Mind the gap: the ratio of yolk androgens and antioxidants varies between sons and daughters dependent on paternal attractiveness

Females are expected to partition resources between offspring in a context-dependent way to maximise total fitness returns from a reproductive attempt. Female zebra finches (Taeniopygia guttata) vary the allocation of yolk androgens and antioxidants among offspring. Importantly, the balance between androgens and antioxidants in yolks may be more important than their independent absolute amounts in terms of fitness consequences for developing young. Therefore, we tested whether the relative allocation of these two resources in yolks varies according to either the Trivers–Willard, positive or compensatory maternal investment hypothesis. We manipulated male attractiveness using coloured leg bands (red-banded males appear attractive; green-banded males, unattractive) and measured yolk androgens and antioxidants in each egg, egg sex, clutch sex ratio and female condition. While female zebra finches manipulated the balance of androgens and antioxidants within and between clutches in response to mate attractiveness, offspring sex and their own condition, they did not do so in a way that consistently followed any of the hypotheses. Mothers paired with unattractive males allocated a larger antioxidant/androgen ratio to daughters than sons. This pattern was reversed when paired to an attractive male; sons received a larger antioxidant/androgen ratio than daughters. We also found offspring sex ratio decreased with increasing female condition for unattractive males, but not for attractive males. However, without knowing the fitness consequences of the balance of different egg constituents, it is difficult to interpret the patterns consistently in terms of the Trivers–Willard, compensatory and positive investment hypotheses.     

Cooperatively breeding superb fairy-wrens show no facultative manipulation of offspring sex ratio despite plausible benefits

We report a long-term study of offspring sex ratios in the cooperatively breeding superb fairy-wren Malurus cyaneus. Detailed study of this species had revealed a suite of potentially strong selection pressures on the sex ratio. First, females gain substantial fitness benefits from the presence of helpers; so females without male helpers would benefit from any strategy that increased the probability of recruiting help, such as overproduction of sons (local resource enhancement hypothesis), but large numbers of helper males compete among themselves, favouring the production of daughters (local resource competition). Second, daughters fledged early in the season have far greater chances of recruitment to the breeding population than late-fledged daughters, so mothers would benefit from production of daughters early in the breeding season (early bird hypothesis). Third, extra-group mate choice imposes strong sexual selection on males, suggesting that females mating with attractive sires could benefit from investing in sons (sexual selection hypothesis). However, the predictions from these and other sex ratio hypotheses were rejected. The only convincing evidence for manipulation of the sex ratio was a slight bias towards sons (11 sons to 10 daughters) that occurred regardless of context. This result does not support current theory.     

Sex allocation in a monomorphic seabird with a single-egg clutch: test of the environment, mate quality, and female condition hypotheses

Sex allocation theory posits that mothers should preferentially invest in sons when environmental conditions are favorable for breeding, their mates are of high quality, or they are in good body condition. We tested these three hypotheses in rhinoceros auklets (Cerorhinca monocerata), monomorphic seabirds that lay a single-egg clutch, in 2 years that differed in environmental conditions for breeding. Results supported the environment and mate quality hypotheses, but these effects were interactive: offspring sex was independent of paternal traits in the poor year for breeding, while females mated to larger and more ornamented males reared more sons in the better year. Conversely, offspring sex was unrelated to female condition, as indexed by hatching date. We propose that good rearing conditions enable females to rear sons possessing the desirable phenotypic attributes of their mates. Results also supported two critical assumptions of sex allocation theory: (1) dimorphism in offspring condition at independence: daughters fledged with higher baseline levels of corticosterone than sons and (2) differential costs of rearing sons versus daughters: mothers rearing sons when environmental conditions were poor completed parental care in poorer condition than mothers rearing daughters in the same year and mothers rearing either sex when conditions were better. These novel results may help to explain the disparate results of previous studies of avian sex allocation.     

Primary sex ratios in zebra finches: no evidence for adaptive manipulation in wild and semi-domesticated populations.

