Sex-specific activity and function of hypothalamic nonapeptide neurons during nest-building in zebra finches

Vertebrate species from fish to humans engage in a complex set of preparatory behaviors referred to as nesting; yet despite its phylogenetic ubiquity, the physiological and neural mechanisms that underlie nesting are not well known. We here test the hypothesis that nesting behavior is influenced by the vasopressin–oxytocin (VP–OT) peptides, based upon the roles they play in parental behavior in mammals. We quantified nesting behavior in male and female zebra finches following both peripheral and central administrations of OT and V_1a receptor (OTR and V1aR, respectively) antagonists. Peripheral injections of the OTR antagonist profoundly reduce nesting behavior in females, but not males, whereas comparable injections of V1aR antagonist produce relatively modest effects in both sexes. However, central antagonist infusions produce no effects on nesting, and OTR antagonist injections into the breast produce significantly weaker effects than those into the inguinal area, suggesting that antagonist effects are mediated peripherally, likely via the oviduct. Finally, immunocytochemistry was used to quantify nesting-induced Fos activation of nonapeptide neurons in the paraventricular and supraoptic nuclei of the hypothalamus and the medial bed nucleus of the stria terminalis. Nest-building induced Fos expression within paraventricular VP neurons of females but not males. Because the avian forms of OT (Ile⁸-OT; mesotocin) and VP (Ile³-VP; vasotocin) exhibit high affinity for the avian OTR, and because both peptide forms modulate uterine contractility, we hypothesize that nesting-related stimuli induce peptide release from paraventricular vasotocin neurons, which then promote female nesting via peripheral feedback from OTR binding in the oviduct uterus.     

Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches

Yolk androgens affect offspring hatching, begging, growth and survival in many bird species. If these effects are sex-specific, yolk androgen deposition may constitute a mechanism for differential investment in male and female offspring. We tested this hypothesis in zebra finches. In this species, females increase yolk-testosterone levels and produce male-biased sex ratios when paired to more attractive males. We therefore predicted that especially sons benefit from elevated yolk androgens. Eggs were injected with testosterone or sesame oil (controls) after 2 days of incubation. Testosterone had no clear effect on sex-specific embryonic mortality and changed the pattern of early nestling mortality independent of offspring sex. Testosterone-treated eggs took longer to hatch than control eggs. Control males begged significantly longer than females during the first days after hatching and grew significantly faster. These sex differences were reduced in offspring from testosterone-treated eggs due to prolonged begging durations of daughters, enhanced growth of daughters and reduced growth of sons. The results show that variation in maternal testosterone can play an important role in avian sex allocation due to its sex-specific effects on offspring begging and growth.     

Sex-specific effects of maternal immunization on yolk antibody transfer and offspring performance in zebra finches

Trans-generational antibody transfer constitutes an important mechanism by which mothers may enhance offspring resistance to pathogens. Thus, differential antibody deposition may potentially allow a female to differentiate offspring performance. Here, we examined whether maternal immunization with sheep red blood cells (SRBC) prior to egg laying affects sex-specific yolk antibody transfer and sex-specific offspring performance in zebra finches (Taeniopygia guttata). We showed that immunized mothers deposit anti-SRBC antibodies into the eggs depending on embryo sex and laying order, and that maternal exposure to SRBC positively affects the body size of female, but not male offspring. This is the first study reporting sex-specific consequences of maternal immunization on offspring performance, and suggests that antibody transfer may constitute an adaptive mechanism of maternal favouritism.     

The effects of an aromatization inhibitor on the reproductive behavior of male zebra finches

Recent evidence indicates that aromatizable androgens are more effective than nonaromatizable androgens in restoring normal levels of sexual behavior in castrated male zebra finches (Poephila guttata). To determine whether the efficacy of treatment with aromatizable androgens, is in part due to their conversion to estrogens, castrated male finches were treated with androstenedione (AE), an aromatizable androgen, and their sexual and aggressive behavior was compared with that of castrates treated with AE plus 1,4,6-androstatriene-3,17-dione (ATD), an aromatization inhibitor. Males treated with AE + ATD showed less courtship activity and less copulatory behavior than AE-treated males, and were unlikely to have nests. Estradiol (E), when given concurrently with AE + ATD, reversed the inhibitory effects of ATD and restored levels of courtship and copulation to those observed in AE-treated males. Only AE- and AE + ATD + E-treated males displayed aggressive behaviors, but the frequency of such behaviors was so low that there were no significant differences across groups. These data affirm the importance of estrogen in the control of reproductive activities in male zebra finches and indicate that aromatization may be an obligatory step for maintaining normal levels of sexual and aggressive behavior.     

