Masculinized sexual partner preference in female zebra finches with sex-reversed gonads

Previous research in the zebra finch, a socially monogamous pair-bonding species, suggests that the preference for opposite-sex partners may arise in part through the organizing actions of sex steroids. To further investigate this process, zebra finch eggs were injected with 20 microg fadrozole, a potent estrogen synthesis inhibitor, or with the saline vehicle on embryonic day 5. As adults they were given two-choice sexual partner preference tests followed by group aviary tests. Fadrozole females had masculinized beak color and had testes or ovotestes instead of ovaries. Males were not affected by fadrozole; they did not differ from controls on any measure. In contrast, sexual partner preference was substantially masculinized in fadrozole females in the group aviary tests. Untreated males given a choice between fadrozole and untreated females preferred the untreated females, but this was equally the case when they were given a choice between saline-treated and untreated females. These results suggest that males do not specifically avoid females with testes and that male avoidance is unlikely to explain why fadrozole-treated females pair with other females. The present data add to the evidence that actions of gonadal steroids during development contribute to adult sex differences in partner preference in this pair-bonding species. Furthermore, because fadrozole-treated females do not produce audible song, the mechanisms regulating partner preference and song system development are dissociated.     

Sexual Imprinting in Zebra-finch Females: Do Females Develop a Preference for Males that Look Like Their Father?

Recently, it has been proposed that through sexual imprinting on their parents, young birds learn to discriminate between males and females. Support for this suggestion was given by a study on zebra-finch males Taniopygia guttata, which showed that males of this species develop a strong sexual preference for mother-like females over father-like females. The present study investigates whether zebra-finch females also develop a sexual preference for mates resembling the opposite-sex parent. The females used had been raised either by normal pairs, by white pairs or by pairs of both morphs. The preferences were tested by confronting these females with normal and white males, both in simultaneous two-stimulus tests and successive one-stimulus tests. In contrast to males, females raised by a pair of mixed-morph parents did not show a preference for mating partners of the opposite-sex-parent's morph. Instead, they showed a preference for males of the mother's plumage type. It is suggested that the difference in which sexual imprinting proceeds in males and females may be related to the different role each sex plays in the pair formation.     

An eye for detail: selective sexual imprinting in zebra finches

To investigate the idea that sexual imprinting creates incipient reproductive isolation between phenotypically diverging populations, I performed experiments to determine whether colony-reared zebra finches would imprint on details of artificial white crests. In the first experiment, adults in one breeding colony wore white crests with a vertical black stripe, while in another colony adults wore crests having a horizontal black stripe; except for their crests, breeders possessed wild-type plumage and conformation. Offspring of both sexes reared in these colonies developed mate preferences for opposite-sexed birds wearing the crest type with which they were reared; neither sex developed a social preference for crested individuals of the same sex. In a second experiment, females reared by crested parents preferred crested males versus males with red leg bands, while control females (reared in a colony of wild-type, uncrested birds) preferred red-banded males in the same test. Results of a third experiment that used sexually dimorphic crest phenotypes indicate that both sexes of offspring imprinted on maternal crest patterns. Results support the hypothesis that sexual imprinting can facilitate isolation both by engendering a preference for population-typical traits and by prioritizing such an imprinting-based preference over species-typical preferences for other traits used in mate choice. Comparison with results of other recent studies indicates that imprinting tendencies of both sexes vary with the characteristics of traits presented as an imprinting stimuli. Tendency to imprint may vary with the perceived information content (e.g., kin, sex, or population indicator) of parental traits, a process dubbed selective sexual imprinting.     

