Divorce in the socially monogamous zebra finch: Hormonal mechanisms and reproductive consequences

Up to 80% of all bird species are socially monogamous. Divorce (switching partners) or pair disruption (due to the death of a partner) has been associated with decreased reproductive success, suggesting social monogamy is a strategy that may maximize fitness via coordination between partners. Previous studies have demonstrated the effects of divorce and pair disruption on immediate reproductive success. Here, we used a paired experimental design in the zebra finch (Taeniopygia guttata) to examine the hormonal mechanisms that modulate parental behavior and reproductive success in response to a partnership change (hereafter divorce). Specifically, we examined the effects of divorce on the avian stress hormone corticosterone (CORT) in both parents and nestlings, parental behaviors (incubation and nestling provisioning), prolactin (PRL), and reproductive success. We found that divorce resulted in delayed clutch initiation, reduced clutch mass, and an increase in nestling CORT response to a standardized stressor. These effects on reproductive investment and chick CORT response were not clearly determined by parental endocrine responses. Divorce had no effect on the level of parental CORT. PRL levels were highly correlated within a pair regardless of treatment, were negatively related to the investment that males made in incubation, and increased in experimental males as a result of pair disruption. This study demonstrates the fundamental impact which divorce has not only on reproduction, but also the physiological stress responses of offspring and suggests that in socially monogamous animals the maintenance of a stable partnership over time could be advantageous for long term fitness.     

Sexual selection and extrapair fertilization in a socially monogamous passerine, the zebra finch (Taeniopygia gullata)

We investigated paternal exclusion rate (the percentage of youngreared by a male that were not his genetic offspring), and behavioraland reproductive variables influencing this rate, in a freelybreeding laboratory population of zebra finches (Tae-niopygiaguttala castanotis), a socially monogamous grassfinch. Priorto the experiment, each male founder was fitted with eithertwo red bands (creating a phenotype previously demonstratedto be attractive to females) or two green bands (unattractiveto females) as part of a unique combination of four leg bands.The overall paternal exclusion rate was 28%, as determined bymultilocus, minisatellite DNA fingerprinting of 278 offspringreared by 26 males and their mates. Mean exclusion rates were16% and 40% for red- and green-banded males, respectively. Exclusionrates were directly proportional to rates of female participationin unforced extrapair copulations (UEPCs) with red-banded malesthat occurred when females were fertile. Rates of fertile, forcedextrapair copulations (FEPCs) and fertile UEPCs involving green-bandedmales either failed to influence exclusion rate or varied inverselywith exclusion rate, indicating that extrapair fertilization(EPF) is under female control. Effort devoted by males to seekingEPFs increased exclusion rate. Results suggest that males placegreater effort into seeking fertile versus infertile EPCs andthat unattractive males accrue fitness gains through high parentalinvestment (PI), whereas attractive males benefit through decreasedPI and increased allocation to EPF.     

Sex ratios and sexual selection in socially monogamous zebra finches

An experiment was performed in which adult sex ratios of zebrafinches, Taeniopygyia guttata castanotis, were varied to testpossible effects of adult population sex ratios on sexual selectionintensity and mating system dynamics in species with biparentalcare. The possibility that sex ratio influences the successof social mating patterns (leading to polygyny when males arerare and polyandry when females are rare) was not supported.Results did support the prediction of the differential allocationhypothesis that individuals of the abundant sex would increasetheir relative parental expenditure (PE). Although total (male+ female) PE did not vary between treatments, relative malePE was significantly higher in the male-biased treatment (MBT;sex ratio 64% male) than in the female-biased treatment (FBT; sexratio 36% male). In both treatments, male PE contributions contributedto female reproductive rate. Results also supported the predictionof the differential access hypothesis that individuals of theabundant sex would experience greater intensity of selectionon sexually selected attributes. Male beak color, a sexuallyselected trait, influenced male social parentage in the MBTbut not in the FBT. Finally, broods in the FBT displayed higher hatchingasynchrony and lower hatching success; we believe this was causedby early onset of incubation, a tactic used as a defense againstintraspecific brood parasitism, which was much higher in theFBT. Population sex ratios may be an important factor affectingfemale ability to influence male parental investment patterns.     

