Mixed sex allocation strategies in a polytocous mammal,the house mouse (<Emphasis Type="Italic">Mus musculus</Emphasis>)

The issue of adaptive adjustment of offspring sex ratio (proportion of male births) in polytocous mammals, producing several offspring per litter, is controversial because females of these species can maximize their fitness mainly by adjusting offspring number. To address this issue, we examined the effect of maternal condition at mating, experimentally decreased by pre-mating food restriction, on the sex ratio variation in 137 female mice. We tested two basic sex allocation hypotheses plausible for polytocous mammals: (1) the Myers hypothesis, predicting that cheaper sex should be favored in poor environmental conditions to maximize offspring number; and (2) the Williams hypothesis, predicting maximum fitness returns by adjusting size- and sex-specific composition of the litter according to the maternal condition. The food-restricted mothers produced larger litters with a higher proportion of cheaper daughters than the control mothers. By contrast, the control mothers optimized size and sex composition of the litter according to their weight at mating. In addition, the offspring of the food-restricted mothers suffered less from pre-weaning mortality than those of the control mothers. Therefore, when comparing the groups, the Myers hypothesis had a general significance while the Williams hypothesis was plausible only for the control mothers. Furthermore, some of the food-restricted mothers partly coped with the pre-mating food restriction and increased the proportion of sons in the litter with the increasing maternal weight loss (during the period of food restriction). The sex ratio variation was thus a result of three sex allocation strategies depending on the maternal condition at mating.     

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.     

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.     

Temperature,age of mating and starvation determine the role of maternal effects on sex allocation in the mealybug <Emphasis Type="Italic">Planococcus citri</Emphasis>

Environmental effects on sex allocation are common, yet the evolutionary significance of these effects remains poorly understood. Environmental effects might influence parents, such that their condition directly influences sex allocation by altering the relative benefits of producing sons versus daughters. Alternatively, the environment might influence the offspring themselves, such that the conditions they find themselves in influence their contribution to parental fitness. In both cases, parents might be selected to bias their sex ratio according to the prevailing environmental conditions. Here, we consider sex allocation in the citrus mealybug Planococcus citri, a species with an unusual genetic system in which paternal genes are lost from the germline in males. We test environmental factors that may influence either female condition directly (rearing temperature and food restriction) or that may be used as cues of the future environment (age at mating). Using cytological techniques to obtain primary sex ratios, we show that high temperature, older age at mating and starvation all affect sex allocation, resulting in female-biased sex ratios. However, the effect of temperature is rather weak, and food restriction appears to be strongly associated with reduced longevity and a truncation of the usual schedule of male and offspring production across a female’s reproductive lifetime. Instead, facultative sex allocation seems most convincingly affected by age at mating, supporting previous work that suggests that social interactions experienced by adult P. citri females are used when allocating sex. Our results highlight that, even within one species, different aspects of the environment may have conflicting effects on sex allocation.     

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.     

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     

Sex ratio bias and reproductive strategies: what sex to produce when?

Several theories predict the evolution of bias in progeny sex ratio based on variations in maternal or offspring reproductive value. For mammals, however, tests of sex-bias theories have produced inconsistent results, and no clear patterns have emerged. Each theory is based on assumptions that are difficult to satisfy, and empirical tests require large data sets. Using a long-term study on bighorn sheep (Ovis canadensis), we identified several parameters that influence progeny sex ratio according to maternal state. For older females, progeny sex ratio was affected by an interaction between reproductive strategy and environmental conditions. When conditions were good, old females reproduced every year but minimized fitness costs by producing daughters. When conditions were poor, old females produced more sons but did not reproduce every year. Sons of older females were of similar mass to those born to younger females under poor conditions but were smaller and likely disadvantaged under good environmental conditions. For young and prime-aged females, progeny sex ratio was independent of environmental conditions. Environmental conditions and age should be considered when studying sex ratio bias, which appears to be a function of maternal state rather than of maternal condition. We suggest that a conservative reproductive strategy drives progeny sex ratio in older females according to the "cost of reproduction hypothesis." By manipulating offspring sex ratio, older females reduced the cost of reproduction and increased their expected fitness returns.     

Climate and maternal effects modify sex ratios in a weakly dimorphic marsupial

There is growing evidence that the sex ratios of wild vertebrate populations are determined by mechanisms that are directly influenced by environmental characteristics. The Trivers–Willard (TWH) and extrinsic modification (EMH) hypotheses postulate differing determinants of mammalian offspring sex ratios. TWH states that mothers allocate resources according to their current condition and sex-specific offspring costs. EMH states that environmental forces that affect maternal condition determine offspring sex ratios, independently of maternal tactics of sex-biased allocation. We statistically assessed support for each of these hypotheses using long-term life histories of the allied rock-wallaby, Petrogale assimilis; a continuously breeding, polygynous, weakly dimorphic marsupial. We showed that birth sex ratios were equal and independent of maternal and environmental conditions. However, secondary sex ratios were male-biased under good environmental conditions and for high quality mothers or mothers in good condition. Sex differences in offspring survival contributed to these biases: (1) environmental conditions strongly influenced survival to pouch emergence (in support of EMH) and (2) maternal quality affected survival to the end of maternal care (in support of TWH). Environmental effects on survival were more important than maternal factors over the entire period of maternal care and contributed most to male-biased sex ratios at pouch emergence. In contrast, maternal mass was the best predictor of sex ratios at the end of maternal care—the life history stage where offspring body mass differed between the sexes.     

