Female tactile cues maximize paternal behavior in prairie voles

Most monogamous male mammals display parental care, but the mechanism by which they become motivated to care for infants remains unknown. We used prairie voles (Microtus ochrogaster) as a model of biparental species to test the hypothesis that physical contact with a female enhances male parental responsiveness before the birth of offspring. We tested four groups of males: mated with physical contact with their mate, mated with only distal cues from their mate, mated with no cues, and unmated with distal cues from a female. The subjects were placed in an oversized cage divided into two compartments by a perforated barrier. At mid-gestation, the bedding and females were removed, and the males’ responses toward two infants were videotaped. Although most males behaved parentally, mated males exposed to their mate’s tactile or distal cues approached the young faster and were more likely to care for both infants than unmated males which received female distal cues. Males who had physical contact with their mate showed “kyphosis” (a crouching position over infants) and contacted infants more frequently than mated males which received no cues from their mate or unmated males which received female distal cues. Furthermore, the frequency of non-social behaviors was lowest in mated males that had physical contact with their mate. The data suggest that exposure to female distal cues after mating is sufficient to increase male parental attentiveness, but female somatosensory cues affect the male's tendency to remain in physical contact with infants.     

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.     

Variations in the birth sex ratio and neonatal mortality in a natural herd of horses

Variations in birth sex ratios and sex differences in juvenile mortality occur in a number of mammalian species, and in many cases have been linked to resource availability. Most of these biases in offspring sex ratios concern polygynous species with pronounced sexual dimorphism, and where females only are philopatric. Data on species with unusual life-history strategies, such as slight sexual dimorphism or dispersal by both sexes, are of particular interest. In this study of a natural herd of horses (Equus caballus) which experienced an eruptive cycle, and therefore a period of nutritional stress, male offspring had higher neonatal mortality rates in nutritionally poor years than in good ones, whereas “year quality” had no effect on the mortality of female offspring; year quality could therefore be used by mares as predictor of sex-specific offspring survival. We show that the environmental conditions that predicted lower survival of males were negatively related to their production: the birth sex ratio the following year was female-biased; and mares were less likely to produce a son when they had produced a son the preceding year. There was no significant effect of mother's parity, age or rank, or the timing of conception or birth on offspring sex ratios. The mechanism leading to biases in the birth sex ratio could have been the loss of male embryos by mares that did not foal. As there was no evidence for selective abortion of male foetuses in females that did foal the next year, it is not necessary to invoke maternal adjustment, though this remains a possibility. Finally, there was a suggestion that male offspring were more costly to raise than females, since mothers that reared a son in poor years tended to experience an increase in the interbirth interval between their two subsequent offspring. Received: 28 December 1996 / Accepted after revision: 27 July 1997     

Infant care,infanticide, and female reproductive strategies in polygynous groups of common marmosets (Callithrix jacchus)

Reproduction in marmoset and tamarin groups is typically restricted to a single dominant female, but it is unclear why subordinate females tolerate delayed reproduction. The presence of two breeding females in free-ranging groups of common marmosets (Callithrix jacchus) presented a unique opportunity to examine differences in the reproductive strategies of dominant and subordinate females. Three groups were monitored for 12–18 months at a forest reserve in northeastern Brazil. Data on infant care were collected during two consecutive all-day follows every 10 days until the infants were 2 months old. Carrying patterns for infants born to dominant females were similar to those observed in groups containing a single breeding female. All group members over 5 months of age participated in infant care, and dominant females allowed some group members to carry their infants from the 1 st day of life. In contrast, subordinate females were protective of their offspring and were their sole caretakers for at least a week following birth. One infant born to a subordinate was killed in an attack involving the dominant female. Overall, dominant females gave birth to more infants and had higher infant survival than did subordinate breeding females. subordinate females were successful in rearing young only when the timing of births was such that they did not overlap with the dependency period of infants born to the dominant female. These patterns suggest that subordinate females may face resource competition, especially over access to helpers. In times of severe competition, subordinate females that delay reproduction may be avoiding a wasted reproductive effort.     

Do female roe deer in good condition produce more sons than daughters

In polygynous roe deer Capreolus capreolus, males are only slightly heavier than females and the overall sex ratio at birth is close to unity. We studied offspring sex ratio and litter size (range 1–4, n = 74) of culled females, in utero, which provided an opportunity to examine responses of sex ratio to maternal condition. Male embryos were heavier than their sisters, and male fawns (9 months old) heavier than female fawns, suggesting a higher growth rate in males. There was no evidence for differential mortality between the sexes from birth to 9 months old. Heavier adult females produced larger embryos than lighter, or primiparous females. The overall sex ratio of embryos did not differ from unity, but adult does had more male embryos (55%) than primiparous does (32%), and the proportion of male embryos in a litter increased with the mother's body mass. Litter size also tended to increase with maternal age and body mass. We argue that this pattern reflects adaptive variation in offspring sex ratio.     

