Habituation to humans affects yolk steroid levels and offspring phenotype in quail

In the field as well as in the laboratory, human-generated stress responses are reduced in adult animals previously habituated to humans in comparison to non-habituated individuals. In birds, yolk steroid levels vary with maternal environment and condition. We tested the hypothesis that the experience of female birds with humans could affect yolk steroids levels and offspring phenotype. Two groups of Japanese quail, one habituated to humans (H) and a second non-habituated (NH), were exposed daily to brief human disturbances. We analysed egg quality, offspring growth, and offspring emotional reactivity. NH females produced eggs with less androgens (testosterone and androstenedione) and more immunoreactive progesterone compared to birds habituated to humans. NH females produced eggs with less yolk, heavier shell and chicks hatching later and being smaller as compared to habituated individuals. A lower emotional reactivity was found in young of NH females compared to young of H females. Thus, human disturbance of the mother triggered different effects on chick phenotype depending on previous experience of mother birds with humans. In addition, we describe for the first time the influence of environmental stimuli on yolk immunoreactive progesterone levels. Our results show that a relatively minor difference in behavioral habituation may have substantial effects on eggs and offspring. This has obvious implications for keeping and handling laboratory animals, for conservation biology and for animal welfare.     

Embryonic temperature shapes behavioural change following social experience in male leopard geckos, Eublepharis macularius

Individual variation in behavioural expression and behavioural plasticity exist in all species, and early experiences are critical determinants of both. The leopard gecko is a lizard with temperature-dependent sex determination, and in this species, embryonic incubation temperature (IncT) affects the display of social behaviours. For example, adult males hatched from eggs incubated at an IncT that produces predominantly males (male-biased IncT, 32.5°C) are more aggressive and less sexually active than males hatched from eggs at an IncT that produces predominantly females (female-biased IncT, 30°C). It is not known, however, whether IncT influences behavioural plasticity in adulthood. We assessed whether adult males hatched from eggs incubated at female- and male-biased IncTs showed different changes in territorial behaviour (scent marking in an empty test arena), anticipatory behaviours (activity, scent marking and tail vibrations in response to cues that predict the introduction of a female) and courtship behaviour following social interactions with females. We found that heterosexual social experiences increased territorial behaviour and the display of anticipatory behaviours in males from the female-biased IncT but not in males from the male-biased IncT. This difference was not due to differences in the amount of social experiences acquired, and the greater change in anticipatory behaviour in males from the female-biased IncT suggest that they acquired sexual conditioning more readily. Differences in sex steroid concentrations or neural metabolism caused by IncT could underlie this difference. These results highlight the profound implications of maternal nest site selection for offspring phenotype and plasticity in this species.Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Effects of male courtship and gonadal steroids on pair formation, egg-laying, and serum LH in Canvasback ducks (Aythya valisineria)

The effects of social stimuli on the reproductive physiology of female birds have been widely studied. This study examined the endocrine and behavioural responses of female Canvasbacks ( Aythya valisineria ) to changes in the behavioural and endocrine states of the male, as signalled by his courtship displays. Male Canvasbacks exposed to female conspecifics exhibited a variety of courtship displays which increased significantly with testosterone administration. However, the testosterone-increased courtship displays of males did not increase female receptivity or serum LH, or stimulate reproductive development or egg-laying in unpaired females placed with them. Females confined in cubicles within a pen that held breeding pairs and a free-swimming flock had higher serum LH levels and laid more eggs than did females in cubicles in another pen without breeding pairs or a free-swimming flock. This suggests that social factors, such as vocalizations from a flock and breeding pairs, may increase serum LH and egg-laying in unpaired females. Oestradiol implants in female Canvasbacks did not elevate receptivity to courting drakes, nor did they stimulate pair formation, nesting activity, or egg-laying behaviour. Testosterone implants in drakes and oestradiol implants in females decreased serum LH in each group. These results show that increasing the amount of courtship is not adequate to stimulate pairing behaviour or increases in reproductive hormones. Thus, our results suggest that female receptivity to male courtship may be a key determinant of pair formation and consequent synchronization of the behaviour patterns between members of a pair of wild birds. Our results may further suggest a dissociation between effects of courtship and pair formation in wild Canvasbacks.     