Sexual imprinting can induce sexual preferences for exaggerated parental traits

Sexual preferences in animals are often skewed toward mates with exaggerated traits. In many vertebrates, parents provide, through the learning process of "sexual imprinting," the model for the later sexual preference. How imprinting can result in sexual preferences for mates having exaggerated traits rather than resembling the parental appearance is not clear. We test the hypothesis that a by-product of the learning process, "peak shift", may induce skewed sexual preferences for exaggerated parental phenotypes. To this end, zebra finch (Taeniopygia guttata) males were raised by white parents, with beak color as the most prominent sexual dimorphism. We manipulated this feature with nail varnish. At adult age, each male was given a preference test in which he could choose among eight females with beak colors ranging from more extreme on the paternal to more extreme on the maternal side. The males preferred females with a beak of a more extreme color than that of their mothers, i.e., they showed a peak shift. Sexual imprinting can thus generate skewed sexual preferences for exaggerated maternal phenotypes, phenotypes that have not been present at the time of the learning. We suggest that such preferences can drive the evolution of sexual dimorphism and exaggerated sexual traits.     

Testosterone increases singing and aggression but not male-typical sexual partner preference in early estrogen treated female zebra finches

Female zebra finches given estradiol benzoate (EB) as nestlings and testosterone propionate (TP) as adults show masculinized sexual partner preference, preferring females instead of males. This suggests an organizational effect of EB on sexual partner preference in a socially monogamous species that pairs for life. It is not known whether there is an activational hormone effect on sexual partner preference in this species, or whether adult testosterone treatment is necessary for masculinized preference to be expressed. In this experiment females were injected with EB daily for the first 2 weeks posthatching. As adults they were given TP filled or empty implants. Subjects were then given two-choice preference tests with male vs female stimuli, in which singing as well as proximity to the stimuli was recorded, followed by tests in a group aviary for social behavior and pairing preference. Females with TP implants sang more than females with empty implants and were more aggressive toward other females. They did not, however, differ from females with empty implants in any measure of sexual partner preference. Neither group showed a marked preference for males; instead both groups were equally interested in males and females. Thus adult testosterone treatment is not necessary for early estrogen treated females to show a shift in sexual partner preference in the male-typical direction.     

Plumage phenotypes and mate preferences in Japanese quail 2. sexual imprinting

Mate selection, with emphasis on early social (sexual imprinting) and subsequent long-term social experience, was studied in a randombred population of Japanese quail consisting of wildtype (W), redhead (R) and Albino (A) plumage colors. Early social experiences involved situations where flocks of the various plumage colors were maintained either separately or intermingled.Initial mate preferences were determined from a series of paired choice-tests between plumage phenotypes. Wildtype and redhead females exhibited no preferences, while albino hens preferred albino males. Preferences exhibited by albino males depended on sexual imprinting; those with no other experience preferred albinos and redheads to wildtypes, whereas those raised with other morphs did not distinguish among phenotypes. Redhead and wildtype males while avoiding albino hens, did not distinguish between redhead and wildtype hens.Combinations of the plumage color-social experience flocks (A&R; A&W; R&W) were housed for long-term observations of mate selection. Albino hens mated only albino males. Redhead and wildtype hens having previous experience with albinos mated more frequently with albino males than those lacking such experience. Redhead and wildtype hens showed no preference between redhead and wildtype males. Albino males did not distinguish among female plumage colors, whereas redhead and wildtype males avoided albino hens, and mated equally with redhead and wildtype hens. In a series of nonsimultaneous choice trials, redhead and wildtype females were mated significantly more than albinos. These results demonstrate the influence of genetic mechanisms, sexual imprinting and subsequent long-term social experiences on the optimization of mate selection.     

Sexual Partner Preference in Female Zebra Finches: The Role of Early Hormones and Social Environment

This experiment investigated the effects of early estrogen treatment and sex composition of the social environment on sexual partner preference in female zebra finches, a pair-bonding socially monogamous species. Birds were injected daily with estradiol benzoate (EB) or the steroid vehicle for the first 2 weeks posthatch and then lived in either a unisex (all-female) or a mixed sex group from 40 to 100 days. After 100 days birds were implanted with testosterone propionate and given three kinds of tests: tests with a stimulus female, two-choice mate preference tests with male and female stimuli, and colony tests to assess pairing preference in a more naturalistic context. Both EB and unisex housing independently resulted in a preference for females (masculinized preference) in the two-choice tests, but only females with both EB treatment and unisex living were more likely to pair with females in the colony tests. Sexual partner preference, a key sexually dimorphic component of mate choice, appears to be organized by sex steroids in this pair-bonding species, but in a manner that may be mediated by the social environment.     

