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).     

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.     

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.     

Influence of social factors on sex ratio at birth,maternal investment and young survival in a prosimian primate

Summary In order to determine whether social factors influence sex ratio at birth in lesser mouse lemurs, experiments were conducted during 5 successive breeding periods on 51 females. At the beginning of the breeding season, females were either isolated (I) or grouped (G) in heterosexual groups with an increasing number of females (2, 3 or 4). To ensure mating, I females were introduced in a group only during the oestrous period. After mating, both I and G females were isolated during pregnancy and lactation. Reproductive capacities of females in terms of oestrus occurrences (n = 324), impregnations (n–210), pregnancies (n = 136) or abortions (n = 38) or litter sizes (1–3 young) were affected neither by age and parity of females nor by group housing prior to conception. G females produced significantly more sons than daughters (67% males for 189 newborn) while females living alone except during the mating period demonstrated a significant inverse tendency (39.6% males for 96 newborn). Distribution of sexes in litters was statistically different from random and varied according to the shift of sex ratio at birth. In G females, the shift in the sex ratio towards males was consistent across the different groups, independent of the number of females living together, suggesting that the presence of only 1 female is sufficient to induce a bias in the sex ratio. No correlation was found between infant survival at weaning and age, parity or group housing of the mother. The maternal investment allocated to male or female newborn was similar provided the litter contained at least 1 male. In litters without males, growth and survival of female infants were significantly less. These results on sex ratio bias in captive female mouse lemurs agree with directions of bias predicted by the local resource competition model for facultative sex ratio adjustment (Clark 1978). Nevertheless, the pattern observed in mouse lemurs appears to be independent of the nutritional state of the female and of differential maternal investment.     

Does male harassment of females contribute to reproductive synchrony in the grey seal by affecting maternal performance?

We investigated the possibility that male harassment of lactating females differed in relation to time of birth in the grey seal, Halichoerus grypus, on Sable Island, Nova Scotia. This was done by comparing the frequency of male disturbances, maternal performance and pup growth for females that either gave birth during the peak of the pupping season or after the peak. Of the females, 58% gave birth in a 7-day period near the beginning of the pupping period, when the operational sex ratio was 2–4 females per male. Late in the pupping period the operational sex ratio reversed to about 1 female for every 2 males. The relative frequency of disturbances by males was significantly greater for late-pupping mothers than for peak-pupping ones (1.9 vs. 1.4 encounters/h). Females that gave birth late also were disturbed by males 3 times more often than females that gave birth during the peak (3.4 vs. 1.1 % of observation time). Late-pupping mothers spent 22% less time suckling (4.0 vs. 5.1 % of observation time), had 30% slower growing pups (1.7 vs. 2.4 kg/d), and weaned pups that were 16% lighter (45.6 vs. 54.0 kg). The effect of birth time on pup mass gain and weaning mass was not attributable to factors such as maternal mass, pup birth mass or pup sex. We conclude that the reduced maternal performance is likely the result of the increased male harassment. As reduced weaning mass can lead to reduced juvenile survival, male harassment may have contributed to the enhanced reproductive synchrony in this species.     

Maternal quality and differences in milk production and composition for male and female Iberian red deer calves (Cervus elaphus hispanicus)

Several theories predict a sex-biased investment either through unbalanced sex ratios in offspring or through differences in provisioning. According to them, one would expect an optimisation in indirect fitness, or else a compensation for increased mortality of one sex. In addition, biases in provisioning may also arise as a consequence of weight-dependent non-adaptive nutrient demands by offspring. This study examines milk provisioning and sex biases in offspring sex ratio together with maternal quality variables. Mothers of higher quality (weight and age) showed greater milk provisioning ability (in terms of production) resulting in greater calf weight gain. Mothers of sons produced greater yields of milk, milk protein, fat and lactose than mothers of daughters, and increased percentage of protein after controlling for higher male birth weight. In contrast, mothers of males did not differ from mothers of females in age or any body weight variables related to maternal quality. These results suggest that differences in milk production and composition for sons and daughters are rather a mechanism to optimise indirect fitness than a mechanism to compensate for increased mortality in male calves, or a consequence of greater weight-dependent nutrient demands by heavier male calves. Results also suggest that biases in milk provisioning may occur without biases in offspring sex ratio, and furthermore, in contrast to the prediction that biases should be relative to the mean investment of the population, that milk provisioning biases might not be relative.Communicated by F. Trillmich     

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     

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.     

