footed booby,<Emphasis Type="Italic"> Sula nebouxii</Emphasis>

Bright colours of male birds have often been shown to be the target of sexual selection through female choice, yet few studies have looked at the role of colour expressed after pairing on female motivation and behaviour. Here we analyse the role of an integumentary colour in the spectral range of 400–700 nm, the foot colour in male blue-footed boobies, Sula nebouxii, which is prominently displayed during pair courtship. Measurements early in the breeding season showed that foot colour of courting males is pale (high values of brightness) and has an aqua-blue chroma, and females in better body condition were mated to males with brighter feet. We carried out an experimental manipulation which modified the foot colour of males in courtship, making it closer to the foot colour of males in low nutritional state. We found that females paired to experimental males courted less and were less likely to copulate than females in the control group. Male behaviour was apparently unaffected by the manipulation; thus the change in female behaviour can be attributed exclusively to foot colour manipulation. These results strongly support the hypothesis of female preference for an integumentary colour and suggest that this dynamic trait is used as a male ornament after pairing.Communicated by J. Graves     

Courtship signalling with a labile bilateral signal: males show their best side

Asymmetries in courtship signals can result from both developmental instability during ontogeny and from temporary or permanent damage following mating, fighting, or interactions with predators. These two types of asymmetries, which can be divided into fluctuating asymmetry (FA) and damage asymmetry (DA), have both been suggested to play an important role in mate choice as potential honest indicators of phenotypic and/or genetic quality, while at the same time, DA may affect ornament asymmetry in a random manner. Interestingly, despite the massive research effort that has been devoted to the study of asymmetry during the past decades, very little is known about how an individual’s behaviour relates to asymmetry. Here, we measure and characterise asymmetry in morphological courtship signals in Corynopoma riisei, a fish where males carry elaborate paddle-like appendices on each side of the body that they display in front of females during courtship. Moreover, we investigate whether male courtship display, employing this bilateral morphological trait, reflects trait asymmetry. Finally, we assess whether males respond to phenotypic manipulations of DA with corresponding changes in courtship behaviour. We show that male display behaviour is asymmetric in a manner that reflects asymmetry of their morphological courtship trait and that male display behaviour responds to manipulations of asymmetry of these paddles. Our results thus suggest that males preferentially use their best side and, hence, that males respond adaptively to temporary changes in signal trait asymmetry.     

Sexual selection in the northern pintail (Anas acuta): the importance of female choice versus male-male competition in the evolution of sexually-selected traits

We experimentally studied the relative importance of plumage, dominance status, and courtship behavior in determining male pairing success in the northern pintail Anas acuta and assessed whether these traits function in female choice, male-male competition or both. In an experiment (experiment IA) that eliminated the confounding effects of male-male competition and social courtship, females chose males with pure white breasts and colorful scapular feathers. When the same group of birds were free to interact (experiment 1B), male behavior was more important: females chose males that courted them intensely and were attentive to them, although preferred males again had whiter breasts and more colorful scapulars. In a second experiment (experiment 2), testing the effect of age on pairing success, females showed a significant preference for 2-year-old males over yearlings: 2-year-old males courted more and were more attentive to the female than yearlings; they were also more colorful than yearlings in a number of plumage measurements. Although males (in both experiments 1B and 2) were aggressive to one another while courting the female and dominant males were sometimes able to exclude subordinates from social courtship, contrary to expectation, we found no relationship between initial dominance rank and pairing success or dominance rank and age. In addition, dominance was not correlated with any of the morphological traits measured. Once chosen, however, subordinate males typically initiated fights with the higher-ranked male(s) and quickly achieved dominance. These results suggest that (1) females choose males based on a suite of morphological and behavioral characteristics, (2) male dominance relationships do not constrain active female choice, (3) a male's position in a dominance hierarchy is largely a result rather than a cause of female choice, and (4) female choice plays a more significant role than male-male competition in the evolution of several secondary sexual traits in male northern pintails.     