Sex steroids modulate changes in social and sexual preference during juvenile development in zebra finches

Zebra finches, like many other animals, have close social relationships mainly with the family at young ages but begin to express interest in opposite-sex extra-family animals as they enter the late juvenile period and sexual maturity. This experiment tested a set of hypotheses that sex steroids are involved in this developmental transition. At 25–30 days, subjects were implanted subcutaneously with Silastic tubes that were empty (controls), filled with testosterone propionate, filled with estradiol benzoate, or filled with a combination of ATD (an aromatization inhibitor) and flutamide (an anti-androgen). Once a week between ages 30 and 90 days, they were given three-choice tests where the three stimulus types were the family members, unpaired males, or unpaired females. The preferred category was defined as the one adjacent to the proximity zone in which the subject spent the most time. Control males were more likely to prefer females and less likely to prefer the family as they got older, and control females were increasingly likely to prefer males. Males treated with testosterone or estradiol showed a premature increase in preferences for females. Females treated with ATD plus flutamide failed to show the normal increase in preferences for males shown by controls. These results indicate an involvement of sex steroids in the maturation of sexual preferences in a socially monogamous species that relies on visual and auditory, rather than olfactory, cues for sexual or other social behavior.     

Removal of adult males from the rearing environment increases preference for same-sex partners in the zebra finch

The developmental processes producing preferences for opposite-sex mating partners are not well understood. Zebra finches, Taeniopygia guttata, are colonial and socially monogamous with biparental care. To determine whether the early social environment contributes to sexual partner preference, we removed adult males from breeding colonies when the oldest chicks were less than 1 week old (male-removal rearing) or left them in the breeding cage (control rearing). At independence, male-removal and control offspring were moved to unisex cages. As adults they were given two-choice tests with male versus female stimuli followed by group aviary tests. Male-removal subjects, unlike controls, did not prefer opposite-sex stimuli in the two-choice tests. Male-removal subjects were less likely than controls to successfully pair with opposite-sex birds in the group aviary tests; 38% of them paired with a same-sex bird. Thus early social experience may contribute to a critical component of mate choice, choosing the opposite sex, in this pair-bonding species. Copyright 2000 The Association for the Study of Animal Behaviour.     

Sex steroids modulate changes in social and sexual preference during juvenile development in zebra finches

Zebra finches, like many other animals, have close social relationships mainly with the family at young ages but begin to express interest in opposite-sex extra-family animals as they enter the late juvenile period and sexual maturity. This experiment tested a set of hypotheses that sex steroids are involved in this developmental transition. At 25-30 days, subjects were implanted subcutaneously with Silastic tubes that were empty (controls), filled with testosterone propionate, filled with estradiol benzoate, or filled with a combination of ATD (an aromatization inhibitor) and flutamide (an anti-androgen). Once a week between ages 30 and 90 days, they were given three-choice tests where the three stimulus types were the family members, unpaired males, or unpaired females. The preferred category was defined as the one adjacent to the proximity zone in which the subject spent the most time. Control males were more likely to prefer females and less likely to prefer the family as they got older, and control females were increasingly likely to prefer males. Males treated with testosterone or estradiol showed a premature increase in preferences for females. Females treated with ATD plus flutamide failed to show the normal increase in preferences for males shown by controls. These results indicate an involvement of sex steroids in the maturation of sexual preferences in a socially monogamous species that relies on visual and auditory, rather than olfactory, cues for sexual or other social behavior.     