Negative effects of elevated testosterone on female fecundity in zebra finches

Although factors influencing androgen deposition in the avian egg and its effects on nestling fitness are recently receiving considerable attention, little is known about the potential costs of high testosterone levels in the females. Our study aimed at determining the effect of injections of testosterone (T) in female zebra finches (Taeniopygia guttata), on clutch size, egg mass, yolk mass, and yolk androgen content. Females were given a single bolus injection of T in a range of doses after laying the first egg. Results show that administration of T negatively affected clutch size; the strength of this effect increased with increasing doses of T. Females injected with the highest testosterone dose showed suppressed oviposition of the third and the fourth eggs. Interestingly, testosterone administration made females produce eggs with relatively large yolks, suggesting that T may mediate the trade-off between number and size of eggs. Testosterone injection resulted in elevated levels of androgen in the eggs, in contrast to control clutches, which showed a decreasing pattern of androgen concentration along the laying sequence. We conclude that high androgen investment in eggs may be limited by physiological requirements of the ovulatory process.     

Sound-induced brain activity depends on stimulus subjective salience in female zebra finches

A key point in the study of acoustic perception is whether brain responsiveness to sounds depends on sound acoustic structure or sound perceptive salience. Songbirds provide some evidence that higher auditory regions are sensitive to the subjective importance of the stimulus for the subject. In the present paper, we compare brain activation elicited by mate versus non-mate calls in female zebra finches Taeniopygia guttata. Using playback, we examined the responsiveness of the caudal telencephalon by measuring the evoked expression of the immediate early gene ZENK. Our results show that mate calls elicit a significantly higher ZENK expression than the calls of another male in hippocampus, but not in auditory areas. Using a hierarchical ascending classification, we show that this difference in brain activation is not explained by call acoustic structure, but relies on call identity. Thus, these results give evidence for a genomic response to calls in hippocampus that differentiate between call identity, and not between call structure. Our study gives further insight into the implication of the hippocampus in sound recognition in female songbirds.     

Working and scrounging by zebra finches in an operant task

Groups of three zebra finches were housed in cages which could be adjoined to an operant chamber. Food was restricted and its availability was signalled by a red light projected behind an operant key (an autoshaping procedure). In addition to the shaping contingency, a single peck to the illuminated key, produced food immediately. Following the first peck to the illuminated key, by any subject in the group, the entire group was placed on a schedule of continuous reinforcement (CRF) wherein hopper operation was contingent upon a keypeck during the light. Comparison of individual's behavior revealed a differential pattern of operant working; one group member worked consistently, one worked periodically and one made few (if any) operant responses. All members consumed some reinforcers. The results suggest that zebra finches, under certain conditions, will form specialized labor roles. These data support similar demonstrations with primates (Chalmeau, R. and Galleau A., 1993. Behav. Processes, 28: 173–180), pigeons (Giraldeau, L. and Lefebvre L., 1987. Anim. Behav., 35: 387–394.) and rats (Thullier, F., Desor, D., Mos, J. and Krafft, B., 1992. Psychol. Behav., 53, 17–20).     

Long-term effects of manipulated natal brood size on metabolic rate in zebra finches

Long-term effects of developmental conditions on health, longevity and other fitness components in humans are drawing increasing attention. In evolutionary ecology, such effects are of similar importance because of their role in the trade-off between quantity and quality of offspring. The central role of energy consumption is well documented for some long-term health effects in humans (e.g. obesity), but little is known of the long-term effects of rearing conditions on energy requirements later in life. We manipulated the rearing conditions in zebra finches (Taeniopygia guttata) using brood size manipulation and cross-fostering. It has previously been shown in this species that being reared in a large brood has negative fitness consequences, and that such effects are stronger in daughters than in sons. We show that, independent of mass, standard metabolic rate of 1-year-old birds was higher when they had been reared in a large brood, and this is to our knowledge the first demonstration of such an effect. Furthermore, the brood size effect was stronger in daughters than in sons. This suggests that metabolic efficiency may play a role in mediating the long-term fitness consequences of rearing conditions.     

Metabolic ageing in individual zebra finches

Oxidative stress is suggested as a contributor to the ageing process. Knowledge of the relationship between age and energy expenditure may contribute to our understanding of ageing patterns, due to the link between oxygen consumption and free radical production. However, studies on basal metabolic rate (BMR) and age have generally been cross-sectional, which may confound estimates of the age effect due to disproportionate mortality (also known as 'selective disappearance'). We therefore performed a longitudinal study of BMR using captive zebra finches (Taeniopygia guttata) up to 5 years of age. BMR declined with age in individuals of both sexes when body mass was controlled for. Males gained mass with age while females did not. There was no evidence for disproportionate mortality with respect to BMR in either sex. To our knowledge, this is the first longitudinal study of avian BMR over such a long proportion of the lifespan of the study species.     