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.     

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     

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.     

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.     

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.     

Philopatry,reproductive success of females,and maternal investment in the red-necked wallaby

Summary Female red-necked wallabies settle within their mothers' home ranges, apparently for life, while males disperse at about two years of age. However, sons spend much more time with their mothers before dispersing than do daughters of similar ages. Females who associate regularly with their subadult offspring are less likely to reproduce successfully at their next breeding attempt than are females who spend little time with their subadults, and sons therefore impose greater short-term reproductive costs on their mothers than do daughters. Females who are generally gregarious also suffer reduced reproductive success, even though reproductive success is independent of local density. It is suggested that the reproductive costs to females of associating with their subadult offspring, and other relatives, are incurred through tolerance of ecological competition from those kin, and therefore reflect a form of prolonged maternal investment, which is initially heaviest in sons but is sustained for longer periods in daughters. Females produce equal numbers of male and female offspring, and spend equal amounts of time suckling them in infancy.     

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.     

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.     

Birth sex ratios in toque macaques and other mammals: integrating the effects of maternal condition and competition

Mammalian life histories suggest that maternal body condition and social dominance (a measure of resource-holding potential) influence the physical and social development of offspring, and thereby their reproductive success. Predictably, a mother should produce that sex of offspring which contributes most to her fitness (as measured by the number of her grandchildren) and that she is best able to raise within the constraints imposed by her condition, social rank, and environment. Such combined effects were investigated by monitoring variations in body condition (weight) and behavior of female toque macaques, Macaca sinica of Sri Lanka, in a changing forest environment over 18 years. Maternal rank, by itself, had no influence on offspring sex, but did affect maternal body condition. The combined effects of rank and condition indicated the following: mothers in robust condition bore more sons, whereas those in moderate condition bore more daughters, but both effects were expressed most strongly among mothers of high rank. Where the consequences of low rank were felt most acutely, as shown by poor condition, mothers underproduced daughters. Environmental quality directly influenced rank and condition interactions, and thus sex ratios. These relationships, and data from other mammals suggest an empirically and theoretically consistent pattern of sex allocation in mammals. New predictions integrate effects, proposed by Trivers and Willard, that are rooted in male mate competition, which is universal among polygynous mammals, with those of local resource competition (and/or female reproductive competition), which are not universal and differ in intensity between the socioecologies and local environments of different species. Received: 30 May 1998 / Accepted after revision: 29 August 1998     

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     

Ecological correlates of duckling adoption among white-winged scoters Melanitta fusca: strategy, epiphenomenon, or combination?

Young waterfowl can frequently join foster females shortly after hatch, resulting in post-hatch brood amalgamation. Much uncertainty remains about physiological or ecological factors that motivate adoption including potential costs and benefits to fostered offspring as well as to females that either lose or accept young. Several hypotheses have been put forth to explain adoption. In this paper, we examine the salvage strategy (SSH) and accidental-mixing (AMH) hypotheses. According to the SSH, females abandon or lose their young due to substantial energetic constraints from incubation and brood rearing. The AMH posits that adoption results from local ecological conditions on breeding areas (i.e., adverse weather conditions, high brood densities) which act to separate offspring and mothers. We used multistate modeling to estimate relationships between probabilities of adoption by white-winged scoter (Melanitta fusca) ducklings from natal to foster females and a set of hypothesized ecological covariates. Results showed that most adoption occurred within 6 days of hatch; additionally, likelihood of adoption was positively related to inclement weather and negatively related to hatch date, size, and condition of natal females, and duckling condition. We conclude that adoption in this population is consistent with both the salvage strategy and accidental-mixing hypotheses. Ultimately, we suggest that adoption in our study population was foremost an outcome of intense gull predation but also of local environmental conditions.     

Sex ratio adjustment and maternal condition in two aphid species

We analyzed how offspring sex ratio varies with maternal condition in order to obtain evidence on the population structure in two aphid species with different life cycles. When fitness returns per unit investment differ for the production of daughters and sons, selection will favor an increasing investment into the sex with the higher returns. Therefore, the offspring sex ratios of individual mothers should become more biased towards the sex with the higher fitness returns as their condition or fecundity improves. The pattern of sex ratio adjustment we found in Uroleucon cirsii indicates local mate competition among males, while the pattern we found in Rhopalosiphum padi suggests local resource competition among sexual females. This might be the first evidence for local resource competition among females in an invertebrate species. Local mate competition means that fitness returns are limited by the availability of females as mates within local breeding groups, whereas local resource competition means that fitness returns are limited by the availability of resources for females competing within local groups. We discuss how the life cycles of both species fit to these hypotheses.