Bill Color Preferences of Zebra Finches

Bill color varies with age and sex in zebra finches. Among birds of similar age and condition, males' bills tend to be redder and darker than those of females, but there is overlap in the phenotypic expression of the sexes. The bills of young birds are paler and less red than those of older birds. There is also interindividual variation within age and sex class. Experiments were performed to measure heterosexual and isosexual (= same sex) preferences of finches. Females preferred to associate with males with the reddest, brightest bills; they even preferred males whose bills were exaggerated through color applications of non-toxic marking pen. Males preferred to associate with females with bill colors in the middle of the phenotypic range. Females thus have “directional” preferences for male bill color, whereas male preference is “stabilizing” with regard to female bill color. In isosexual tests, neither sex showed a consistent preference for particular bill colors. Both sexes, however, displayed a tendency toward individual variability in preference. Bill color appears to be more important in heterosexual than in isosexual interactions. Several authors have recently suggested that organisms prefer brightly colored mates because bright coloration indicates superior physical condition. Results reported here do not support this hypothesis. Alternative functional explanations for the observed preferences are that bill color signals mating status, age or reproductive value. None of these appears to be a cogent explanation for the trends. Preferences do not appear to result from sexual imprinting. The possibility that the preferences are aesthetic and non-functional is discussed.     

Repeatability of Male Mate Choice in the Mosquitofish, Gambusia holbrooki

Male mate choice has evolved in many species in which female fecundity increases with body size. In these species, males are thought to have been selected to favour mating with large females over smaller ones, thereby potentially increasing their reproductive success. While male mate choice is known to occur, it is less well studied than female mate choice and little is known about variation in mating preference among individual males. Here, we presented individual male eastern mosquitofish ( Gambusia holbrooki ) with paired females that differed in body size, and we quantified their mate preference on two consecutive days, allowing us to assess repeatability of preferences expressed. When males were allowed to view paired stimulus females, but not to acquire chemical or tactile cues from them, they exhibited a strong preference for large females over smaller ones. However, individual males were not consistent in the strength of their preference and repeatability was not significant. When individual males were allowed to fully interact with pairs of females, the males again exhibited a preference for large females over smaller ones, as revealed by a greater number of attempted copulations with large females than with smaller ones. In the latter social context, individual male preference was significantly repeatable. These results indicate that male eastern mosquitofish from our Florida study population possess, on average, a mating preference for larger females and that this preference is repeatable when males socially interact freely with females. The significant repeatability for mating preference, based on female body size, obtained for male mosquitofish in the current study is consistent with the presence of additive genetic variation for such preferences in our study population and thus with the opportunity for the further evolution of large body size in female mosquitofish through male mate choice.     

Sexual Imprinting on a Novel Adornment Influences Mate Preferences in the Javanese Mannikin Lonchura leucogastroides

We investigated whether sexual imprinting on an artificial novel adornment in the Javanese Mannikin Lonchura leucogastroides , a monomorphic estrildid finch, can occur and might provide a mechanism for the evolution of novel traits. We introduced a red feather on the forehead as a novel adornment. Young were raised by parents which were both adorned, which were both unadorned, or only one of which was adorned with the red feather. We tested the female and male offspring of those parents in mate choice tests with an adorned and unadorned conspecific of the opposite sex. Males raised by an adorned mother or adorned parents preferred adorned females significantly more often than males raised by unadorned parents. We conclude that males were sexually imprinted on the red feather. Females raised by an adorned mother or raised by adorned parents significantly preferred adorned males, whereas females raised by unadorned parents showed no preference for adorned males. Thus, females also became imprinted on the red feather. Males might learn the novel adornment in combination with the parent's sex or learn just the most conspicuous sex, whereas females showed a preference for the adornment independent of which sex bore the feather. Our study shows that sexual imprinting might be an effective mechanism for the evolution of a novel trait and that males and females might become imprinted on a novel trait in different ways.     