When breeding diet is restricted, domesticated zebra finches,Taeniopygia guttata, produce male-biased primary and secondary sex ratios, but unexpectedly produce unbiased ratios when food is unrestricted. We investigated the primary sex ratios (at laying) of wild zebra finches in southeastern Australia in response to food supplementation and environmental factors predicted to enhance female breeding condition and to bias the primary sex ratio towards daughters. Molecular sexing of all nestlings in 54 complete broods where every egg hatched, failed to show any significant biases from random. Time of egg laying (month, season) and environmental conditions (rainfall, temperature) did not significantly predict variation in the primary sex ratio, but time of breeding did affect clutch size. Wild zebra finches at our colony did not bias their sex allocation as there were no differences in the primary sex ratio and no differences in the numbers and mass of sons and daughters at the end of parental care (day 35–40 post-hatch). Biases in primary sex ratio of our wild population are probably weak or non-existent possibly due to the unpredictable environment and/or multiple contrary selective forces acting on sex ratios. We also investigated the effects of photoperiod, biases in the adult sex ratio, and parental attractiveness on primary sex ratios of semi-domesticated, laboratory zebra finches. Molecular sexing of three-day old embryos from complete clutches, failed to reveal significant biases from random. In contrast to previous studies, sex of eggs did not correlate with laying order and egg mass declined with order, rather than increased. Domestication may be responsible for these differences.     

Female-biased sex allocation of offspring by an <Emphasis Type="Italic">Apodemus</Emphasis> mouse in an unstable environment

We investigated the effects of population fluctuation on the offspring’s sex allocation by a weakly polygynous mouse, Apodemus argenteus, for 3 years. In acorn-poor seasons, heavier mothers invested more in sons, and lighter mothers invested more in daughters. In acorn-rich seasons, heavier mothers invested more in daughters, and lighter mothers invested more in sons. Maternal body condition and litter size affected the sex allocation. Furthermore, there was a maternal investment trade-off between a son’s birth mass and the number of daughters. Based upon the effect of population fluctuation on the lifetime reproductive success of each sex, we proposed the new “safe bet hypothesis”. This hypothesis predicts that frequent and unpredictable change in female distribution, which is often caused by abrupt fall in food condition, favors female-biased maternal investment to offspring by polygynous mammals and is applicable to many small mammals inhabiting in unstable environments.     

Sex allocation and paternity in a cooperatively breeding passerine: evidence for the male attractiveness hypothesis?

Sex allocation theory predicts that female birds with high-quality mates will benefit from producing more sons, since sons will inherit their father’s superior traits and enjoy a great reproductive success, whereas females with low-quality mates will benefit from producing more daughters, since the variance in reproductive success among daughters is typically lower. The male attractiveness hypothesis may apply to extra-pair paternity (EPP) because socially monogamous females routinely mate with higher quality males outside the pair bond. We test these predictions using the Tibetan ground tit (Pseudopodoces humilis), a sexually monomorphic, socially monogamous, facultatively cooperative breeder. There was greater variation in actual reproductive success among males than females due to EPP. An excess of sons was detected for bi-parental (i.e., non-cooperative) broods wherein EPP was mainly sired by bi-parental males. The pattern was attributed to male-biased sex ratios produced for both EPP and within-pair offspring within the same broods. The reason for the latter case might be a random allocation of more offspring to sons by the potentially EPP-exposed females that have an inability to control fertilization by specific males. In cooperative broods where EPP mostly resulted from within-group helpers of presumed low-quality, as indicated by their failure in acquiring a social mate, there was a non-significant tendency for EPP offspring to be daughters and for within-pair offspring in the same broods to be unbiased. These results support the EPP-related male attractiveness hypothesis especially in terms of the overproduction of sons. Offspring produced through quasi-parasitism was unbiased towards either sex, suggesting a weak female choiceness with respect to the quality of host males.     

