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.     

Brood sex ratios, female harem status and resources for nestling provisioning in the great reed warbler (Acrocephalus arundinaceus)

The theory of parental investment and brood sex ratio manipulation predicts that parents should invest in the more costly sex during conditions when resources are abundant. In the polygynous great reed warbler, Acrocephalus arundinaceus, females of primary harem status have more resources for nestling provisioning than secondary females, because polygynous males predominantly assist the primary female whereas the secondary female has to feed her young alone. Sons weigh significantly more than daughters, and are hence likely to be the more costly sex. In the present study, we measured the brood sex ratio when the chicks were 9 days old, i.e. the fledging sex ratio. As expected from theory, we found that female great reed warblers of primary status had a higher proportion of sons in their broods than females of lower (secondary) harem status. This pattern is in accordance with the results from two other species of marsh-nesting polygynous birds, the oriental reed warbler, Acrocephalus orientalis, and the yellow-headed blackbird Xanthocephalus xanthocephalus. As in the oriental reed warbler, we found that great reed warbler males increased their share of parental care as the proportion of sons in the brood increased. We did not find any difference in fitness of sons and daughters raised in primary and secondary nests. The occurrence of adaptive sex ratio manipulations in birds has been questioned, and it is therefore important that three studies of polygynous bird species, including our own, have demonstrated the same pattern of a male-biased offspring sex ratio in primary compared with secondary nests. Received: 1 June 1999 / Received in revised form: 10 January 2000 / Accepted: 12 February 2000     

Local mate competition in the solitary parasitoid wasp <Emphasis Type="Italic">Ooencyrtus kuvanae</Emphasis>

Local mate competition (LMC) occurs when brothers compete with each other for mating opportunities, resulting in selection for a female-biased sex ratio within local groups. If multiple females oviposit in the same patch, their sons compete for mating opportunities with non-brothers. Females, in the presence of other females, should thus produce relatively more sons. Sex ratio theory also predicts a more female-biased sex ratio when ovipositing females are genetically related, and sex-ratio responses to foundress size if it differentially affects fitness gains from sons versus daughters. The mating system of the parasitoid wasp Ooencyrtus kuvanae meets assumptions of LMC. Females insert a single egg into each accessible egg of gypsy moth, Lymantria dispar, host egg masses. Wasps complete development inside host eggs and emerge en masse, as sexually mature adults, resulting in intense competition among brothers. We tested the hypothesis that O. kuvanae exhibits LMC by manipulating the number of wasp foundresses on egg masses with identical numbers of eggs. As predicted by LMC theory, with increasing numbers of wasp foundresses on an egg mass, the proportions of emerging sons increased. In contrast, the presence of a sibling compared to a non-sibling female during oviposition, or the size of a female, did not affect the number or sex ratio of offspring produced. The O. kuvanae system differs from others in that larvae do not compete for local resources and thus do not distort the sex ratio in favor of sons. With no resource competition among O. kuvanae larvae, the sex ratio of emergent son and daughter wasps is due entirely to the sex allocation by ovipositing wasp foundresses on host egg masses.     

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.     

Evidence of equal maternal investment in the sexes in the polygynous and sexually dimorphic grey seal (Halichoerus grypus)

In polygynous and sexually dimorphic mammals, parents may be expected to bias their investment towards sons because variation in reproductive success is usually higher among males than among females. Moreover, male reproductive success often depends on adult body size, which, in turn, may depend on the level of parental investment. We therefore predicted that in the grey seal (Halichoerus grypus), a polygynous and sexually dimorphic phocid seal, females should invest more in individual sons than in individual daughters. We found that male pups were born heavier than female pups, but that the growth rates and suckling behaviour were similar for the two sexes. The growth rates and the birth weights were not correlated for the pups of either sex. Mothers did not behave differentially towards offspring of the two sexes, except that mothers of male pups spent more time in visual contact with their pups. Male and female pups had similar activity levels and begged at similar rates. We argue that reports of equal expenditure on the two sexes can be accepted as evidence of equal investment, provided that three assumptions are fulfilled. First, parental care must be costly to the parent. Second, energy expenditure must be the most important component of parental investment. Third, there must be no negative correlation between maternal body condition and the ratio of sons to daughters produced. We argue that these assumptions are met in our study, and that our results provide evidence of equal maternal investment in the sexes in grey seals.     

Maternal investment and sex-allocation in the Galapagos fur seal,Arctocephalus galapagoensis

Summary Maternal investment and sex-allocation were measured in a large, sexually dimorphic mammal, the Galapagos fur seal (Arctocephalus galapagoensis). The sex ratio at birth was 1.06. Males were always heavier than females and, at least initially, grew faster. Growth was variable from year to year suggesting energetic constraints on maternal investment. Sucking time conrrelated with milk intake. Mothers suckled yearling and 2-year-old sons more than daughters of the same age. Age at weaning appeared to be the same in both sexes or even slightly greater in males. No sex differences was found in mortality prior to weaning or in post-weaning dispersal. Birth rates of females with yearlings or 2-year-olds were significantly lower than those of females with no dependent young. Mothers invested more in sons than in daughters until weaning. It is unlikely that higher post-weaning investment in daughters balances the higher pre-weaning investment in sons. Data on sex ratio at birth, different growth rates, and weaning age of the sexes are typical of otariid seals as a group. The results of this study fit Maynard Smith's (1980) model of the evolution of sex allocation better than Fisher's (1930).     