Inhibition of adult social behaviour in ducks induced by juvenile administration of gonadal hormones

This experiment was designed to study the long-term behavioural effects of gonadal hormone injections into domestic ducklings. Ten male and four female ducklings were injected daily from their 4th day onwards: the males with testosterone propionate and the females with oestradiol benzoate. Five males were injected for 40 days, the other ducklings (5♀ + 4♂) for 80 days. Behavioural effects of these treatments were assessed when the birds were six months old. Social displays were strongly inhibited in the injected males as compared with control birds but no general significant effect was observed for the aggressive and sexual behaviour. The inhibition of social displays is consistent with the view that these behaviour patterns are regulated by the pituitary-gonadal axis and the different levels at which the functional inhibition could have occured are discussed. Far fewer social displays were performed by the males presented with injected females which, on the other hand, showed less sexual behaviour than the control females. This supports the idea that the female plays an important part in the social display of ducks.     

Females lay fewer eggs for males with greater courtship success in a lekking Drosophila

The evolutionary basis for female mate choice in lek mating systems has been a common subject of research in animal behaviour. Because males apparently provide only gametes to females in lekking species, most research has focused on possible indirect (genetic) benefits that females might gain by discriminating among males. Despite the emphasis on indirect benefits, it has been recognized that females in non-resource-based systems such as leks could potentially gain direct benefits via mate choice if males varied in fertilization abilities, for example. Previous evidence has shown that females of a lekking Hawaiian Drosophila, D. grimshawi, vary in fecundity when mated to certain males, and that females possess preferences for vigorously courting males. This study tests the hypothesis that D. grimshawi females gain direct benefits by preferentially mating with more sexually vigorous males. Male courtship vigour (performance of wing and head-under-wing displays) and the consequences of female choice on offspring production were evaluated separately using different females. Unexpectedly, matings involving more vigorously courting males resulted in fewer offspring being produced. Reduced offspring number resulted because females laid fewer eggs when mating with males having greater courtship success. These results are discussed in light of sexual conflict and possible multiple mating by females. Females also demonstrated considerable variation in mating behaviour and behavioural variation was correlated with mating benefits. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Sexual conflict and the evolution of female mate choice and male social dominance

Conflicts between the sexes over control of reproduction are thought to lead to a cost of sexual selection through the evolution of male traits that manipulate female reproductive physiology and behaviour, and female traits that resist this manipulation. Although studies have begun to document negative fitness effects of sexual conflict, studies showing the expected association between sexual conflict and the specific behavioural mechanisms of sexual selection are lacking. Here we experimentally manipulated the opportunity for sexual conflict in the cockroach. Nauphoeta cinerea and showed that, for this species, odour cues in the social environment influence the behavioural strategies and fitness of males and females during sexual selection. Females provided with the opportunity for discriminating between males but not necessarily mating with preferred males produced fewer male offspring than females mated at random. The number of female offspring produced was not affected, nor was the viability of the offspring. Experimental modification of the composition of the males' pheromone showed that the fecundity effects were caused by exposure to the pheromone component that makes males attractive to females but also makes males less likely to be dominant. Female mate choice therefore carries a demographic cost but functions to avoid male manipulation and aggression. Male-male competition appears to function to circumvent mate choice rather than directly manipulating females, as the mate choice can be cryptic. The dynamic struggle between the sexes for control of mating opportunities and outcomes in N. cinerea therefore reveals a unique role for sexual conflict in the evolution of the behavioural components of sexual selection.     

Age affects the expression of maternal care and subsequent behavioural development of offspring in a precocial bird

Variations of breeding success with age have been studied largely in iteroparous species and particularly in birds: survival of offspring increases with parental age until senescence. Nevertheless, these results are from observations of free-living individuals and therefore, it remains impossible to determine whether these variations result from parental investment or efficiency or both, and whether these variations occur during the prenatal or the postnatal stage or during both. Our study aimed first, to determine whether age had an impact on the expression of maternal breeding care by comparing inexperienced female birds of two different ages, and second, to define how these potential differences impact chicks' growth and behavioural development. We made 22 2-month-old and 22 8-month-old female Japanese quail foster 1-day-old chicks. We observed their maternal behaviour until the chicks were 11 days old and then tested these chicks after separation from their mothers. Several behavioural tests estimated their fearfulness and their sociality. We observed first that a longer induction was required for young females to express maternal behaviour. Subsequently as many young females as elder females expressed maternal behaviour, but young females warmed chicks less, expressed less covering postures and rejected their chicks more. Chicks brooded by elder females presented higher growth rates and more fearfulness and sociality. Our results reveal that maternal investment increased with age independently of maternal experience, suggesting modification of hormone levels implied in maternal behaviour. Isolated effects of maternal experience should now be assessed in females of the same age. In addition, our results show, for first time in birds, that variations in maternal care directly induce important differences in the behavioural development of chicks. Finally, our results confirm that Japanese quail remains a great laboratory model of avian maternal behaviour and that the way we sample maternal behaviour is highly productive.     