Effects of prenatal yolk androgens on armaments and ornaments of the ring-necked pheasant

Mothers may profoundly affect offspring phenotype and performance by adjusting egg components, including steroid hormones. We studied the effects of elevated prenatal testosterone (T) exposure in the ring-necked pheasant on the expression of a suite of male and female traits, including perinatal response to stress, immune response, growth, and secondary sexual traits. Prenatal T levels were increased by injecting the yolk of unincubated eggs with physiological doses of the hormone. Yolk T injection resulted in a reduced length of male tarsal spurs, a trait which positively predicts male success in intra- and intersexual selection and viability, whereas no direct effect on male wattle characteristics or plumage traits of either sex was observed. Female spur length was also negatively affected by T, but to a lesser extent than in males. In addition, the covariation between male secondary sexual traits, which are reliable quality indicators, differed between T and control males, suggesting that the manipulation may have altered the assessment of overall male quality by other males and females. In conclusion, the negative effects of elevated yolk T on spur length, a trait which positively predicts male fitness, coupled with the lack of effects on growth or other traits in both sexes, provided limited evidence for mothers being subjected to a trade-off between positive and negative consequences of yolk T deposition on offspring traits and suggest that directional selection for reduced yolk T levels may occur in the ring-necked pheasant.     

Parentally biased favouritism in relation to offspring sex in zebra finches

Family conflicts over parental care result in offspring attempting to exert control using solicitation behaviours, whilst the parents are potentially able to retaliate through provisioning rules. However, the evolutionary interests of one parent may not necessarily support the evolutionary interests of the other parent, and such conflicts of interest may be expressed in how the two parents allocate the same form of parental care to individual offspring. Theory suggests that such parentally biased favouritism is a universally predicted outcome of evolutionary conflicts of interest, and empirical evidence suggests that parentally biased favouritism occurs in relation to offspring size and solicitation behaviours. However, unequivocal empirical evidence of parentally biased favouritism in relation to offspring sex is absent, due to being strongly confounded by sex differences in size and solicitation behaviours. Here, we present strong evidence for parentally biased favouritism in relation to offspring sex in zebra finches (Taeniopygia guttata), independent of the effects of chick size and begging intensity. Mothers preferentially provisioned sons over daughters, whilst fathers showed no bias, meaning that sons received more food than daughters. Parentally biased favouritism in relation to offspring sex facilitates parental control over evolutionary conflicts of interest and is probably more widespread than previously realised.     

Status,reproductive success and fitness in Cape mountain zebra (Equus zebra zebra)

Summary Demographic data relating to herd size and stability are given for a population of Cape mountain zebra (Equus zebra zebra) under longterm observation. Temporal dispersion patterns of male and female offspring differed and were independent of the mother's status. Dispersion in females appeared to be related to physiological state, and dispersion in both sexes was related to age rather than changes in parental behaviour. Reproductive success of dominant and subordinate mares was equal and independent of age and social and reproductive variables. Fitness of dominant mares, however, was significantly higher than that of subordinates, the latter having a higher foal mortality, part of which could be attributable to dominants' aggression. The fitness of all males born was 1.6:1 compared with all females. Dominant mares produced significantly more daughters than sons. This trend was not found for subordinates. Mother's status was positively correlated with dominant status in her female offspring but not related to the subsequent status of her sons. Daughters had a more than twice as great a chance of breeding than sons. For maximum fitness gains, therefore, dominant mares should produce more daughters, since a high proportion of these would also have high status and fitness. This tendency is reflected in the sex ratio skewed towards females found for dominant mares.     

Impacts of flight distance on sex ratio and resource allocation to offspring in the leafcutter bee, Megachile rotundata

Fisher's theoretical prediction of equal investment in each sex for a panmictic population (The genetical theory of natural selection. Clarendon, Oxford, 1930) can be altered by a number of factors. For example, the sex ratio theory predicts variation in equal investment in each sex when the maternal fitness gains from increased investment differ between sexes. Changing sex allocation because of changing payoffs may result from different ecological situations, such as foraging conditions. We investigated the impact of foraging travel cost on relative investment in sons vs daughters. Field studies were carried out with the central-place-foraging leafcutter bee Megachile rotundata (Fabricius), which has smaller males than females. Therefore, less investment is required to produce a viable son compared with a daughter. We found that with increased flight distance to resources, females produced a greater proportion of sons. Females also invested fewer resources in individual sons and daughters and produced fewer offspring with increased flight distance.     