Parental investment and the secondary sex ratio in northern elephant seals

Summary Data on northern elephant seals, Mirounga angustirostris, bearing on sex ratio theory were collected at Año Nuevo, California, and other Californian and Mexican Islands, during the period 1967 to 1988. The mass of males exceeded that of females by 7–8% at birth and at weaning. The sex ratio was biased to males at birth (51.2%) and was near unity at weaning (49.6% males). The sex ratio did not vary as a function of maternal age or maternal mass except in 6-year-old females, who produced significantly more males. Although sons cost more to rear in energetic terms than daughters, and mothers were more successful weaning the latter, the sex of the pup reared exerted no significant effect on the mother's reproductive performance the following year or on her subsequent survival. These data suggest that parents invest equally in sons and daughters when investment is measured in terms of future reproduction (Fisher 1930) and provide no support for the theory of adaptive shifts in sex ratio (Trivers and Willard 1973). The small sex difference in mass due to maternal effort reflects the fact that females fast during lactation and all energy transferred is from limited body stores. Because of these circumstances, selection for superior condition at the end of the period of parental investment may act more strongly on pups, who have the opportunity to steal milk, than on their mothers.     

Sex ratio and maternal rank in wild spider monkeys: when daughters disperse

Summary Data from a long-term field study of the spider monkey, Ateles paniscus, in Peru indicate that a strongly female-biased sex ratio exists from birth in this population. Of 46 infants born between July 1981 and June 1986, 12 were male, 32 were female and 2 were of undetermined sex. This effect is consistent between years as well, with more females than males born in each year of the study (Table 1). This bias is driven by the fact that low-ranking females produce daughters almost exclusively, while high-ranking females bias their investment somewhat less strongly towards sons (Table 2). The unusual pattern of female-biased maternal investment observed in this population of Ateles probably occurs for a combination of the following reasons: (1) maternal investment in individual male offspring is somewhat greater than in individual female offspring; (2) males remain with their natal groups, and the sons of high-ranking females are likely to be competitively superior to the sons of low-ranking females; (3) males compete for mates, and only the one or two most dominant males within a community are likely to achieve significant reproductive success. Two possible mechanisms of sex-ratio adjustment and the evidence for each are discussed.     

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.     

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.     

Conditional sex allocation in the Red Mason bee, Osmia rufa

Trivers' and Willard's hypothesis that natural selection favors sex allocation in relation to maternal condition assumes iteropary. Though this assumption is not met in most solitary Aculeata, the reproductive life span of semelparous females may be divided into discrete successive cycles by the risk of open-cell parasitism. Females can avoid losing their investment to parasites attacking the open cell only by limiting the provision time for each cell. The restriction of time available for the investment in a single progeny irrespective of the condition of the female leads to de facto iteropary. Moreover, in Hymenoptera, there are no costs for sex allocation due to the haplodiploid mode of sex determination. In sexually size dimorphic species, females in poor condition are predicted to invest in the smaller sex and vice versa. The resulting prediction of a conditional sex allocation in solitary Aculeata was tested in the Red Mason bee, Osmia rufa (Osmia bicornis), a stem or hole-nesting, polylectic, univoltine megachilid bee. Body size is a key component of condition in females of nest-constructing solitary bees. Large females collect the same amount of pollen and nectar in a shorter time than small ones and should suffer less from parasitism. We found that small females dealt with their handicap of a low provisioning performance by shifting the sex ratio toward sons (the smaller sex) and by reducing the body size of daughters. Large females, however, shifted their offspring sex ratio toward daughters, the sex that depends more on body size in its reproductive value. The sex ratio in the population met the expected Fisherian sex ratio. Although females allocated their investment in the sexes according to their body mass, the population-level investment was balanced.     