Maternal Epigenetic Transmission of Social Motivation in Birds

Behavioural development is a complex phenomenon involving interactions between genetic constraints and environmental influences. One of the most potent environmental influences during the ontogeny of the behavioural characteristics of young is played by mothers. In particular, mammalian mothers modulate the social competences of their young, influencing all their future social life. Here, we investigated the influence of the social characteristics of adoptive mother birds ( Coturnix coturnix japonica ) on the social motivation (origin of every social relationship) of the young they reared. We characterized the social behaviour of standard stock chicks reared by female quail, genetically selected either for low (LSR) or high (HSR) levels of social reinstatement (index of treadmill behaviour which combined the tendency to run towards conspecifics with the tendency to move away from them), to investigate epigenetic transmission of social motivation. Our results show that HSR and LSR adoptive mothers partially transmitted their social characteristics to their young: chicks reared by HSR females presented higher levels of social motivation than chicks reared by LSR females. This maternal influence appeared much clearer in young males than in young females. Our study reveals that, as in mammals, bird mothers influence epigenetically the development of the social behaviour of their young.     

Offspring viability benefits but no apparent costs of mating with high quality males

Traditional models of sexual selection posit that male courtship signals evolve as indicators of underlying male genetic quality. An alternative hypothesis is that sexual conflict over mating generates antagonistic coevolution between male courtship persistence and female resistance. In the scarabaeine dung beetle Onthophagus taurus, females are more likely to mate with males that have high courtship rates. Here, we examine the effects of exposing females to males with either high or low courtship rates on female lifetime productivity and offspring viability. Females exposed to males with high courtship rates mated more often and produced offspring with greater egg-adult viability. Female productivity and lifespan were unaffected by exposure to males with high courtship rates. The data are consistent with models of sexual selection based on indirect genetic benefits, and provide little evidence for sexual conflict in this system.     

Psychobiology of sexual behavior in a whiptail lizard, Cnemidophorus inornatus

This study investigated the effects of social environment on gonadal recrudescence and sexual behavior in male and female Little Striped Whiptail lizards (Cnemidophorus inornatus). The presence of sexually active males facilitates ovarian recrudescence in conspecific females. Similarly, the presence of reproductively active females facilitates testicular recrudescence in conspecific males. Males housed with females, however, had lower average circulating concentrations of testosterone and dihydrotestosterone, and higher average concentrations of corticosterone compared to intact males housed in isolation. In other studies, the presence of reproductively active females partially restored courtship behavior in castrated males compared to castrated males housed in isolation. Despite the stimulatory effects of females on castrates, exogenous androgens are required for complete restoration of all components of sexual behavior in male C. inornatus. Females are receptive to male courtship and copulatory behavior only during the vitellogenic stages; females in previtellogenic or postovulatory ovarian stages aggressively reject male courtship advances. These findings demonstrate reciprocal effects of sexual behaviors of males and females upon each other's reproductive behavior and physiology.     

Correlated response in yolk testosterone levels following divergent genetic selection for social behaviour in Japanese quail

Maternal effects are a powerful tool that parents can use to modify the phenotype of their offspring. In birds, the amount of androgens that females deposit in their eggs has been shown to influence early development and adult behavioural phenotypes. Differences in such behavioural strategies have been used as the target of artificial selection programmes with a view to improve animal welfare. In this study, we tested whether artificial selection for divergent social behaviour in Japanese quail had resulted in correlated changes in yolk androgen levels. We used lines that had been selected at the chick stage for high and low motivation to regain contact with a group of conspecific chicks. This procedure has led to important behavioural differences in the high and low line in a suite of behavioural correlates of sociality. We found that eggs laid by the line selected for high motivation for social reinstatement contained more than twice the amount of yolk testosterone of eggs laid by females from the low line, while the unselected line laid eggs with intermediate levels. This finding strongly suggests a functional link between these two traits, and underlines the possible role of yolk androgen modulation in promoting the evolution of behavioural syndromes.     