Behavioral and neural lateralization of vision in courtship singing of the zebra finch

Along with human speech and language processing, birdsong has been one of the best-characterized model systems for understanding the relationship of lateralization of brain function to behavior. Lateralization of song production has been extensively characterized, and lateralization of song perception has begun to be studied. Here we have begun to examine whether behavior and brain function are lateralized in relation to communicative aspects of singing, as well. In order to monitor central brain function, we assayed the levels of several activity dependent immediate early genes after directed courtship singing. Consistent with a lateralization of visual processing during communication, there were higher levels of expression of both egr-1 and c-fos in the left optic tectum after directed singing. Because input from the eyes to the brain is almost completely contralateral in birds, these results suggest that visual input from the right eye should be favored during normal singing to females. Consistent with this, we further found that males sang more when they could use only their right eye compared to when they could use only their left eye. Normal levels of singing, though, required free use of both eyes to view the female. These results suggest that there is a preference for visual processing by the right eye and left brain hemisphere during courtship singing. This may reflect a proposed specialization of the avian left hemisphere in sustaining attention on stimuli toward which a motor response is planned.     

Diet,maternal condition,and offspring sex ratio in the zebra finch,Poephila guttata

Where maternal condition affects condition and reproductive potential of offspring differentially with respect to sex, mothers in relatively good condition should produce more of the sex whose fitness is more dependent on condition. We experimentally manipulated body-condition in unmated zebra finches by feeding them for three months on high- or low-quality diets. Birds were then allowed to breed, while keeping the same diets. Females on the lower quality diet were in better condition and hatched significantly more males than females. Poorer condition females hatched an equal sex ratio. Chicks fed on the low-quality diet, but not on the high-quality diet, showed female-biased mortality. These results show that facultative sex ratio manipulation and sex-biased mortality can act together to produce extreme sex ratios in this vertebrate.     

Costly steroids: egg testosterone modulates nestling metabolic rate in the zebra finch

The transfer of non-genetic resources from mother to the offspring often has considerable consequences for offspring performance. In birds, maternally derived hormones are known to influence a variety of morphological, physiological and behavioural traits in the chick. So far, the range of these hormonal effects involves benefits in terms of enhanced growth and competitive ability as well as costs in terms of immunosuppression. However, since yolk hormones can enhance growth and begging activity, high levels of these hormones may also involve energetic costs. Here, we show experimentally that elevated levels of prenatal testosterone increase resting metabolic rate in nestling zebra finches (Taeniopygia guttata). Surprisingly, however, elevation of prenatal testosterone did not result in higher growth rates and, thus, differences in resting metabolism do not seem to be linked to nestling growth. We conclude that apart from immunosuppressive effects, high levels of egg steroids may also entail costs in terms of increased energy expenditure.     

The evolution of courtship rituals in monogamous species

In this paper we propose an alternative explanation for theevolution of courtship rituals in monogamous species. We demonstrate,using computer simulations, how male courtship might developas males exploit response biases in females to manipulate thefemale into starting reproduction before she has been ableto assess the male's intentions. In our coevolutionary simulations, a recurrent, artificial neural network is used to model thefemale recognition mechanism, while the displaying male isrepresented by a sequence of signals. Our particular modelsituation is just one example of how a reproductive conflictcould result in the evolution of ritualized displays in monogamous species. Since reproductive conflicts occur even after pairformations, the explanation we propose may also apply to ritualsthat occur after pair formation.     

Sexual differentiation of the zebra finch song system parallels genetic, not gonadal, sex.

Mechanisms regulating sexual differentiation of the zebra finch song system present an intriguing puzzle. Masculine development of brain regions and behavior can be induced in genetic females by posthatching estradiol treatment. That result is consistent with the hypothesis that estradiol, converted within the brain from testicular androgen via the aromatase enzyme, masculinizes neural structure and function. In contrast, treatment during specific stages of development with the aromatase inhibitor Fadrozole has not prevented masculine development, and the presence of testicular tissue in genetic females did not induce masculine organization of neuroanatomy or singing behavior. Fadrozole treatments in those previous studies were limited, however, and most genetic females had both ovarian and testicular tissue. The present experiments were designed to provide increased aromatase inhibition and to reliably produce genetic females with only testicular tissue. Eggs received a single injection at a later age or with higher doses of Fadrozole than had been used previously. Some embryos were exposed to Fadrozole more frequently by either injecting eggs on 2 days of development or dipping them for 10-12 days in Fadrozole. Finally, in some individuals from Fadrozole-treated eggs, the left gonad was removed, leaving each genetic male and female with a single right testis. None of these treatments significantly affected development of the song system compared to appropriate control groups. These results suggest that sexual differentiation of the zebra finch song system is not regulated by embryonic aromatase activity or by gonadal secretions and instead involves events that need not be mediated by steroid hormones.     