Sex ratio manipulation and decreased growth of male offspring of undernourished golden hamsters (Mesocricetus auratus)

Summary The theory that female mammals in poor condition may increase individual fitness by skewing the sex ratio of their offspring toward daughters and by investing more resources in daughters than in sons was tested in hamsters. Newly mated experimental females were food-restricted during pregnancy and lactation (RR) or during lactation only (AR). Controls received food ad libitum. Maternal body weights were assessed daily from mating to 25 days postpartum. Litter survival (% litters with at least one pup surviving on any day), litter size, offspring sex ratios (=% males), and pup weights were monitored daily from birth (Day 1) to Day 25. All control and AR dams gave birth 16 days after mating. Gestation was extended by 1–3 days for 35.4% of RR dams. RR dams weighed significantly less at parturition than controls and AR females. During lactation, AR females showed the greatest weight loss and control females the least. AR weight loss exceeded that of RR females, possibly because the former maintained larger litters. Survival was highest for controls, intermediate for AR, and lowest for RR litters. Mean sex ratio at birth was significantly less for RR (40.7%) than for control (49.6%) and AR (48.8%) litters. RR sex ratio did not change significantly postnatally. Sex ratios of control and AR litters never differed statistically from 50%. Control male pups were significantly heavier than their sisters throughout the experiment. No significant gender differences were observed for AR pup weights after Day 2 postpartum. RR female offspring weighed more than their brothers throughout the experiment, and this difference was statistically significant immediately prior to the time that pups began to feed independently (Days 14–17). RR female pup weights were similar to, and sometimes significantly greater than, weights of control daughters during the period of postnatal maternal investment. Control males were always heavier than males from the other treatments. Patterns of weight gain by AR and RR males varied with age. We conclude that underfed female hamsters are able to adjust the sex ratio of offspring prenatally and parental investment postnatally to favor daughters.     

Contradictory findings in studies of sex ratio variation in roe deer (Capreolus capreolus)

Patterns of sex ratio variation and maternal investment reported in the literature are often inconsistent. This could be due to intra- and inter-specific variation in social systems, but may also be a result of the a posteriori nature of much of this type of analysis or the testing of models which are inappropriate. Two recent papers reported directly opposed results concerning variation in offspring sex ratios in relation to maternal condition in roe deer, interpreting the results as support for the Trivers and Willard model and for the local resource competition hypothesis, respectively. In this paper, we present data on offspring sex ratios and early juvenile body weight from two long-term studies of this species to test predictions arising from these two models concerning sex biases in litter composition and maternal care. First, we observed no consistent pattern of sex differences in an index of weaning weight or body weight at 1 month old in either population, indicating a lack of sex bias in maternal care. However, in one population, higher maternal body weight was associated with higher juvenile body weight of daughters, but not of sons. Secondly, we found a negative, but not statistically significant, relationship between maternal body weight and litter sex ratio such that heavier females tended to produce more daughters and lighter females to produce more sons. These results indicate that roe females which have additional investment potential available do not invest it in sons, as predicted by the Trivers and Willard model. Our results may provide some support that roe deer are subject to local resource competition acting at the level of the individual mother; however, the fact that particular trends in sex ratio data can be explained in functional terms provides no indication that they are actually adaptive. Received: 9 December 1997 / Accepted after revision: 11 November 1998     