Sexual Strategies of a North American ‘Tarantula’ (Araneae: Theraphosidae)

Despite their general notoriety and popularity as pets, little is known of the behavioural ecology of ‘tarantulas’ or theraphosid spiders. We studied a theraphosid of the Arizona deserts, Aphonopelma sp., to determine behavioural events crucial to successful courtship and mating. Males search for spatially scattered females and, at short range, may detect females by substrate-borne cues. When two males are present with a single female, no direct competition such as aggression is observed. Both males may mate with a single female in rapid succession, with no evidence of post-copulatory mate guarding. Despite the potential for sexual cannibalism, courtship and mating behaviour patterns exhibit few aggressive elements and males nearly always survive sexual encounters with females. The mating system of this Aphonopelma species may best be described as a type of scramble-competition polygyny, in which the ability of males to locate receptive females is an important determinant of mating success in males. Multiple mating by females renders predictions concerning fertilization success uncertain, due to the possibility of sperm competition and ‘cryptic’ female mate choice.     

A female's past experience with predators affects male courtship and the care her offspring will receive from their father

Differential allocation occurs when individuals adjust their reproductive investment based on their partner''s traits. However, it remains unknown whether animals differentially allocate based on their partner''s past experiences with predation risk. If animals can detect a potential mate''s experience with predators, this might inform them about the stress level of their potential mate, the likelihood of parental effects in offspring and/or the dangers present in the environment. Using threespined stickleback (Gasterosteus aculeatus), we examined whether a female''s previous experience with being chased by a model predator while yolking eggs affects male mating effort and offspring care. Males displayed fewer conspicuous courtship behaviours towards females that had experienced predation risk in the past compared with unexposed females. This differential allocation extended to how males cared for the resulting offspring of these matings: fathers provided less parental care to offspring of females that had experienced predation risk in the past. Our results show for the first time, to our knowledge, that variation among females in their predator encounters can contribute to behavioural variation among males in courtship and parental care, even when males themselves do not encounter a predator. These results, together with previous findings, suggest that maternal predator exposure can influence offspring development both directly and indirectly, through how it affects father care.     

Effects of courtship and relative mate size on sexual motivation in Atlantic salmon

Both sexes of Atlantic salmon Salmo salar were very sensitive to the absence of their mate on the spawning ground, particularly females during the last hour before oviposition. The improvement of behavioural chaining just before viposition might elicit the accurate timing of synchronized gamete release for successful fertilization. While the reproductive behaviour of the opposite sex could largely affect breeding activity, relative mate size appeared to be the prevailing sexual motivation factor in this species. Even in the absence of courtship, large mate size may constitute a supra-stimulus inducing an increase in spawning behaviour of the other sex. Females with smaller males delayed their first spawning activity, took longer to spawn and made more nests than those with large males. However, female egg retention was not influenced by relative male size.     

Sex and context: hormones and primate sexual motivation

Gonadal hormones regulate the ability to copulate in most mammalian species, but not in primates because copulatory ability has been emancipated from hormonal control. Instead, gonadal hormones primarily influence sexual motivation. This separation of mating ability from hormonally modulated mating interest allows social experience and context to powerfully influence the expression of sexual behavior in nonhuman primates, both developmentally and in adulthood. For example, male rhesus monkeys mount males and females equally as juveniles, but mount females almost exclusively as adults. Having ejaculated with a female better predicted this transition to female mounting partners than did increased pubertal testosterone (T). It is proposed that increased pubertal T stimulates male sexual motivation, increasing the male's probability of sexual experience with females, ultimately producing a sexual preference for females. Eliminating T in adulthood reduces male sexual motivation in both humans and rhesus monkeys, but does not eliminate the capacity to engage in sex. In male rhesus monkeys the effects of reduced androgens on sexual behavior vary with social status and sexual experience. Human sexual behavior also varies with hormonal state, social context, and cultural conventions. Ovarian hormones influence female sexual desire, but the specific sexual behaviors engaged in are affected by perceived pregnancy risk, suggesting that cognition plays an important role in human sexual behavior. How the physical capacity to mate became emancipated from hormonal regulation in primates is not understood. This emancipation, however, increases the importance of motivational systems and results in primate sexual behavior being strongly influenced by social context.     

Social environment affects female and egg testosterone levels in the house sparrow (Passer domesticus)

Maternal effects can have an adaptive value if they improve the performance of offspring. As such, the transfer of maternal testosterone (T) to the eggs has been suggested as a mechanism for adaptive maternal control of offspring phenotype in birds, although recent studies have shown negative effects of testosterone on hatching rate and chick survival. Here, we experimentally investigated whether socially stressful conditions experienced by female house sparrows during egg laying affected their circulating levels of androgens and the amount transferred to the eggs. Social stress was simulated by the intrusion of a foreign male placed near the nest box during the egg‐laying sequence. We found that (1) both female and yolk testosterone titres were positively related to breeding density; (2) yolk testosterone was negatively correlated with maternal testosterone; (3) yolk testosterone was positively correlated with the behavioural response of females towards the intruder and (4) the interaction between social intrusion and breeding density affected the amount of testosterone transferred to the eggs. Altogether, our results suggest that females may be able to modulate the amount of testosterone they allocate to their eggs according to the social environment they experience during egg laying.     