The coevolution of sexual imprinting by males and females

Sexual imprinting is the learning of a mate preference by direct observation of the phenotype of another member of the population. Sexual imprinting can be paternal, maternal, or oblique if individuals learn to prefer the phenotypes of their fathers, mothers, or other members of the population, respectively. Which phenotypes are learned can affect trait evolution and speciation rates. “Good genes” models of polygynous systems predict that females should evolve to imprint on their fathers, because paternal imprinting helps females to choose mates that will produce offspring that are both viable and sexy. Sexual imprinting by males has been observed in nature, but a theory for the evolution of sexual imprinting by males does not exist. We developed a good genes model to study the conditions under which sexual imprinting by males or by both sexes can evolve and to ask which sexual imprinting strategies maximize the fitness of the choosy sex. We found that when only males imprint, maternal imprinting is the most advantageous strategy. When both sexes imprint, it is most advantageous for both sexes to use paternal imprinting. Previous theory suggests that, in a given population, either males or females but not both will evolve choosiness in mating. We show how environmental change can lead to the evolution of sexual imprinting behavior by both sexes in the same population.     

Female mate preferences for male body size and shape promote sexual isolation in threespine sticklebacks

Female mate preferences for ecologically relevant traits may enhance natural selection, leading to rapid divergence. They may also forge a link between mate choice within species and sexual isolation between species. Here, we examine female mate preference for two ecologically important traits: body size and body shape. We measured female preferences within and between species of benthic, limnetic, and anadromous threespine sticklebacks (Gasterosteus aculeatus species complex). We found that mate preferences differed between species and between contexts (i.e., within vs. between species). Within species, anadromous females preferred males that were deep bodied for their size, benthic females preferred larger males (as measured by centroid size), and limnetic females preferred males that were more limnetic shaped. In heterospecific mating trials between benthics and limnetics, limnetic females continued to prefer males that were more limnetic like in shape when presented with benthic males. Benthic females showed no preferences for size when presented with limnetic males. These results show that females use ecologically relevant traits to select mates in all three species and that female preference has diverged between species. These results suggest that sexual selection may act in concert with natural selection on stickleback size and shape. Further, our results suggest that female preferences may track adaptation to local environments and contribute to sexual isolation between benthic and limnetic sticklebacks.     

Female Cowbird Song Perception: Evidence for Plasticity of Preference

The goal of the research reported here was to look for evidence of modifiability of preference for male song in female cowbirds, Molothrus ater. To this end, we investigated whether social experience affected the breadth and consistency of females’ playback preferences for geographic variants of male song. In three experiments, we varied female cowbirds’ exposure to males. Wild‐caught juvenile females showed a preference for local song in their first year when housed without males in sound‐attenuating chambers, as we had found previously with adult females. But we found that neither adult nor juvenile females showed a preference for local over distant song after they had been housed in large, outdoor aviaries with other females but without male residents. Aviary housing with local males did lead to preferences for local songs. These data represent the first unqualified evidence that adult and juvenile female cowbird preferences for song are modifiable. These data add to the growing body of literature suggesting that receivers, as well as signalers, rely on learning during development of their communication system.     

Exposure to developing females induces polyuria, polydipsia, and altered urinary levels of creatinine, 17β-estradiol, and testosterone in adult male mice (Mus musculus)

Novel male mice can accelerate reproductive maturation in proximal developing females, an effect mediated by the chemistry of the males' urine. Exogenous estrogens can similarly accelerate female sexual development. In Experiment 1, adult male mice were housed across wire grid from either empty compartments or those containing post-weanling females. Proximity of females caused males to urinate more, progressively over days of exposure, with most urination directed towards females' compartments. Male urine collected after 5 days in these conditions was analyzed by enzyme immunoassay for 17β-estradiol, testosterone, and creatinine. Urinary creatinine of isolated males significantly exceeded that of female-exposed males. Unadjusted urinary steroids also trended toward higher levels in isolates, but creatinine-adjusted estradiol and testosterone of female-exposed males significantly exceeded that of isolated males. In Experiment 2, measurement of water consumption indicated significantly greater drinking by female-exposed as opposed to isolated males. In Experiment 3, males were housed in isolation or beside post-weanling intact (sham-operated) females, ovariectomized females, or intact (sham-operated) males. Male water consumption was elevated in all conditions involving social contact. Urinary creatinine was significantly lower in female-exposed males compared to isolated controls, while unadjusted testosterone was significantly lower in males in all social conditions. Again, creatinine-adjusted estradiol in female-exposed males significantly exceeded that of isolates. These data indicate that adult males drink and urinate more, have more dilute urine, and have a higher ratio of estradiol to creatinine when they are near developing females. These dynamics increase females' exposure to urinary steroids and other urinary constituents that can hasten sexual maturity.     