Maternal investment in rhesus macaques (Macaca mulatta): reproductive costs and consequences of raising sons

Maternal investment in offspring is expected to vary according to offspring sex when the reproductive success of the progeny is a function of differential levels of parental expenditure. We conducted a longitudinal investigation of rhesus macaques to determine whether variation in male progeny production, measured with both DNA fingerprinting and short tandem repeat marker typing, could be traced back to patterns of maternal investment. Males weigh significantly more than females at birth, despite an absence of sex differences in gestation length. Size dimorphism increases during infancy, with maternal rank associated with son’s, but not daughter’s, weight at the end of the period of maternal investment. Son’s, but not daughter’s, weight at 1 year of age is significantly correlated with adult weight, and male, but not female, weight accounts for a portion of the variance in reproductive success. Variance in annual offspring output was three- to fourfold higher in males than in females. We suggest that energetic costs of rearing sons could be buffered by fetal delivery of testosterone to the mother, which is aromatized to estrogen and fosters fat accumulation during gestation. We conclude that maternal investment is only slightly greater in sons than in daughters, with mothers endowing sons with extra resources because son, but not daughter, mass has ramifications for offspring sirehood. However, male reproductive tactics supersede maternal investment patterns as fundamental regulators of male fitness. Received: 23 July 1999 / Received in revised form: 23 February 2000 / Accepted: 13 March 2000     

Cooperatively breeding carrion crows adjust offspring sex ratio according to group composition

In cooperatively breeding species, parents should bias offspring sex ratio towards the philopatric sex to obtain new helpers (helper repayment hypothesis). However, philopatric offspring might increase within-group competition for resources (local resource competition hypothesis), diluting the benefits of helper acquisition. Furthermore, benefits of offspring sex bias on parents’ fitness may depend on different costs of production and/or different breeding opportunities of sons and daughters. Because of these counteracting factors, strategies of offspring sex allocation in cooperative species are often difficult to investigate. In carrion crows Corvus corone corone in northern Spain, sons are more philopatric and more helpful at the nest than daughters, which disperse earlier and have higher chances to find a breeding vacancy. Consistent with the helper repayment hypothesis, we found that crows fledged more sons in groups short of subordinate males than in groups with sufficient helper contingent, where daughters were preferred. Crow females also proved able to bias primary sex ratio, allocating offspring sex along the hatching sequence in a way that provided the highest fledging probability to sons in the first breeding attempt and to daughters in the following ones. The higher cost of producing male offspring may explain this pattern, with breeding females shifting to the cheapest sex (female) as a response to the costs generated by previous reproductive attempts. Our results suggest complex adjustments of offspring sex ratio that allowed crows to maximize the value of daughters and sons.     

Optimal investment in sons and daughters when parents do not know the sex of their offspring

Optimal parental investment usually differs depending on the sex of the offspring. However, parents in most organisms cannot discriminate the sex of their young until those young are energetically independent. In a species with physical male–male competition, males are often larger and usually develop sexual ornaments, so male offspring are often more costly to produce. However, Onthophagus dung beetles (Coleoptera; Scarabaeidae) are highly dimorphic in secondary sexual characters, but sexually monomorphic in body size, despite strong male–male competition for mates. We demonstrate that because parents provide all resources required by their offspring before adulthood, O. atripennis exhibits no sexual size dimorphism irrespective of sexual selection pressure favoring sexual dimorphism. By constructing a graphic model with three fitness curves (for sons, daughters, and expected fitness return for parents), we demonstrate that natural selection favors parents that provide both sons and daughters with the optimal amount of investment for sons, which is far greater than that for daughters. This is because the cost of producing small sons, that are unable to compete for mates, is far greater than the cost of producing daughters that are larger than necessary. This theoretical prediction can explain sexual dimorphism without sexual size dimorphism, widely observed in species with crucial parental care such as dung beetles and leaf-rolling beetles, and may provide an insight into the enigmatic relationship between sexual size dimorphism and sexual dimorphism.     