Visual sex discrimination in goldfish: seasonal, sexual, and androgenic influences

The olfactory signals used by goldfish for sexual and aggressive communication have been studied extensively, but little work has addressed the role of other sensory modalities in social communication in this species. We therefore investigated the role that visual stimuli play in sex discrimination and the ability of androgens, which masculinize courtship behavior, to affect behavioral responses toward female visual stimuli. We found that males selectively orient toward female visual stimuli during the breeding season but not outside it, whereas prostaglandin F2-alpha (PGF2alpha)-injected females do not differentially approach male and female visual stimuli, even during the breeding season. Implanting adult females with testosterone (T) and 11-ketotestosterone (KT), however, induced orientation responses toward female visual stimuli similar to those observed in males. These results indicate that visual sexual stimuli are likely important for reproductive signaling in goldfish, potentially helping males identify ovulating females from a distance in a shoal of fish, and that androgens can influence mechanisms associated with orientation responses toward such stimuli.     

Consistency of females’ stridulatory behaviour during inter‐sexual interactions in spiders

In a sexual context, it is expected that females base their choice of mate on the behaviours that males perform during courtship, as such behaviours are associated with the male's mate quality. Stridulation is one form of female communication in arthropods, for example, spiders. In spiders, stridulation during sexual interactions is relatively common in some groups but mainly restricted to males. In the pholcid spider Holocnemus pluchei (Pholcidae), both sexes have stridulatory organs. The aims of the present work were to: (a) determine possible differences in the frequency of occurrence of stridulation between females during inter‐sexual interactions, (b) establish female consistency in stridulation along repeated interactions and (c) analyse if female stridulation is associated with certain male behaviours during pre‐copulatory courtship and with male size. Female H. pluchei showed highly repeatable differences in their frequency of stridulation across consecutive encounters with males (ICC = 0.64). However, only a modest level of repeatability was detected in total time females spent stridulating across trials (ICC = 0.19). Females’ mean stridulatory behaviour did not change across ten consecutive trials spread across 20 days, and their behaviour was apparently unaffected by male persistence of copulatory attempted and/or size. These results imply that the frequency of female stridulatory behaviour is a trait that is highly characteristic of each individual. Finally, our work opens the door to determine whether behavioural consistency manifests in other ecological contexts and their functional implications.     

Sexual and maternal behaviour at the postpartum oestrus: The role of experience in time-sharing

The postpartum sexual and maternal behaviour of Norway rats (Rattus norvegicus) was observed in a seminatural habitat. Behavioural decision-making by the female was examined by disrupting the nest and newborn offspring during mating. In experiment 1, multiparous females responded to nest disruption with an increase in maternal behaviour that was largely restricted to the post-ejaculatory intervals. The temporal and frequency measures of copulation were largely unaffected, implicating behavioural time-sharing. In experiment 2, following nest disruption primiparous females did not switch efficiently between maternal and sexual behaviour, showed poor retrieval of pups, and returned to the nest during ejaculatory series. They did not display the characteristics of behavioural time-sharing, indicating that previous experience may play a role in the ability to time-share.     

SEXUAL SELECTION IN A WOLF SPIDER: MALE DRUMMING ACTIVITY,BODY SIZE,AND VIABILITY

Females are often believed to actively choose highly ornamented males (males with extravagant morphological signals or intense sexual display), and ornaments should be honest signals of male viability. However, this belief is relying only on some pieces of empirical evidence from birds. Our study reports active female choice on sexual display that indicates male viability in spiders. We established trials in which we studied female choice in relation to male courtship drumming activity and body size. Females chose the most actively drumming males as mating partners, but the body size of the males did not seem to be selected. Male drumming activity turned out to be a good predictor of male viability, whereas male viability was independent of male body mass. Our results suggest that by actively choosing mates according to male drumming performance, but independently of male body mass, females are preferring viable males as mates. Because Hygrolycosa rubrofasciata males do not provide obvious direct benefits to their offspring, females may gain some indirect benefits; offspring may have higher chance of survival, or the offspring may inherit the attractiveness of their father.