Social environment during molt and the expression of melanin-based plumage pigmentation in male house sparrows (<Emphasis Type="Italic">Passer domesticus</Emphasis>)

Evolutionary biologists have shown much recent interest in the costliness and signal content of colorful plumage displays in birds. Although many studies suggest that both carotenoid- and structurally-based plumage colors are condition-dependent indicators of health and nutritional state at the time ornamental feathers are grown, there is little experimental evidence supporting the idea that melanin pigmentation is a reliable signal of condition during molt. Instead, melanin-based ornamental coloration often reveals the competitive ability and dominance of individuals throughout the year. However, this work does not indicate which proximate environmental factors shape the expression of melanin pigmentation at the time of feather growth. Because of the link between melanin coloration and the social environment, it is possible that the development of brightly colored plumage may be associated with aggressive social interactions during feather molt. Here, we show that melanin-based ornamental coloration in male house sparrows (Passer domesticus) is correlated with the degree to which individuals interact aggressively with conspecifics during molt. Males that were dominant (beta, but not alpha) within captive social groups during molt grew larger badges than subordinates. Groups of males that had higher rates of aggression during molt grew larger badges than less aggressive triads. To our knowledge, this is the first demonstration that melanin pigmentation and plumage-based status badges are related to the competitive history of individuals during feather development. By coupling badge size directly with aggressive experiences during molt, birds can use their status signal to honestly indicate their likelihood of winning agonistic encounters throughout the year.     

Developmental stress affects the attractiveness of male song and female choice in the zebra finch (Taeniopygia guttata)

Developmental stress has recently been shown to have adverse effects upon adult male song structure in birds, which may well act as an honest signal of male quality to discriminating females. However, it still remains to be shown if females can discriminate between the songs of stressed and non-stressed males. Here we use a novel experimental design using an active choice paradigm to investigate preferences in captive female zebra finches (Taeniopygia guttata). Nine females were exposed to ten pairs of songs by previously stressed and non-stressed birds that had learned their song from the same tutor. Song pairs differed significantly in terms of song complexity, with songs of stressed males exhibiting lower numbers of syllables and fewer different syllables in a phrase. Song rate and peak frequency did not differ between stressed and non-stressed males. Females showed a significant preference for non-stressed songs in terms of directed perching activity and time spent on perches. Our results therefore indicate that developmental stress affects not only the structure of male song, but that such structural differences are biologically relevant to female mate choice decisions.     

Sex-specific plasticity in brain morphology depends on social environment of the guppy, Poecilia reticulata

The vertebrate brain is a remarkably plastic organ, which responds quickly to environmental changes. However, to date, studies investigating plasticity in brain morphology have focused mostly on the physical properties of the surrounding environment, and little is known about brain plasticity in response to the social environment. Moreover, sex differences in brain plasticity remain virtually unexplored. Here, we tested how the social environment influenced brain morphology in adult males and females using experimental manipulation of the sex composition of social pairs (same sex vs. mixed sex) in the guppy (Poecilia reticulata). We detected substantial sex-specific plasticity in both the overall brain size (controlling for body size) and separate brain structures. The brain size was larger in males that interacted with females, and female optic tectum was larger in female-only groups. Overall, females had larger olfactory bulbs and cerebellum in comparison to males. While net sexual dimorphism in the brain structure can be explained in light of the known differences in boldness and foraging behaviour between the sexes, our results also support that cognitive demands associated with courtship behaviour can lead to plastic changes in the brain size. Our findings demonstrate that not only social environment can generate rapid, plastic responses in the vertebrate brain but also that such responses can depend strongly on sex.     

Relative importance of multiple plumage ornaments as status signals in golden whistlers (<Emphasis Type="Italic">Pachycephala pectoralis</Emphasis>)

Status signals are traits that advertise an individual’s competitive abilities to conspecifics during aggressive disputes. Most studies of status signals in birds have focussed on melanin-based plumage signals, but recent research shows that carotenoid-based signals may also play a role in aggressive signaling. We assessed the relative importance of melanin- and carotenoid-based plumage patches as agonistic signals in a small passerine, the golden whistler (Pachycephala pectoralis). Display signals in male golden whistlers include an unpigmented white throat patch, a carotenoid-based yellow breast and nape band, and a melanin-based black chin-stripe. We found that only the white throat patch was correlated with contest-related attributes. Males possessing large throat patches defended larger territories and commenced breeding earlier. When caged males with either experimentally reduced, or unmanipulated throat patches were presented to conspecifics, those with experimentally reduced patches attracted less aggression from male subjects. Focal males also responded faster to caged males with throat patches similar in size to their own, suggesting that they may assess relative throat patch size before engaging in aggressive encounters. Females did not discriminate between “reduced” or “control” treatments. Our data strongly suggest that only the unpigmented throat patch functions as a status signal. As this signal is unlikely to have significant development costs, honesty may be maintained through social costs.     