Adaptive significance of sex ratio adjustment in semifree-ranging Barbary macaques (Macaca sylvanus) at Salem

Summary New data on the secondary sex ratio in semi-free-ranging Barbary macaques at Salem confirm the observation that the offspring of high-ranking females in this colony are biased towards sons while the offspring of low-ranking females are biased towards daughters. Analysis of interbirth intervals yielded no consistent differences in the relative costs of rearing male and female offspring for either high- or low-ranking females. Survivorship to adulthood of male and female offspring born to mothers of all rank classes was remarkably high, and there was no indication that juvenile females of low-ranking mothers face any greater risk. Daughters of high- and low-ranking mothers showed no substantial differences in reproductive success, while mating and probably reproductive success of sons seemed to be dependent on maternal rank, at least at the beginning of their reproductive career. The results suggest that variation in sex ratio does increase parental fitness. Offprint requests to: A. Paul     

Long-lasting effects of yolk androgens on phenotype in the pied flycatcher (Ficedula hypoleuca)

The hormonal environment during early development, such as maternally derived androgens in bird eggs, shapes the development of the offspring in ways that may have important long-term consequences for phenotype and behavior and, ultimately, fitness. We studied the long-term effects of yolk androgens on several phenotypic and physiological traits in male and female pied flycatchers (Ficedula hypoleuca) by experimentally elevating yolk androgen levels and rearing birds in common-garden environment in captivity. We found that high yolk androgen levels increased the basal metabolic rates in both females and males in adulthood. High yolk androgen levels did not affect male melanin coloration or plumage ornaments, or timing or speed of moult in either sex. No effect of androgen treatment on cell-mediated or humoral immune response was found in either sex. Covariation among the measured phenotypic traits was further not altered by androgen treatment. Our results suggest that exposure to high androgen levels can have long-lasting effects on some offspring traits, but do not seem to lead to different phenotypes. Furthermore, the role of yolk androgens affecting sexually selected male traits in our study species seems to be minor. The fitness consequences of yolk androgen-induced higher metabolic rates remain to be studied.     

Offspring sex ratio variation in the bridled nailtail wallaby, Onychogalea fraenata

The bridled nailtail wallaby is a sexually size dimorphic, promiscuous, solitary macropod. Sex ratios of pouch young were studied at two sites over 3 years, beginning with 14 months of severe drought. Females that were in better condition were more likely to have sons, and condition was dependent on body size. Females at one site were heavier, were consequently in better condition, and produced more sons than females at the other site. Females that declined in condition had more daughters during the most severe part of the drought than females that maintained condition, but endoparasite infection did not affect the pouch young sex ratio. Age also appeared to affect sex ratio adjustment, because weight was strongly influenced by age. Sex ratio bias was not caused by early offspring mortality, but occurred at conception. Mothers did not appear to bias energy expenditure on sons or daughters; males and females did not differ in condition at the end of pouch life. Pouch young sex ratio variation was most consistent with the Trivers-Willard hypothesis, but could also have been influenced by local resource competition, since sons dispersed further than daughters. Offspring condition was related to survival, and was correlated with maternal condition. Received: 14 April 1998 / Accepted after revision: 10 November 1998     

Sex bias or equal opportunity? Patterns of maternal investment in bison

Summary In polygynous mammals, it may be adaptive for mothers to invest more in sons and/or to adjust the sex ratio of offspring in relation to body condition. Calving patterns were examined over an 8-year period (1982–1989) for a population of Bison bison in which barren females are not selectively culled. From these data, we tested predictions of the sex ratio adjustment hypothesis as well as two assumptions: (1) that offspring weight at the end of the period of parental investment (PI) is correlated with later condition, and (2) that maternal and offspring condition during the period of PI are correlated. In contrast to predictions, there was little evidence that mothers in better condition bear more sons. Short- and long-term measures of maternal condition (previous reproductive status, age, dominance status, pre-pubertal body weight, age at first reproduction, birth date, and the duration of the mother's own suckling period) were little related to offspring sex ratio, although the last calves of old females were nearly always female. Similarly, there was little evidence for sex-biased PI. Weights at about 7 months of age were greater for males than females; males also had somewhat later birth dates, suggesting either longer gestation or later conception. However, maternal reproductive costs, as measured by subsequent fecundity, weight loss, and interbirth intervals, did not vary with calf sex. Both assumptions of the model received some support. However, while maternal condition was correlated with offspring condition, there may be sex differences in investment patterns. Mothers appear better able to influence the condition of daughters than of sons. This sex difference may negate any benefit from male-biased investment.     