Song discrimination learning in zebra finches

Young male and female zebra finches, Taeniopygia guttata, were tested for their ability to discriminate between the song of their father or tutor and that of another male in two types of preference test, one with a male whose song was dissimilar to that of the father or tutor and one with a male who sang a similar song, on removal from the father, at 4 months and at 6 months of age. Birds that were isolated from their father at 25 days (group A) did not show a preference for their father's song whereas those isolated from the father at 35 days (groups B and C) learnt to prefer their father's song. In addition, group C, which were housed with tutor 1 from 35 to 70 days and with tutor 2 from 4 to 6 months of age, preferred their tutors' songs to those of other males. If one compares the strength of preference in the two types of test, group B showed a weaker preference for the father in tests with the father and a similar male. Further, group C showed a weaker preference in the test with tutor 1 versus a similar male. The possible influence of tutor, sibling and own song on the discrimination of the father's song is discussed, and the results are compared with those for song performance learning. Finally, the mother birds preferred their mate's song.     

Transgenerational effects on body size caused by early developmental stress in zebra finches

The nutritional and social conditions that individuals experience during early development can have profound effects on their morphology, physiology, behaviour and life history. Experimental increases in brood size in birds can result in reduced offspring condition and survival, indicating that developmental deficits in enlarged broods have negative fitness consequences within the affected generation. To study long-term effects (i.e. transgenerational effects of developmental stress), we conducted a two-step breeding experiment in which we manipulated early developmental conditions in zebra finches Taeniopygia guttata. We raised zebra finches by manipulating brood sizes and controlled for maternal and genetic effects by cross-fostering. In a previous study, we showed that offspring condition and body size decreased with increasing brood size. Here we show that this effect was carried over to the next generation. Body size in nestlings and at nutritional independence was affected by the brood size in which the mothers were raised. Female offspring did significantly worse than male offspring when the mother had been raised in large broods, suggesting a sex-specific influence of maternal effects. These findings link early developmental stress in females with the phenotype of the next generation via maternal effects.     

Sex-dependent effects of nutrition on telomere dynamics in zebra finches (Taeniopygia guttata)

At a cellular level, oxidative stress is known to increase telomere attrition, and hence cellular senescence and risk of disease. It has been proposed that dietary micronutrients play an important role in telomere protection due to their antioxidant properties. We experimentally manipulated dietary micronutrients during early life in zebra finches (Taeniopygia guttata). We found no effects of micronutrient intake on telomere loss during chick growth. However, females given a diet high in micronutrients during sexual maturation showed reduced telomere loss; there was no such effect in males. These results suggest that micronutrients may influence rates of cellular senescence, but differences in micronutrient requirement and allocation strategies, probably linked to the development of sexual coloration, may underlie sex differences in response.     

Modeling immune responses with handling time

Simple predator-prey type models have brought much insight into the dynamics of both nonspecific and antigen-specific immune responses. However, until now most attention has been focused on examining how the dynamics of interactions between the parasite and the immune system depends on the nature of the function describing the rate of activation or proliferation of immune cells in response to the parasite. In this paper we focus on the term describing the killing of the parasite by cell-mediated immune responses. This term has previously been assumed to be a simple mass-action term dependent solely on the product of the densities of the parasite and the immune cells and does not take into account a handling time (which we define as the time of interaction between an immune cell and its target, during which the immune cell cannot interact with and/or destroy additional targets). We show how the handling time (i) can be incorporated into simple models of nonspecific and specific immunity and (ii) how it affects the dynamics of both nonspecific and antigen-specific immune responses, and in particular the ability of the immune response to control the infection.     

Factors limiting song acquisition in adult zebra finches

Song learning takes place in two separate or partially overlapping periods, a sensory phase in which a tutor song is memorized and a sensorimotor phase in which a copy of the model is produced. The stage of song development where song becomes stable and stereotyped is called crystallization. Adult birds usually do not learn new song in many species including the zebra finch. However, it is not known whether song crystallization as such or aging impedes adult learning. Exposure to loud noises prevents birds from developing and crystallizing their song, because they cannot control their voice by auditory feedback. Zebra finches even without previous experience of hearing or singing a song failed to learn a song model provided in adulthood. Thus, neither the absence of a tutor song nor the lack of song crystallization enables new song learning in adulthood, but age per se limits the ability or motivation to learn song. © 2009 Wiley Periodicals, Inc. Develop Neurobiol 2009     

Male bill colour and competition in zebra finches

Several studies have assessed the role of bill colour in sexual selection and especially with respect to sexual preferences. Even though there are indications that bill colour is related to male quality, so far it has not been shown that bill colour influences male-male interaction. We used male zebra finches with artificially coloured bills in a competitive context to measure the effect of bill colour. In these tests the experimental bird could choose between two feeding sites, each near a stimulus bird with a different bill colour. We tested orange against red, no bird against orange/red and orange/red against green respectively. We found no difference in behaviour towards an orange compared to a red billed stimulus. However the birds spent relatively more time eating when alone compared to being close to a potential competitor. In addition, more time was spent eating than on other behaviours when the birds were close to the orange/red billed stimulus compared to the green billed stimulus. So, although no effect was found in the orange against red test, the results suggest that bill colour may play some role in male-male interaction.