Experimentally elevated plasma levels of testosterone do not increase male reproductive success in blue tits

In temperate passerines, increased testosterone (T) levels during breeding mediate male aggressive and mating behaviour. If individual variability in T levels is reflected in behavioural differences during mating, males with higher T might gain higher reproductive success. This can be tested experimentally by elevating T levels. However, high exogenous T levels are known to have negative effects on male sperm production. This may reduce male fitness, particularly if sperm competition is intense. We experimentally elevated T levels in breeding blue tit males to investigate how T levels above the natural mean influence male reproductive success. Contrary to most—if not all—previous experimental manipulations of T levels in birds, we restricted the treatment with exogenous T to the time when females were fertile and T levels were naturally high in males. In blue tits, extra-pair paternity is an important component of male reproductive success, and its frequency is likely influenced by androgen-mediated behaviours such as mate attraction and aggression towards other males. Here we show that T-males were equally likely to become cuckolded and did not gain more extra-pair paternity than control males. Cuckolded T-males, however, lost more paternity than control males. We discuss the possibility that this is caused by negative effects of T treatment on sperm production.Communicated by M. Webster     

Flight initiation distance decreases during social activity in lizards (<Emphasis Type="Italic">Sceloporus virgatus</Emphasis>)

Flight initiation distance, the predator–prey distance when escape begins, is predicted by escape theory to decrease if fleeing entails loss of benefits. Shortening of flight initiation distance during social interactions is known only in males and only in a few species. In a previous study, male, but not female, Sceloporus virgatus lizards had shorter flight initiation distance when interacting with tethered conspecifics. Females in that study were not gravid or close to ovulating. I predicted that flight initiation distance would be shorter in gravid females that perform sidle-hopping displays to reject courtship than in lone females. I tested this prediction and examined effects of social interactions by males with free-ranging conspecifics to ensure that previous findings were not artifacts of tethering and experimental introduction of conspecifics. Flight initiation distance was shorter in females when interacting with males than when alone; it was also shorter in males interacting with either sex. Thus, when beneficial for reproductive reasons, social interaction affects flight initiation distance in females, but at other times, it does not. Lesser shortening of flight initiation distance in females than males may be a consequence of greater social benefit to males and protection of reproductive investment by females.     

Female brown-headed cowbirds' (<Emphasis Type="Italic">Molothrus ater</Emphasis>) social assortment changes in response to male song: a potential source of public information

In many species, females' behavior appears to be influenced by that of other females, particularly regarding mate choice. Females theoretically can reduce the costs associated with independent male assessment by observing conspecifics. Studies of brown-headed cowbirds suggest that females pay attention to other females' behavior. Group-housed females modify their song preferences, whereas females housed in pairs do not. What information is available to females in a group environment? To address this question, we studied two groups of juvenile (i.e. hatch-year birds) and adult female cowbirds in a naturalistic group setting. We used a longitudinal ABA design, consecutively introducing and removing males that differed in age, amount of song production and stage of song development, to isolate the male characteristics that related to changes in female behavior. Juvenile and adult females assorted by age class when singing adult males were in the aviary, but not when singing juveniles or silent males of any age class were in the aviary. Results from playback tests confirmed that adult male song alone influenced female age class assortment. Videotape analysis from playback tests revealed that females also wing stroked in response to male song. Other females sometimes approached females who wing stroked and observed them. We hypothesize that group-level changes in social organization and individual females' responses can serve as visual signals for other individuals.     

Deterring predators, daunting opponents or drawing partners? Signaling rates across diverse contexts in the lizard Anolis sagrei

Although the visual display behavior in Anolis lizards has received ample attention, the function of dewlap extensions (DE), push-ups (PU), and head-nods (HN) in general, and in Anolis sagrei in particular, remains highly equivocal. Therefore, our primary goal was to quantify the display rates of these visual signal types (DE, PU, and HN) in a variety of contexts, using A. sagrei as study species. To our knowledge, this is the first study to test individuals of both sexes in a repeated-measures design across multiple contexts, including predator, non-predator and social interactions (mirror, male–male, male–female, female–male). We found that males have an overall higher signaling rate than females across all contexts. In addition, we found that lizards of both sexes exhibited higher display rates in the presence of conspecifics than when confronted with a predator or non-predator, suggesting that DE, PU, and HN function in intraspecific communication, not in predator deterrence. Whereas females did not significantly raise display rates in a consexual and heterosexual context with respect to subject-alone context, males did. The PU signal type only appears to play a major role for A. sagrei males during aggressive encounters. During heterosexual interactions, increased frequencies of all signal types suggest that DE, PU, and HN are essential for male courtship. Finally, we suggest that intersexual selection is probably a driving force for frequency-related dewlap use in both sexes. In contrast, pronounced intersexual differences were detected for PU and HN rates within a social context.     