Effects of elevated yolk testosterone levels on survival, growth and immunity of male and female yellow-legged gull chicks

Androgen hormones of maternal origin contained in the eggs of avian species are considered to have positive effects on offspring characteristics and performance. However, negative consequences have also been reported, suggesting that mothers may experience a trade-off between beneficial and detrimental effects of egg androgens to offspring fitness. We studied the effects of elevated yolk testosterone (T) concentration on survival, development and phenotype of male and female yellow-legged gull (Larus michahellis) chicks by injecting egg yolks with physiological doses of the hormone. Elevated yolk T resulted in a male-biased post-hatching sex ratio, T-treated clutches producing a greater proportion of males compared to control ones at day 4 post-hatching, likely resulting from a reduction of female embryonic survival, whereas no effect of hormone treatment on hatching success or short-term chick survival was observed. In addition, T depressed post-hatching body mass in both sexes but had no effects on the intensity of the cell-mediated immune response or skeletal growth. No sex differences in egg characteristics or chick phenotype were detected. Time to hatching was not affected by T, but females originating from first laid eggs hatched earlier than males of the same laying order, independently of hormone treatment. However, the implications of sex differences in hatching times are unclear in the study species. Taken together, our results suggest that female yellow-legged gulls may be constrained in transferring androgens to their eggs by negative consequences on the viability of female offspring and growth of chicks of the two sexes.     

Sex-specific effects of yolk-androgens on growth of nestling American kestrels

Maternally derived androgen hormones concentrate in avian egg yolks as the yolks grow on the female’s ovary, possibly forming a basis for important maternal effects in birds. In the American kestrel (Falco sparverius), experimental elevation of yolk androgens in the first-laid egg of a clutch (a-egg) to the concentrations found naturally in a clutch’s later-laid eggs reduces the growth rate of a-egg nestlings compared to controls. These findings, together with discoveries from other species that the effects of yolk androgens on growth of female nestlings may differ from their effects on growth of male nestlings, raise the hypothesis that natural changes in yolk-androgen concentrations with laying order are ultimately due to a difference between the sexes in their yolk-androgen sensitivity and between early- and late-laid eggs in their sex ratio. By re-analyzing previously published data and adding to the analysis data from previously unanalyzed blood samples used for sex determination, we investigated possible sex-specific effects of yolk-androgens in the context of a potential sex-biased laying order in free-living American kestrels. We used a multi-level, mixed model with a Gompertz function to analyze growth of nestlings hatching from a-eggs that were control-treated or in which we experimentally elevated yolk-androgen concentrations shortly after laying to the higher concentrations naturally found in later-laid eggs. We discovered that male nestlings were more susceptible than female nestlings to growth inhibition by yolk-androgen elevation but did not find a bias in sex ratio with respect to laying order. Together, these findings do not support the above hypothesis. However, they are consistent with the hypothesis that sex differences in yolk-androgen sensitivity enable mothers to economically tune reproductive effort to an individual offspring’s reproductive value, which can vary more for one sex than the other.     

Offspring sex ratio response to host size in the parasitoid wasp Spalangia endius

The host size model, an adaptive model for maternal manipulation of offspring sex ratio, was examined for the parasitoid wasp Spalangia endius. In a Florida strain, as the model predicts, daughters emerged from larger hosts than sons, but only when mothers received both small and large hosts simultaneously. The pattern appeared to result from the mother's ovipositional choice and not from differential mortality of the sexes during development. If sex ratio manipulation is adaptive in the Florida strain, it appears to be through a benefit to daughters of developing on large hosts rather than through a benefit to sons of developing on small hosts. Both female and male parasitoids were larger when they developed on larger hosts. For females, developing on a larger host (1) increased offspring production, except for the largest hosts, (2) increased longevity, (3) lengthened development, and (4) had no effect on wing loading. For males, development on a larger host had no effect on any measure of male fitness – mating success, longevity, development duration, or wing loading. In contrast, a strain from India showed no difference in the size of hosts from which daughters versus sons emerged, although both female and male parasitoids were larger when they developed on larger hosts. These results together with previous studies of Spalangia reveal no consistent connection between host-size-dependent sex ratio and host-size-dependent parasitoid size among strains of S. endius or among species of Spalangia. Received: 28 October 1998 / Received in revised form: 20 May 1999 / Accepted: 30 May 1999