Effect of estradiol-treated females on all-female groups of rhesus monkeys during the transition between the nonbreeding and breeding seasons

Behavior, sex steroid levels and sex skin color were monitored in 2 out-door-housed all-female groups of rhesus monkeys during the nonbreeding season and into the breeding period. Each group contained gonadally intact and ovariectomized (OVX) females. In one group, 2 OVX females were implanted with estradiol benzoate pellets. Female-to-female sexual behavior, sex skin redness and endocrine indices of ovulation (in intact females) all increased as the breeding season approached. The two groups did not differ with regard to these measures. This lack of difference suggests that the presence of males may be required to mediate socially facilitated out-of-season breeding by females. No strong relationships were detected between steroid levels of intact females and sex skin color or female-to-female sexual behavior in all-female groups.     

Sex differences in developmental plasticity and canalization shape population divergence in mate preferences

Sexual selection of high-quality mates can conflict with species recognition if traits that govern intraspecific mate preferences also influence interspecific recognition. This conflict might be resolved by developmental plasticity and learned mate preferences, which could drive preference divergence in populations that differ in local species composition. We integrate field and laboratory experiments on two calopterygid damselfly species with population genetic data to investigate how sex differences in developmental plasticity affect population divergence in the face of gene flow. Whereas male species recognition is fixed at emergence, females instead learn to recognize heterospecifics. Females are therefore more plastic in their mate preferences than males. We suggest that this results from sex differences in the balance between sexual selection for high-quality mates and selection for species recognition. As a result of these sex differences, females develop more pronounced population divergence in their mate preferences compared with males. Local ecological community context and presence of heterospecifics in combination with sex differences in plasticity and canalization therefore shape population divergence in mate preferences. As ongoing environmental change and habitat fragmentation bring formerly allopatric species into secondary contact, developmental plasticity of mate preferences in either or both sexes might facilitate coexistence and prevent local species extinction.     

Social Environment Affects Peripheral Oxytocin and Cortisol during Stress Responses in Guinea-Pigs

Numerous studies have demonstrated interactions between oxytocin (OT) secretion, adrenal activity, an animal's social environment, and stress responses. In the present study, we hypothesized that partner preference and pair bonding cause increased peripheral OT, which down‐regulates the adrenal and behavioral response in stress. In addition, we tested whether these interactions depended on sex, the social environment of the individual, or the type of stressor. Experiments were carried out on guinea‐pigs held in sexual‐pairs or stressed by isolation. Among the paired individuals choice tests were carried out to document partner preference. Female preference for a male was expressed by spatial cohesion. Stress responses to abiotic stimuli were examined and compared between isolated and cohabited animals with or without preference. Results show that OT of cohabited animals was significantly higher than during isolation. OT levels were further increased in males preferred by females. Cortisol (CORT) levels were elevated in isolated animals. There were no significant differences between pairs with and without female preference. Behaviorally, partner preferences were expressed by high amounts of tactile contact. The stress‐induced behavioral immobility response after exposure to a noise stressor was significantly reduced in preferred males and to a lesser extent in their female partners. Only females with preferences showed an endocrine stress response. Their levels of OT increased. There was no consistent post‐stressor release of CORT. The data indicate that the social environment of an individual, here expressed as preference or isolation, influences peripheral OT secretion. Behavioral stress responses were similarly affected by social factors without a clear involvement of peripheral CORT or OT.