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).     

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.     

Sex-specific energy requirements in nestlings of an extremely sexually size dimorphic bird, the European sparrowhawk (Accipiter nisus)

Allocation of parental investment is predicted to be equal at the population level between both sexes of offspring, and should lead to sex ratio biases in species that exhibit a sex-difference in parental care. Sex-differences in parental care are rarely quantified. We measured daily energy expenditure in free-living nestlings of the extremely sexually size dimorphic European sparrowhawk (Accipiter nisus), using the doubly labelled water method. These data were combined with measured growth characteristics to estimate daily and total metabolised energy intake of male and female young during the nestling stage. Females reached an asymptotic body mass 1.6 times higher than males. This resulted in a total metabolised energy an estimated 1.4 times higher for the nestling stage. Furthermore, we observed a decline in daily metabolised energy with an increase in brood size, which was significantly stronger for females than for males. These results are discussed in the context of Fishers equal allocation theory. Empirical evidence of a sex ratio bias at the end of parental care, with an overall excess of males, is lacking in this species. Consequently, our data do not support the idea of equal allocation between the sexes. The observed sex difference in daily metabolised energy in response to brood size may give scope for sex ratio bias at the level of the individual brood.     

Maternal investment in Antarctic fur seals: evidence for equality in the sexes?

Studies of the otariids (fur seals and sea lions), a highly sexually dimorphic group, have provided conflicting evidence of differential maternal expenditure in male and female offspring and, thus, suggestions that they conform to predictions of investment theory are equivocal. Since the mid-1970s, a diversity of research on Antarctic fur seals (Arctocephalus gazella) including studies of their reproductive ecology, lactation energetics, and foraging behaviour have been conducted at Bird Island, South Georgia that have resulted in one of the more complete and diverse data sets for any species of otariid. These long-term data were reviewed to determine whether there was any evidence to support that differential maternal expenditure occurred in Antarctic fur seals. Most of the data examined were collected during five consecutive austral summers from 1988 through 1992 and included years in which local food resources were abundant and scarce. We were unable to detect differences in the sex ratios of pups at birth or sex-biased differences in growth rates estimated from serial data, the number of foraging trips made, the duration of attendance ashore, diving behaviour, suckling behaviour, or milk consumption in any year and in the duration of foraging trips or age at weaning in 2 of 3 years. In addition, we found no evidence of greater reproductive costs between mothers with sons or daughters relative to their reproductive performance the following year. In contrast, sex-biased differences were only found in the duration of foraging trips in 1990, the age at weaning in 1988, and consistently in growth rates estimated from cross-sectional data. We suggest that differential maternal expenditure does not occur in Antarctic fur seals because male pups probably do not gain greater benefit from additional maternal expenditure than female pups. After weaning, males experience a period of rapid juvenile growth over 3–4 years during which time body mass nearly trebles. This growth will almost certainly be dependent upon available food resources then rather than on any maternal expenditure received over the first 4 months of life and, thus, the assumptions of the Trivers and Willard hypothesis are probably invalid for Antarctic fur seals. Received: 10 July 1996 / Accepted after revision: 3 March 1997     

Parental investment in southern elephant seals,Mirounga leonina

Summary The southern elephant seal is among the most sexually dimorphic and polygynous of all mammals: males may be more than 10 times the weight of reproducing females and only the largest 2–3% of males are likely to breed. Current optimization theories of sexual selection predict that evolution would favor greater parental investment in individual males than in females. Because southern elephant seals represent an extreme of polygyny and sexual dimorphism, they might be expected to show a dramatic difference in parental investment in male and female pups. However, in a study of parental investment in elephant seals at South Georgia, using several different methods, we found no such difference after parturition. Mother-pup pairs were immobilized and weighed early in lactation, recaptured near the end of lactation and reweighed. A further 30 pups were weighed an average of five times during lactation to establish the shape of the growth curve and to serve as partial controls for the previous set of animals. Initial post-partum weight in females ranged from 346 to 803 kg (=506, SD=111, n=26). Pup birth weight was related to mothers' post-partum weight in female pups but small females often gave birth to large male pups. Male pups were significantly heavier at birth than females. However, this size difference did not persist. Male and female pups were suckled for the same period, grew at the same rate and were not significantly different in weight at weaning. Mothers lost weight at the same rate regardless of their pup's sex.     

Paternal expenditure is related to brood sex ratio in polygynous great reed warblers

In many polygynous animals, parents invest more heavily in individual sons than in daughters. However, it is unclear if these differences in investment are a consequence of sex differences in the demand of offspring related to sexual size dimorphism or a consequence of parental manipulation. Here, we report on parental food delivery frequency in relation to brood size and brood sex ratio in a wild population of polygynous great reed warblers Acrocephalus arundinaceus. We used the polymorphic microsatellite loci on the Z chromosome to sex chicks. We found that paternal feeding frequency (times/h per nest) increased not with brood size, but with the proportion of males in the brood, although the demand per nest was more closely related to brood size than to brood sex ratio. Additionally, the increase in rate of paternal feeding frequency in relation to the brood sex ratio was much higher than the increase in rate of nestling food demands. Maternal feeding frequency was independent of both brood size and brood sex ratio. These results strongly suggest that fathers preferentially invest in their sons. We propose that parents can afford sex-biased parental care in animals in which food provisioning is enough for all offspring to survive. Received: 22 January 1996/Accepted after revision: 30 June 1996     

Parental investment, adult sex ratios, and sexual selection in a socially monogamous seabird

Although most birds are monogamous, theory predicts that greater female parental investment and female-biased adult sex ratios will lower the polygyny threshold. This should result in polygynous mating, unless obligate biparental care or the spatial and temporal distribution of fertilizable females constrains a male’s ability to take advantage of a lowered polygyny threshold. Here we present data on the extent of male sexually dimorphic plumage, adult sex ratios and breeding season synchrony in three populations of a socially monogamous seabird, the brown booby Sula leucogaster. For one of these populations, San Pedro Mártir Island, we also present data on differences in male and female parental investment, mortality and probability of pairing. The extent of plumage dimorphism varied among populations. Sex ratios were female biased in all populations. On San Pedro Mártir Island, parental investment was female biased, females failed more often than males to find a mate, but there was no polygyny. We suggest that on San Pedro Mártir: (1) a period of obligate biparental care coupled with a relatively synchronous breeding season constrained the ability of males to take advantage of a high environmental polygamy potential and (2) the resulting socially monogamous mating system, in combination with the female-biased adult sex ratio, caused females to be limited by the availability of males despite their greater parental investment. Received: 18 November 1999 / Accepted: 24 January 2000     

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.     

Male-biased sex ratios in New Zealand fur seal pups relative to environmental variation

A number of models have been proposed to provide adaptive explanations of sex-ratio variation in mammals. Two models have been applied commonly to primates and ungulates with varying success—the Trivers-Willard (TW) hypothesis, and the local resource competition (LRC) hypothesis. For polygynous, sexually dimorphic mammals, where males are larger and disperse more readily, these models predict opposite outcomes of sex-ratio adjustment within the same environmental context (high-resource years: TW—more sons; LRC—more daughters). However, many of the predictions of these two models can vary depending on factors influencing resource availability, such as environmental stochasticity, resource predictability, and population density. The New Zealand fur seal (Arctocephalus forsteri) is a polygynous mammal showing marked sexual dimorphism (larger males), with higher variation in male reproductive success expected. We provide clear evidence of male-biased sex ratios from a large sample of A. forsteri pups captured around South Island, New Zealand during 1996/1998, even after accounting for a sex bias in capture probability. The extent of the bias depended upon year and, in 1998, strong climatic perturbations (El Niño/Southern Oscillation, ENSO) probably reduced food availability. Significant male-biased sex ratios were found in all years; however, there was a significant decline in the male bias in 1998. There was no relationship between sex ratio and population density. We suggest that the sex-ratio bias resulted from the production of relatively more male pups. Under the density-independent scenario, the strong male bias in A. forsteri sex ratios is support for the TW model within an environment of high resource predictability. We suggest that some plasticity in the determination of pup sex among years is a mechanism by which A. forsteri females in New Zealand, and perhaps other otariid seals, can maximise fitness benefits when living in regions of high, yet apparently predictable, environmental variability. We also suggest that much of the inconsistency in the reported sex ratios for otariid seals results from the complex interaction of population density and environmental stochasticity influencing relative food availability over time.     

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     

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.     

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     

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.     

Sex-specific maternal effect on egg mass,laying order,and sibling competition in the Bengalese finch (<Emphasis Type="Italic">Lonchura striata</Emphasis> var. <Emphasis Type="Italic">domestica</Emphasis>)

Maternal effects, such as investment in eggs, have profound effects on offspring fitness. Mothers are expected to skew their investment depending on the laying order and sex when unequal sibling competition occurs within a brood because of sex-specific vulnerability and age hierarchy caused by asynchronous hatching. The Bengalese finch hatches asynchronously and shows a moderate reversed sexual size dimorphism. However, contrary to commonly accepted assumptions of size-dependent vulnerability, the smaller sex (male) is more vulnerable to developmental stress caused by sibling competition. We investigated whether maternal investment would be biased by the position in laying order and the sex of eggs, and also explored the possible differences in growth patterns depending on sex, laying order, and age hierarchy by observing chicks fostered to experimentally manipulated broods where brood composition was controlled and age hierarchy was more enhanced than in natural breeding conditions. We found that overall patterns of maternal investment favored the disadvantageous sectors of sibling competition, i.e., eggs of later laying order and sons over those of early laying order and daughters. We also examined the effect of laying order on adult body size and sex differences in growth patterns. When reared in the subordinate age hierarchy, females could compensate for the deficit of decreased growth rate by taking longer to mature, whereas males could not. We suggest that this sex-specific growth pattern could be the cause of sex differences in vulnerability to early developmental stress.     

Measurement of parental investment and sex allocation in the European beewolf Philanthus triangulum F. (Hymenoptera: Sphecidae)

Fisher’s 1930 theory of sex allocation predicts a population-wide 1:1 ratio of parental investment. We tested this prediction in the European beewolf, a sphecid wasp that hunts for honeybees as larval food. Because the method to quantify parental investment is of crucial importance, we compared the suitability of several different investment measures. Female/male cost ratios were determined from a sample and the total investment in sons and daughters was calculated. In addition, the actual number of prey items for sons and daughters was directly determined by excavating nests and counting the cuticle remains of the prey. Though mortality was high (70%), it had only a weak effect on the estimate of the investment ratio. Based on commonly used measures like fresh and dry weight of emerged adults, the investment ratio did not deviate from Fisher’s prediction of equal investment. However, progeny weight considerably underestimates investment in males and investment in large progeny. Measures that reflect the allocation of resources more directly (amount of provisions, brood cell volume) revealed a significant male bias and thus contradicted Fisher’s theory. Three kinds of explanation are discussed. First, non-adaptive explanations are unlikely. Second, from the spectrum of alternative adaptive theories, only models that assume a non-linear relationship between amount of investment and progeny fitness seem to be relevant for the study species. Third, though the number of prey in a brood cell seems to be a rather good measure of parental investment in European beewolves, some problems in measuring parental investment remain. These problems are of broad significance. Received: 17 June 1999 / Received in revised form: 6 July 1999 / Accepted: 11 July 1999     

Sex allocation in the solitary bee Osmia cornuta: do females behave in agreement with Fisher's theory?

Fisher's theory of sex allocation predicts that, in a panmictic population, parental investment will be equally distributed between male and female progeny. Most studies on parental investment in nesting solitary bees and wasps use offspring or provision weight as estimators of parental investment and do not corroborate Fisher's theory. The measurement of parental investment may be confounded by several factors. First, the use of offspring or provision size does not account for seasonal variation in foraging costs associated with aging of nesting females. Second, provision or offspring size do not reflect parental investment associated with nest construction. In this two-year study we measured parental investment in a solitary bee. We calculated sex allocation using both provision weight and foraging time as parental investment estimators. Investment in pollen-nectar provisions decreased, while investment in mud structures (nest construction) increased, as the nesting period progressed. Overall investment in provisions per nest was ∼25 times higher than investment in mud. Pollen-nectar foraging trips became longer as the season progressed, but mud trip duration did not vary. Due to weather differences between years, more offspring per female were produced in the first year, but progeny sex ratio and mean offspring size of both sexes were similar between years. Mortality did not differ between sexes. As predicted by Fisher's theory, production cost ratios did not differ from 1 in either year, irrespective of the currency used to estimate parental investment (provision weight or foraging time). Our results strongly support Fisher's theory.     

Relationship between body size, provisioning rate, longevity and reproductive success in females of the solitary bee Osmia cornuta

Body size has often been related to reproductive success in bees and wasps. The objective of this 3-year study was to analyze the relationship between nesting female body size, provisioning rate and longevity and their effect on several traits related to parental investment and reproductive success in the solitary bee Osmia cornuta. Body size was not correlated to longevity, and it was only correlated to provisioning rate in the third year (with poor weather conditions during nesting). Variation in fecundity, offspring size and offspring mortality was not well explained by nesting female body size in any of the 3 years. However, in the third year, small females biased their investment toward males, the sex requiring smaller pollen–nectar provisions. Large females were more successful usurpers of other females' nests, but fecundity of usurpers was no higher than fecundity of nonusurpers. Large females were more likely to establish at the release site, probably in relation to size-dependent vigor at emergence. A review of the literature on parental investment in solitary aculeate Hymenoptera showed a stronger relationship between body size and reproductive success in wasps than in bees. In O. cornuta, fecundity was strongly related to longevity and provisioning rate in all 3 years. Offspring size was associated with provisioning rate in 1 year, when females with higher provisioning rates tended to produce larger sons and daughters. Both longevity and provisioning rate appeared to be strongly conditioned by stochastic events.     

Paternal care in the European starling,Sturnus vulgaris: nestling provisioning

The extent to which male birds in polygynous species with biparental care assist in nestling feeding often varies considerably between nests of different mating status. Both how much polygynous males assist and how they divide their effort between nests may have a profound effect on the evolution of mating systems. In this study we investigated how males in the facultatively polygynous European starling Sturnus vulgaris invested in their different nests. The amount of male assistance affected the quality of the offspring. Polygynous males invested as much as monogamous males, but divided their effort asymmetrically between nests, predominantly feeding nestlings of first-mated (primary) females. Although females partly compensated for loss of male assistance, total feeding frequency was lower at primary females’ nests than at monogamous females nests. Secondary females received even less assistance with nestling rearing, and the extent to which males assisted decreased with the length of the interval between the hatching of the primary and secondary clutches. These results are contrasted with those from a Belgian populations of starlings with a much more protracted breeding season and thus greater opportunities for males to attract additional mates during the nestling rearing period. The results show that both the “defence of male parental investment model” and the “asynchronous settlement model” have explanatory power, but that their validity depends on the potential length of the breeding season. Received: 21 July 1995/Accepted after revision: 13 July 1996     

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     

Parental investment, potential reproductive rates, and mating system in the strawberry dart-poison frog, Dendrobates pumilio

We studied the effect of relative parental investment on potential reproductive rates (PRRs) to explain sex differences in selectivity and competition in the dart-poison frog Dendrobates pumilio. We recorded the reproductive behavior of this species in a Costa Rican lowland rainforest for almost 6 months. Females spent more time on parental care than males, and `time out' estimates suggest that PRRs of males are much higher than than those of females, rendering females the limiting sex in the mating process. Males defended territories that provide suitable calling sites, space for courtship and oviposition, and prevent interference by competitors. Male mating success was highly variable, from 0 to 12 matings, and was significantly correlated with calling activity and average perch height, but was independent of body size and weight. Estimates of opportunity for sexual selection and variation in male mating success are given. The mating system is polygamous: males and females mated several times with different mates. Females were more selective than males and may sample males between matings. The discrepancy in PRRs between the sexes due to differences in parental investment and the prolonged breeding season is sufficient to explain the observed mating pattern i.e., selective females, high variance in male mating success, and the considerable opportunity for sexual selection. Received: 9 June 1998 / Received in revised form: 27 March 1999 / Accepted: 3 April 1999