Sex-specific maternal investment in pronghorn,and the question of a limit on differential provisioning in ungulates

Summary Prediction that mothers will invest more in individual sons than daughters in polygynous mammals has been confirmed in several species. However, among polygynous ungulates, differential investment occurs in some species, but not in others. Because ungulates have postnatal growth rates among the highest in mammals, we hypothesized that level of maternal investment limits the ability of offspring of one sex to evolve faster growth rates, even when intrasexual selection might favor faster growth. We predicted that comparative rate of maternal investment would explain the distribution of differential investment among ungulates, and examined our data on pronghorn (Antilocapra americana), which show the highest-known rate of maternal investment among ungulates. Data on birth weights, suckling rates, ages-pecific frequency of maternal termination of suckling bouts, age at weaning, and rate of rejected suckle attempts showed either no sex differences or else a slight excess investment in daughters. In concordance with these data, female fawns spent more energy in activity than did male fawns. Among ungulates for which data are available, the best predictor of differential investment is not degree of adult sexual dimorphism; it is comparative rate of maternal investment.     

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.     

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.     

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     

The influence of maternal rank and infant sex on maternal investment trends in rhesus macaques: birth sex ratios,inter-birth intervals and suckling patterns

Summary In the new colony of rhesus macaques at Madingley, no overall difference was found in the length of the inter-birth intervals following the birth of male and female infants. The lack of overall differences in the reproductive costs of raising sons and daughters, was associated with an absence of differences in suckling patterns between male and female infants. It is argued that similar pre-weaning investment in sons and daughters may be related to the presence of similar growth rates for male and female infants during the first year of life. Most high ranking mothers reproduced in consecutive years, while low ranking mothers were more likely to experience two year long inter-birth intervals. Further analyses revealed that this difference was mainly due to the fact that low ranking mothers always failed to reproduce the year after raising a daughter. Thus, no difference was found in the length of inter-birth intervals between high ranking mothers with infants of either sex and low ranking mothers with sons. The daughters of low ranking females suckled more frequently and making more nipple contacts per bout, and such high nipple stimulation was responsible for the reproductive inhibition experienced by their mothers. It is suggested that the high degrees of nipple stimulation may have been a consequence of the high levels of aggression that low ranking females with daughters have been shown to receive, since their mothers could have allowed frequent ventro-ventral contact in order to protect them. Given that low ranking mothers find daughters reproductively costly to raise, it is possible that such high reproductive costs have played a significant role in the evolution of sex ratio biases at birth. As in other primate populations, in this colony low ranking females produced a greater proportion of sons than daughters, and high ranking mothers showed the opposite trend.     

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.     

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.     

Short-term consequences of different breeding histories for captive rhesus macaque mothers and young

Summary Life histories of rhesus monkey mothers (Macaca mulatta) were classified in terms of (1) whether the mothers were top ranking or not, (2) gave birth to more daughters than sons or vice versa, and (3) gave birth at intervals of one year or of more than a year. Bearing daughters at intervals of more than a year was the most common history among top ranking mothers, while bearing sons annually was most common among other mothers. The consequences for the infants and mothers of such histories were examined and (1) infants were more likely to die as neonates if they had an older sister, especially if the sister had been born in the previous birth season; (2) dyads with daughters received more aggression from other adults in the daughter's first year, but not necessarily through the year following the birth of the next infant (3) when mothers of daughters gave birth of the next infant after at least one fallow year, their daughters directed considerable amounts of harassing aggression to their next-born sibling; and (4) mothers of sons but not of daughters delayed longer when they received more aggression from other adults.We discuss the views that birth sex ratios may be affected by a mother's rank rather than how often she is involved in aggressive encounters with other adults; and that in top-ranking mothers, birth intervals may be controlled more by the infant's sex than aggression the family received. Fitting the data into a life history strategy model is done as a provisional and speculative exercise     

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.     

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