Androgen-dependent maternal effects on offspring fitness in zebra finches

There is accumulating evidence that maternal hormones may play a role in offspring sex adjustment, but little is known about the costs of such hormone-mediated mechanisms. Recent studies have reported sex-specific effects of hormones on offspring viability. Specifically, we previously found that elevating the plasma androgen level in mothers results in a male-biased offspring primary sex ratio, but it affects the viability of sons negatively and daughters positively in zebra finches (Taeniopygia guttata; Rutkowska and Cichoń, Anim Behav, 71:1283–1288, 2006). In this study, we studied further fitness consequences of exposure to elevated yolk androgen levels in zebra finches. We measured growth rate and cellular immune response of nestlings that hatched from eggs laid by females injected with testosterone during egg laying and nestlings of unaffected control females. We found that sons of testosterone-treated females grew slower in comparison to sons of control females. The significant interaction between experimental group and offspring sex indicates that sons of testosterone-treated mothers suffered impaired immune responsiveness while daughters seemed to benefit from elevated androgen level in terms of enhanced immune responsiveness. We found no effects of androgens on offspring performance at adulthood—neither fecundity of females nor attractiveness of males was affected. We conclude that the benefits of biasing sex ratio towards males by increasing androgen level in the yolk may be limited due to negative effects on male offspring performance early in life.     

Adaptive sex allocation by brood reduction in antechinuses

Antechinuses (Dasyuridae: Marsupialia) exhibit dramatic interpopulation variation in the sex ratio at birth, a pattern which has previously been interpreted in terms of both local resource competition and Trivers/Willard effects. However, Antechinus stuartii usually fail to wean all the young that attach to their teats. At least in captivity, this is because they often eat their young. In free-living populations, brood reduction affects sons and daughters differently. Mothers virtually always wean some daughters. The probability that a daughter will be weaned declines with the number of daughters in the pouch. The health or quality of the mother does not affect the number of daughters weaned. By contrast, mothers tend to wean all or none of their sons. A strong correlate of infanticide against sons is senescence. Old mothers rarely invest in sons, and produce low-quality daughters. Mothers suffer a direct cost (mortality during lace lactation) of male-biased litters. Coupled with data on prenatal sex allocation, these results support the conjoint influence of local resource competition and the Trivers-Willard effect. However, they suggest that in populations where females are largely semelparous, the population optimum generated by local resource competition may be unattainable, because of the importance of producing at least one daughter. These observations support recent theoretical claims that the sex ratio at the population level is not easily predicted, but suggest that the diversity of mammalian sex allocation tactics has been underestimated.     

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.     

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.     

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.     

Flight initiation distance decreases during social activity in lizards (<Emphasis Type="Italic">Sceloporus virgatus</Emphasis>)

Flight initiation distance, the predator–prey distance when escape begins, is predicted by escape theory to decrease if fleeing entails loss of benefits. Shortening of flight initiation distance during social interactions is known only in males and only in a few species. In a previous study, male, but not female, Sceloporus virgatus lizards had shorter flight initiation distance when interacting with tethered conspecifics. Females in that study were not gravid or close to ovulating. I predicted that flight initiation distance would be shorter in gravid females that perform sidle-hopping displays to reject courtship than in lone females. I tested this prediction and examined effects of social interactions by males with free-ranging conspecifics to ensure that previous findings were not artifacts of tethering and experimental introduction of conspecifics. Flight initiation distance was shorter in females when interacting with males than when alone; it was also shorter in males interacting with either sex. Thus, when beneficial for reproductive reasons, social interaction affects flight initiation distance in females, but at other times, it does not. Lesser shortening of flight initiation distance in females than males may be a consequence of greater social benefit to males and protection of reproductive investment by females.     

Male-biased maternal expenditure and associated costs in fallow deer

This study tested whether fallow deer mothers, Dama dama, bias their investment towards sons and, thus, whether sons are more costly to produce than daughters. Young (2 years) and old (≥3 years) hinds were analysed separately. Old hinds who raised sons accumulated less body mass than those who raised daughters, during the period between late gestation and the end of lactation. This difference in body mass persisted to the following spring. Mothers who had raised sons gave birth later and their offspring's pre-winter mass was lower the following year than for mothers who had raised daughters. These results indicate higher expenditure for hinds who raise sons and support theories of male-biased maternal investment. However, young mothers with sons and those with daughters did not differ in reproductive performance the following year. One reason might be that young mothers are close to the maximum level of maternal expenditure, since they are still growing, and cannot invest any extra resources in sons. Received: 28 August 1997 / Accepted after revision: 5 April 1998     

Biased primary sex ratio in the bushcricket Poecilimon veluchianus,an insect with sex chromosomes

Offspring sex ratio at hatching was examined in the bushcricket Poecilimon veluchianus. Offspring sex ratios varied significantly between females (Fig. 1). Low mortality prior to sex determination established that this heterogeneity was already present in the primary offspring sex ratio. Sperm age and female age had no influence on offspring sex ratio (Fig. 2). Male age at copulation, however, correlated significantly with offspring sex ratio (Fig. 3). There were two types of males: one type produced predominantly daughters when young and an increasing proportion of sons with age. The other type produced, independent of age, 1:1 offspring sex ratios (Fig. 4). The two types of males seem to occur in approximately equal numbers. Sex ratio variation (1) may adaptively compensate for local sex ratio biases caused by sex-specific motility, or (2) it may be adaptive if there is a sex-differential effect of laying date on offspring fitness. Received: 14 March 1996/Accepted after revision: 24 June 1996