Does sex matter? Differential responses to corticosterone administration in the zebra finch

Because of potentially deleterious effects of chronic stress, physiological measurements of stress hormones (in birds, corticosterone (CORT)) are often used to determine the consequences of natural or human-induced change. Often, it is assumed that CORT levels will be similar between the sexes and the results are pooled. However, recent studies have reported sex differences in CORT concentrations in avian species. As zebra finches (Taeniopygia guttata) are one of the most widely used bird species in laboratory studies worldwide, potential sex-specific differences in hormone metabolism, as well as the clearance rate of oral doses of exogenous CORT, are highly relevant. The results of this study show that female zebra finches have a significantly higher baseline CORT than males, which could partially be a product of differential responses to semi-isolation. In addition, a single dose of exogenous CORT resulted in different blood profiles between the sexes over time, though exogenous CORT was cleared from blood within 90 min following treatment in both sexes. Interestingly, exposure to multiple doses of exogenous CORT resulted in elevated CORT levels 24 h after treatment in both sexes. These results highlight the need for further investigations into potential sex differences in hormone metabolism, as well as possible cumulative effects of repeated stress.     

The temporal pattern of feeding in the zebra finch

Feeding in zebra finches occurs in clearly defined bouts, but strong individual differences have been found in the finer details of its pattern. Some birds showed a constant probability of starting feeding with passage of time between meals and a constant probability of stopping during a meal. In these cases meal length (number of pecks at seed) tended to correlate with the length of the preceding gap. By contrast, in most individuals both meals and gaps tended to be of a typical length, and in some of these autocorrelation showed feeding to follow a cycle approximately 24 to 30 min long. Meal length in most of these birds correlated strongly with the length of the succeeding gap. The individual differences found are discussed and hypotheses put forward for their causation.     

The zebra finch neuropeptidome: prediction,detection and expression

Background  

Among songbirds, the zebra finch (Taeniopygia guttata) is an excellent model system for investigating the neural mechanisms underlying complex behaviours such as vocal communication, learning and social interactions. Neuropeptides and peptide hormones are cell-to-cell signalling molecules known to mediate similar behaviours in other animals. However, in the zebra finch, this information is limited. With the newly-released zebra finch genome as a foundation, we combined bioinformatics, mass-spectrometry (MS)-enabled peptidomics and molecular techniques to identify the complete suite of neuropeptide prohormones and final peptide products and their distributions.     

Grazing pressure affects offspring sex ratio in a socially monogamous passerine on the Tibet Plateau

Livestock grazing can affect habitat structure and availability of arthropod prey for grassland birds, and ultimately determines habitat quality. The habitat quality may affect breeding strategies (e.g. sex ratio adjustment) in bird species, but studies investigating grazing intensity on offspring sex ratio are still rare. In this paper, we examined the effect of grazing intensity by livestock on the secondary sex ratio of an alpine‐steppe passerine, the isabelline wheatear Oenanthe isabellina, on the Tibet Plateau. Offspring sex ratio of isabelline wheatears significantly correlated with a quadratic term – (grazing intensity)². The wheatears nesting in areas grazed at low intensity by mixed livestocks produced significantly more sons than those in ungrazed area (0.41 vs 0.58, Z = –2.836, p = 0.005), while brood sex ratios from other treatments (ungrazing vs intensive grazing and low‐intensity grazing vs intensive grazing) did not differ significantly. Variation in offspring sex ratio was not related to other factors such as maternal condition, paternal condition and other two‐way interactions. These results suggest that breeding birds of grasslands are sensitive to variation in habitat conditions, and provide additional evidence that grazing intensity affects avian reproduction in cryptic ways that are rarely studied. Our findings suggest that flexible management including timely rotational grazing is needed to optimize bird species reproduction and maintain ecosystem health.     

State-dependent incubation behaviour in the zebra finch

State dependence is thought to be an important factor in resource allocation decisions, particularly in those decisions relating to parental care. Incubation behaviour is a costly part of avian parental care, and therefore likely to depend on the parent's body condition. We manipulated the body condition of zebra finches, Taeniopygia guttata, during incubation by using prelaying diets of different protein content, and induced birds to lay a similar number of eggs. We tested the hypothesis that birds in better body condition would invest more in incubation than birds in poorer condition when incubating on the same diet. Females that had received a high-protein prelaying diet lost more body mass than those that had received a low-protein diet. They also increased the length of their incubation bouts between early and middle incubation, whereas females that had received a low-protein prelaying diet increased bout length only between middle and late incubation. There were no differences between males from the two diet groups, and males were responsible for a lesser proportion of incubation than females. These results indicate that incubation behaviour is state dependent in female zebra finches, and that birds of different body condition adopt different incubation strategies. We found no differences in incubation duration and hatching success between the two incubation strategies in captivity, but the potential risk of nest predation in the wild may differ. We suggest that only females in good condition can afford to adopt a strategy of increasing bout length early in incubation; females in poorer condition first have to recover their body condition after having produced a clutch. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour