Multi-scale habitat selection affects offspring survival in a precocial species

In theory, habitat preferences should be adaptive. Accordingly, fitness is often assumed to be greater in preferred habitats; however, this assumption is rarely tested and, when it is, the results are often equivocal. Habitat preferences may not directly convey fitness advantages if animals are constrained by tradeoffs with other selective pressures like predation or food availability. We address unresolved questions about the survival consequences of habitat choices made during brood-rearing in a precocial species with exclusive maternal care (mallard Anas platyrhynchos, n = 582 radio-marked females on 27 sites over 8 years). We directly linked duckling survival with habitat selection patterns at two spatial scales using logistic regression and model selection techniques. At the landscape scale (55–80 km²), females that demonstrated stronger selection of areas with more cover type 4 wetlands and greater total cover type 3 wetland area (wetlands with large expanses of open water surrounded by either a narrow or wide peripheral band of vegetation, respectively) had lower duckling survival rates than did females that demonstrated weaker selection of these habitats. At finer scales (0.32–7.16 km²), females selected brood-rearing areas with a greater proportion of wetland habitat with no consequences for duckling survival. However, females that avoided woody perennial habitats composed of trees and shrubs fledged more ducklings. The relationship between habitat selection and survival depended on both spatial scale and habitats considered. Females did not consistently select brood-rearing habitats that conferred the greatest benefits, an unexpected finding, although one that has also been reported in other recent studies of breeding birds.     

Post-hatching parental care behaviour and hormonal status in a precocial bird

In birds, the link between parental care behaviour and prolactin release during incubation persists after hatching in altricial birds, but has never been precisely studied during the whole rearing period in precocial species, such as ducks. The present study aims to understand how changes in parental care after hatching are related to circulating prolactin levels in mallard hens rearing ducklings. Blood was sampled in hens over at least 13 post-hatching weeks and the behaviour of the hens and the ducklings was recorded daily until fledging. Contacts between hens and the ducklings, leadership of the ducklings and gathering of them steadily decreased over post-hatching time. Conversely, resting, preening and agonistic behaviour of hens towards ducklings increased. Plasma prolactin concentrations remained at high levels after hatching and then fell after week 6 when body mass and structural size of the young were close to those of the hen. Parental care behaviour declined linearly with brood age, showed a disruption of the hen-brood bond at week 6 post-hatching and was related to prolactin concentration according to a sigmoid function. Our results suggest that a definite threshold in circulating prolactin is necessary to promote and/or to maintain post-hatching parental care in ducks.     

A chemical signal of offspring quality affects maternal care in a social insect

Begging signals of offspring are condition-dependent cues that are usually predicted to display information about the short-term need (i.e. hunger) to which parents respond by allocating more food. However, recent models and experiments have revealed that parents, depending on the species and context, may respond to signals of quality (i.e. offspring reproductive value) rather than need. Despite the critical importance of this distinction for life history and conflict resolution theory, there is still limited knowledge of alternative functions of offspring signals. In this study, we investigated the communication between offspring and caring females of the common earwig, Forficula auricularia, hypothesizing that offspring chemical cues display information about nutritional condition to which females respond in terms of maternal food provisioning. Consistent with the prediction for a signal of quality we found that mothers exposed to chemical cues from well-fed nymphs foraged significantly more and allocated food to more nymphs compared with females exposed to solvent (control) or chemical cues from poorly fed nymphs. Chemical analysis revealed significant differences in the relative quantities of specific cuticular hydrocarbon compounds between treatments. To our knowledge, this study demonstrates for the first time that an offspring chemical signal reflects nutritional quality and influences maternal care.     

Sexual dimorphism,survival, and parental investment in relation to offspring sex in a precocial bird

Differential growth rate between males and females, owing to a sexual size dimorphism, has been proposed as a mechanism driving sex‐biased survival. How parents respond to this selection pressure through sex ratio manipulation and sex‐biased parental investment can have a dramatic influence on fitness. We determined how differential growth rates during early life resulting from sexual size dimorphism affected survival of young and how parents may respond in a precocial bird, the black brant Branta bernicla nigricans. We hypothesized that more rapidly growing male goslings would suffer greater mortality than females during brood rearing and that parents would respond to this by manipulating their primary sex ratio and parental investment. Male brant goslings suffered a 19.5% reduction in survival relative to female goslings and, based on simulation, we determined that a female biased population sex ratio at fledging was never overcome even though previous work demonstrated a slight male‐biased post‐fledging survival rate. Contrary to the Fisherian sex ratio adjustment hypothesis we found that individual adult female brant did not manipulate their primary sex ratio (50.39% male, n = 645), in response to the sex‐biased population level sex ratio. However, female condition at the start of the parental care period was a good predictor of their primary sex ratio. Finally, we examined how females changed their behavior in response to primary sex ratio of their broods. We hypothesized that parents would take male biased broods to areas with increased growth rates. Parents with male biased primary sex ratios took broods to areas with higher growth rates. These factors together suggest that sex‐biased growth rates during early life can dramatically affect population dynamics through sex‐biased survival and recruitment which in turn affects decisions parents make about sex allocation and sex‐biased parental investment in offspring to maximize fitness.     

Factors affecting offspring survival and development in a cooperative bird: social, maternal and environmental effects

1. In many noncooperative vertebrates, maternal effects commonly influence offspring survival and development. In cooperative vertebrates, where multiple adults help to raise young from a single brood, social effects may reduce or replace maternal effects on offspring. 2. Factors affecting offspring survival and development at different stages (fledging, nutritional independence and adulthood) were tested in the cooperatively breeding Arabian babbler to determine the relative importance of social, maternal and environmental factors at each stage. An influence of maternal effects was found during the nestling stage only. 3. Social factors affected the survival and development of young at all stages. The amount of food received from helpers influenced post-fledging weight gain, development of foraging skills, and survival to reproductive age. Environmental effects were also important, with groups occupying high-quality territories more likely to produce young that survived to maturity. 4. The strong influence of helper contributions on the survival and development of young at all stages from hatching to maturity suggests social factors may have important long-term effects on offspring fitness in cooperative societies. Traditional measures of offspring survival in cooperative birds, which commonly measure survival to fledging age only, may underestimate the significant benefit of helper contributions on the survival and development of young.     

Environmental and not maternal effects determine variation in offspring phenotypes in a passerine bird

Maternal and environmental effects can profoundly influence offspring phenotypes, independent of genetic effects. Within avian broods, both the asymmetric post‐hatching environment created by hatching asynchrony and the differential maternal investment through the laying sequence have important consequences for individual nestlings in terms of the allocation of resources to body structures with different contributions to fitness. The purpose of this study was to evaluate the relative importance of post‐hatching environmental and maternal effects in generating variation in offspring phenotypes. First, an observational study showed that within blue tit, Cyanistes caeruleus, broods, late‐hatched nestlings allocated resources to tarsus development, maintained mass gain and head‐bill growth and directed resources away from the development of fourth primary feathers. Second, a hatching order manipulation experiment resulted in nestlings from first‐laid eggs hatching last, thereby allowing comparison with both late and early‐hatched nestlings. Experimental nestlings had growth patterns which were closer to late‐hatched nestlings, suggesting that within‐brood growth patterns are determined by post‐hatching environmental effects. Therefore, we conclude that post‐hatching environmental effects play an important role in generating variation in offspring phenotypes.     

Effects of egg yolk testosterone on growth and immunity in a precocial bird

In oviparous vertebrates, maternal steroid allocation to eggs can have important fitness consequences for the offspring. However, elevated testosterone levels are not only associated with beneficial postnatal effects, such as enhanced growth and high social status, but may also entail costs by suppressing the immune system. In this study, testosterone levels in eggs of Chinese painted quail (Coturnix chinensis) were experimentally manipulated to evaluate its effects on growth and immunocompetence. Testosterone did not affect embryonic development, body size or growth during the first 20 days. However, elevated testosterone levels during embryonic development were immunosuppressive for chicks with inherently higher growth rate. Adaptive scenarios where only beneficial effects of increased testosterone levels are considered may therefore need to be re-evaluated.     

Prenatal light exposure affects development of behavioural lateralization in a livebearing fish

The existence of individual differences in handedness and other lateralized functions is an unresolved problem. Genetic factors account for only a small proportion of the variance but the contribution of environmental influences is still largely unexplored. In chicks and zebrafish the amount of environmental light reaching embryos during development greatly influences the lateralization of adults. To investigate whether a similar effect is present in livebearers, we measured behavioural lateralization in ten-day-old goldbelly topminnows born from females that have been maintained at high or low light intensities during pregnancy. Fish from high-light treatment were significantly lateralized in both visual and motor tests while fish exposed to low light intensities were not. As observed in chicks and zebrafish, the main consequence of light exposure was the alignment of the laterality of different individuals in the same direction. Lateralization is known to affect a number of fitness-related traits in topminnow and we suggest that light influence may be part of an adaptive mechanism allowing to adjust the developmental trajectories of offspring to the prevailing environmental conditions.     

Interaction between maternal effects: onset of incubation and offspring sex in two populations of a passerine bird

Maternal phenotype and maternal environment can profoundly affect the phenotype and fitness of offspring. Yet the causes of variation in such maternal effects are rarely known. Embryos in avian eggs cannot develop without being incubated and this creates an opportunity for maternal control of duration and onset of offspring development. However, females might adjust the start of incubation (e.g., coincident with the first egg or delayed until after egg-laying) in response to environmental conditions that they experience at the time of breeding. We studied two populations of the house finch ( Carpodacus mexicanus) that breed at the climatic extremes of the species' geographical range (Montana and Alabama) and found that in both populations, the timing of incubation onset was closely associated with the bias in the sequence in which male and female eggs were laid within a clutch. When females started incubation with the first egg, they produced sons and daughters in highly biased sequence, when females delayed the onset of incubation until after the egg-laying, the sequence of sons and daughters was not biased. Because in both populations, onset of incubation was associated with the ambient temperature, these results emphasize that maternal effects on offspring can be influenced by ecological conditions experienced by parental generation.     

Chronic maternal stress affects growth, behaviour and hypothalamo-pituitary-adrenal function in juvenile offspring

Maternal stress during pregnancy, particularly that combined with low socioeconomic status (SES), has been linked to an increased risk for impaired behavioural and emotional development and affective disorders in children. In animal models, acute periods of prenatal stress have profound effects on hypothalamo-pituitary-adrenal (HPA) function and behaviour. However, few studies have determined the impact of chronic exposure to stress in animal models. The objective of this study was to determine the effects of chronic maternal stress (CMS) during the 2nd half of pregnancy and nursing on growth, locomotor behaviour and HPA axis function in juvenile guinea pig offspring. Pregnant guinea pigs were exposed to a random combination of variable stressors every other day over the 2nd half of gestation and from postnatal day (pnd) 1 until weaning (pnd25). CMS mothers displayed increased basal salivary cortisol levels in the later stages of pregnancy compared to control mothers (p < 0.05). The male offspring of CMS mothers had a lower bodyweight, which was maintained to weaning (p < 0.01). In open-field testing, CMS male offspring showed a decrease in activity compared to controls (p < 0.05). There was no effect of CMS on bodyweight or activity in female offspring. In contrast, both male and female offspring born to CMS mothers displayed increased (p < 0.05) basal salivary cortisol at pnd25, but a blunted adrenocortical response to exposure to the novel open-field enclosure. In conclusion, CMS leads to modification of growth trajectory, locomotor activity and adrenocortical responses to stress in juvenile offspring. Further, males appear considerably more vulnerable to these effects than females.     

Maternal postpartum learned helplessness (LH) affects maternal care by dams and responses to the LH test in adolescent offspring

It is known that the early environment affects the mental development of rodent and human offspring. However, it is not known specifically whether a postpartum depressive state influences the depressive state in offspring. Using learned helplessness (LH) in rats as an animal model of depression, we examined the influence of maternal postpartum LH on responses to the LH test of offspring. Dam rats were judged as LH or non-helpless (nLH) on postnatal days (PN) 2-3, and maternal behavior was recorded during PN2-14. On PN 45-46, offspring were subjected to the LH test. Plasma corticosterone (CORT) levels, hippocampal levels of glucocorticoid receptor (GR) and brain-derived neurotrophic factor (BDNF) mRNA were measured before and after the LH test in offspring. Active nursing in LH dams was significantly lower than that in nLH dams. Susceptibility to LH in the offspring of LH dams was significantly higher than in those of nLH dams, and was negatively correlated with active nursing by LH dams. The GR mRNA levels before and after the LH test were lower in the offspring of LH dams than in those of nLH dams, and the reduced basal GR mRNA and protein might have resulted in the higher CORT response after the LH test. There was no significant difference in BDNF mRNA in the offspring of LH and nLH dams. These findings suggest that early postpartum LH decreased active nursing and increased depression-like behavior in the adolescent offspring via dysfunction of the hypothalamic-pituitary-adrenal axis.     

Larger clutch size increases fledging success and offspring quality in a precocial species

1. We tested the hypothesis that the ability of parents to raise viable offspring limits clutch size in the greater snow goose ( Anser caerulescens atlanticus L.), a precocial bird.
2. We manipulated clutch size by exchanging complete clutches between pairs of nests to increase or decrease the clutch size by zero (control), one, two or three eggs in 314 nests over 2 years.
3. Pre-fledging survival of goslings increased in enlarged broods and decreased in reduced broods compared to control. Consequently, enlarged broods fledged more offspring and the reverse was true for reduced broods.
4. Size and mass of goslings near fledging was also higher in enlarged broods than in control, which suggests that offspring quality was also enhanced by the manipulation. This is contrary to the common trade-off between offspring numbers and quality.
5. Large families were dominant over smaller ones in feeding sites, which could explain the increased survival and growth of enlarged broods.
6. Our results suggest that the ability to raise young does not limit clutch size in this species and that parents could be more successful (i.e. increase both the number and quality of their offspring) by laying more eggs. However, the time required to lay additional eggs reduces the viability of all offspring and may explain why females do not lay more eggs.     

Maternal photoperiodic history affects offspring development in Syrian hamsters

During the first 7 weeks of postnatal life, short day lengths inhibit the onset of puberty in many photoperiodic rodents, but not in Syrian hamsters. In this species, timing of puberty and fecundity are independent of the early postnatal photoperiod. Gestational day length affects postnatal reproductive development in several rodents; its role in Syrian hamsters has not been assessed. We tested the hypothesis that cumulative effects of pre- and postnatal short day lengths would restrain gonadal development in male Syrian hamsters. Males with prenatal short day exposure were generated by dams transferred to short day lengths 6 weeks, 3 weeks, and 0 weeks prior to mating. Additional groups were gestated in long day lengths and transferred to short days at birth, at 4 weeks of age, or not transferred (control hamsters). In pups of dams exposed to short day treatment throughout gestation, decreased testis growth was apparent by 3 weeks and persisted through 9 weeks of age, at which time maximum testis size was attained. A subset of males (14%), whose dams had been in short days for 3 to 6 weeks prior to mating displayed pronounced delays in testicular development, similar to those of other photoperiodic rodents. This treatment also increased the percentage of male offspring that underwent little or no gonadal regression postnatally (39%). By 19 weeks of age, males housed in short days completed spontaneous gonadal development. After prolonged long day treatment to break refractoriness, hamsters that initially were classified as nonregressors underwent testicular regression in response to a 2nd sequence of short day lengths. The combined action of prenatal and early postnatal short day lengths diminishes testicular growth of prepubertal Syrian hamsters no later than the 3rd week of postnatal life, albeit to a lesser extent than in other photoperiodic rodents.     

Sperm variation within a single ejaculate affects offspring development in Atlantic salmon

It is generally believed that variation in sperm phenotype within a single ejaculate has no consequences for offspring performance, because sperm phenotypes are thought not to reflect sperm genotypes. We show that variation in individual sperm function within an ejaculate affects the performance of the resulting offspring in the Atlantic salmon Salmo salar. We experimentally manipulated the time between sperm activation and fertilization in order to select for sperm cohorts differing in longevity within single ejaculates of wild caught male salmon. We found that within-ejaculate variation in sperm longevity significantly affected offspring development and hence time until hatching. Whether these effects have a genetic or epigenetic basis needs to be further evaluated. However, our results provide experimental evidence for transgenerational effects of individual sperm function.     

Parental quality and egg size affect chick survival in a precocial bird, the lapwing Vanellus vanellus

Effects of egg size and parental quality on lapwing Vanellus vanellus chick survival were studied in southwestern Sweden over 6 years. Chicks from large eggs were heavier at hatching and survived significantly better than those from small eggs. To control for the confounding effect of parental quality on egg size and chick survival, we performed a cross-fostering experiment during 2 years, exchanging clutches between nests with large and small eggs. In control clutches, chicks from large eggs survived better than those from small eggs, but we found no significant difference in chick survival between exchanged clutches. Thus, egg size did not affect chick survival independently of parental quality. Fledging success increased with parental age and/or experience, and with female body mass. Hence, both egg size and parental quality affect chick survival in the lapwing. Received: 22 February 1996 / Accepted: 30 September 1996     

The quantitative genetic basis of offspring solicitation and parental response in a passerine bird with biparental care.

The coevolution of parental investment and offspring solicitation is driven by partly different evolutionary interests of genes expressed in parents and their offspring. In species with biparental care, the outcome of this conflict may be influenced by the sexual conflict over parental investment. Models for the resolution of such family conflicts have made so far untested assumptions about genetic variation and covariation in the parental resource provisioning response and the level of offspring solicitation. Using a combination of cross-fostering and begging playback experiments, we show that, in the great tit (Parus major), (i) the begging call intensity of nestlings depends on their common origin, suggesting genetic variation for this begging display, (ii) only mothers respond to begging calls by increased food provisioning, and (iii) the size of the parental response is positively related to the begging call intensity of nestlings in the maternal but not paternal line. This study indicates that genetic covariation, its differential expression in the maternal and paternal lines and/or early environmental and parental effects need to be taken into account when predicting the phenotypic outcome of the conflict over investment between genes expressed in each parent and the offspring.     

Effects of experimentally manipulated yolk thyroid hormone levels on offspring development in a wild bird species

Maternal effects are a crucial mechanism in a wide array of taxa to generate phenotypic variation, thereby affecting offspring development and fitness. Maternally derived thyroid hormones (THs) are known to be essential for offspring development in mammalian and fish models, but have been largely neglected in avian studies, especially in respect to natural variation and an ecological context. We studied, for the first time in a wild species and population, the effects of maternally derived THs on offspring development, behavior, physiology and fitness-related traits by experimental elevation of thyroxine and triiodothyronine in ovo within the physiological range in great tits (Parus major). We found that elevated yolk TH levels had a sex-specific effect on growth, increasing male and decreasing female growth, relative to controls, and this effect was similar throughout the nestling period. Hatching or fledging success, motor coordination behavior, stress reactivity and resting metabolic rate were not affected by the TH treatment. We conclude that natural variation in maternally derived THs may affect some offspring traits in a wild species. As this is the first study on yolk thyroid hormones in a wild species and population, more such studies are needed to investigate its effects on pre-hatching development, and juvenile and adult fitness before generalizations on the importance of maternally derived yolk thyroid hormones can be made. However, this opens a new, interesting avenue for further research in the field of hormone mediated maternal effects.     

Effect of maternal obesity on diabetes development in adult rat offspring

This study aimed to evaluate whether maternal obesity leads to the onset of diabetes in adult Wistar rats offspring. MSG solution neonatally administration induced obesity in rats (F(1)MSG group, n=30); and saline solution was also administrated to control rats (F(1)CON group, n=13). In 3rd month of age, both control and MSG groups were mated for offspring (generation F(2)), named as F(2)CON, n=28 and F(2)MSG groups, n=15; and so both generations were studied until 7th month of life. Lee Index was measured for experimental obesity validation from 5th to 7th month. Glycemia was weekly determined during pregnancy and monthly from 3rd to 7th month. In the end of experimental period all rats were submitted to oral glucose tolerance test (OGTT), with estimation of total area under the curve (AUC); and insulin tolerance test (ITT). Rats were then anesthetized and killed. Data were statistically analyzed with significance level of p<0.05. Lee Index has confirmed obesity in all MSG rats. Glycemic levels comparisons between generations showed significant maternal interference in control and MSG groups. OGTT analysis showed higher glycemia in obese rats (F(1)MSG) and their offspring (F(2)MSG) as compared to their respective controls; and MSG groups increased AUC from OGTT. As regards ITT, F(2)MSG showed higher glycemia at 30 and 120 min, suggesting a delay of insulin action decreasing. Although glucose intolerance and insulin resistance clinical conditions represent as a factors for type 2 Diabetes mellitus development, this experimental model proposal was not efficient to induce type 2 Diabetes mellitus, but for obesity developing, glucose intolerance and insulin resistance in successive generations of rats.