Courtship solicitation by females of the checkered white butterfly,Pieris protodice

Summary The willingness of some females of the checkered white butterfly to approach and chase conspecifies was studied in the field. Both virgin and mated females were observed approaching and chasing conspecifics. Such responses to males result in the solicitation or continuation of male courtship attempts, which in turn may lead to copulation.Mated females that approached conspecifics had significantly smaller spermatophores than females in a random sample from the same population.Females that approached tethered animals spent more time chasing tethered males than tethered females. Females with small spermatophores spent more time chasing tethered males than did females with larger spermatophores.These results confirm the hypothesis that mated females that approach and chase conspecifics are doing so in an effort to solicit male courtship attempts and to potentially receive a fresh spermatophore. The selective forces favoring courtship solicitation by females are discussed.     

Operational sex ratio and alternative reproductive behaviours in the European bitterling,<Emphasis Type="Italic"> Rhodeus sericeus</Emphasis>

We investigated the effects of male population density and male-biased operational sex ratio (OSR) with constant and limited resource density on male mating tactics shown by a freshwater fish, the European bitterling, Rhodeus sericeus. This species spawns inside living unionid mussels. Large males defended territories and were aggressive towards conspecifics under equal sex ratios. They also monopolised pair spawnings with females, releasing 98% of all sperm clouds during mating. However, the mating tactic changed at high male density where large males ceased to be territorial and instead competed with groups of smaller males to release sperm when females spawned. Large, medium and small males now obtained 61%, 33%, and 6% of sperm releases respectively, thereby reducing the opportunity for sexual selection by half. Females spawned at equal rates in the two densities of males, despite lower courtship at high density. These results run counter to the usual expectation that an increasingly male-biased OSR should lead to higher variance in male mating success. Instead, the use of alternative reproductive behaviours by males can lead to lower resource competition and mating variance at high male densities.     

Vocalizations and courtship intensity correlate with mounting success in marginated tortoises<Emphasis Type="Italic"> Testudo marginata</Emphasis>

The courtship and mounting behaviour of tortoises is elaborate, and based on a multiple signalling system involving visual, olfactory and acoustic signals. Vocalizations related to mounting seem to be particularly significant because tortoises vocalize mainly at this time. Vocalizations and courtship behaviour may be costly for males, and if these costs increase differentially for different males, then the potential exists for vocalizations and displays to reveal male individual quality. In this correlative study, we analysed relationships between male mounting success and morphological and behavioural traits, particularly acoustic signals, exhibited by male marginated tortoises (Testudo marginata) during courtship, in a group of 94 individuals breeding in semi-natural enclosures. For each male, we estimated general body condition, courtship intensity and mounting success; calls of mounting males were recorded and four sonagraphic features were measured. Calls differed significantly among males, and two features varied according to body condition. Male mounting success significantly increased according to the male/female size-ratio, suggesting the existence of a size-based assortative mating. Mounting success was also highly correlated with courtship intensity, measured as number of bites and rams given to females before mounting, and with number of calls emitted during mounting. Finally, mounting success was negatively related to call duration. To our knowledge, this is the first study in which features of tortoise vocalizations are shown to convey reliable information about male quality in socio-sexual contexts.Communicated by T. Czeschlik     

Differences in olfactory species recognition in the females of two Australian songbird species

Although birds have recently been shown to possess olfactory abilities and to use chemical cues in communication, limited effort has been made to demonstrate the use of odorants in social contexts. Even less is known regarding the use of odorants in species recognition. The ability to recognize conspecifics should be more pronounced in social species. This study investigated the importance of olfactory cues in species recognition in females of two estrildid finch species with different levels of sociality. Combining odor preference tests with chemical analyses, we surveyed whether female zebra finches and diamond firetails are able to distinguish between the species based on volatile traits and whether individuals exhibit species-specific differences in body odorants. Zebra finches are more social than diamond firetails; nevertheless, both species have an overlapping distribution area. Applying an experimental Y-maze paradigm, we showed that zebra finches can use differences in their species odor fingerprints and displayed a significant preference for the odor of conspecifics over that of heterospecifics, whereas diamond firetails did not reveal a preference. Using gas chromatography and mass spectrometry, we demonstrated that body odorants of the two species were significantly different in relative composition. This finding demonstrates the potential importance of olfactory cues in species recognition, at least in social bird species. Even these two closely related species displayed remarkable differences in their responsiveness to similar chemical cues, which might be caused by species-specific differences in ecology, physiology, or evolution.