Facultative sex-ratio adjustment in Norway rats: litters born asynchronously are female biased

Summary Previously we reported that inter-litter competition reduces the survival of pups born to pairs of female rats living and breeding in the same nesting environment. Inter-litter competition occurred when females gave birth asynchronously; specifically, when a female gave birth in the presence of 15 to 28-day-old pups, her newborn pups were likely to die as a result of nest intrusion by the older pups. In contrast, inter-litter competition occurred rarely when the two females gave birth synchronously. Because theories of facultative sex ratio adjustment predict that mothers giving birth in unfavorable circumstances should bias their offspring towards the more viable or less expensive sex, we predicted that litters born asynchronously would be female biased. Conversely, we also predicted that females giving birth under favorable conditions, i.e., synchronously, would bias their litters toward males. We found a female bias in asynchronous litters, but did not find a male bias in synchronous litters. Moreover, in contrast to other reports in the literature, the female bias in asynchronous litters was achieved without a reduction in litter size. Based on correlational data, we suggest several mechanisms that could produce this female bias: conditions at fertilization and implantation, time since the male last mated and number of pups suckling concurrently during gestation. Correspondence to: M.K. McClintock     

Sex-specific patterns of lifetime reproductive success in single and repeat breeding steelhead trout (Oncorhynchus mykiss)

All other things being equal, the lifetime reproductive success (LRS) of iteroparous and semelparous individuals should scale with the number of breeding seasons. Deviations from this relationship may occur for many reasons, including age- or size-related fecundity or life history trade-offs, which may differ between sexes. We used 19 brood years of DNA parentage analysis in a small (N = 4–143 year⁻¹) wild, unexploited population of steelhead trout (Oncorhynchus mykiss) to compare the LRS of individuals that spawned only once [“one time spawners” (OTS), N = 355 male, 371 female] to those spawning twice [“repeat spawners” (RPS), N = 13 male, 49 female]. Female RPS had nearly twice the LRS of female OTS (1.17 offspring per female vs 0.91 offspring per female), whereas male RPS had nearly three times the LRS of male OTS (1.54 offspring per male vs 0.57 offspring per male). Female RPS produced slightly more adult offspring during their second breeding season than their first (0.78 vs 0.82 offspring per female); however, male RPS produced all of their adult offspring in their second breeding season (0 vs 1.54 offspring per male). The additional growth in body size of males between breeding seasons may give them an advantage in their second breeding season, but the lack of offspring produced in their first season suggests a trade-off between survival and future reproduction that was not expressed in females.     

Offspring sex ratio in relation to female size in southern elephant seals,Mirounga leonina

Southern elephant seals Mirounga leonina display extreme sexual dimorphism. In addition females show great variation in size and stored resources at parturition. Therefore they present an excellent opportunity for examination of responses of sex ratio to resource availability. We studied the relationships between the size of southern elephant seal females at parturition and the size and sex of their pups at South Georgia over four breeding seasons. We found a large individual variation in maternal post-partum mass (range 296–977 kg, n=151). Larger mothers gave birth to larger pups, irrespective of the sex of their pup. Male pups were on average 14% larger than females at birth and consequently more costly to bring to parturition. Our results suggest that female southern elephant seals must weigh more than 300 kg if they are to breed at all, and more than 380 kg if they are to give birth to a male pup. Above this threshold the proportion of males among offspring rapidly increases with maternal mass, and stabilizes at a level not significantly different from parity. These results show that smaller females of southern elephant seals vary offspring sex ratio in a way that is consistent with theories on adaptive offspring sex ratio. A smaller mother with a male foetus may benefit from terminating her pregnancy and allocating the resources she saves to her own growth. She could then give birth to and raise a larger pup in the subsequent season.     

“Friendships” between new mothers and adult males: adaptive benefits and determinants in wild baboons (<Emphasis Type="Italic">Papio cynocephalus</Emphasis>)

Close associations between adult males and lactating females and their dependent infants are not commonly described in non-monogamous mammals. However, such associations [sometimes called “friendships” (Smuts 1985)] are regularly observed in several primate species in which females mate with multiple males during the fertile period. The absence of mating exclusivity among “friends” suggests that males should invest little in infant care, raising questions about the adaptive significance of friendship bonds. Using data from genetic paternity analyses, patterns of behavior, and long-term demographic and reproductive records, we evaluated the extent to which friendships in four multi-male, multi-female yellow baboon (Papio cynocephalus) groups in Amboseli, Kenya represent joint parental care of offspring or male mating effort. We found evidence that mothers and infants benefited directly from friendships; friendships provided mother–infant dyads protection from harassment from other adult and immature females. In addition, nearly half of all male friends were the genetic fathers of offspring and had been observed mating with mothers during the days of most likely conception for those offspring. In contrast, nearly all friends who were not fathers were also not observed to consort with the mother during the days of most likely conception, suggesting that friendships between mothers and non-fathers did not result from paternity confusion. Finally, we found no evidence that prior friendship increased a male’s chances of mating with a female in future reproductive cycles. Our results suggest that, for many male–female pairs at Amboseli, friendships represented a form of biparental care of offspring. Males in the remaining friendship dyads may be trading protection of infants in exchange for some resources or services not yet identified. Our study is the first to find evidence that female primates gain social benefits from their early associations with adult males. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Maternal characteristics and the production and recruitment of sons in the eastern kingbird (<Emphasis Type="BoldItalic">Tyrannus tyrannus</Emphasis>)

Sex allocation theory predicts that if variance in reproductive success differs between the sexes, females who are able to produce high-quality young should bias offspring sex ratio towards the sex with the higher potential reproductive success. We tested the hypothesis that high-quality (i.e., heavy) female eastern kingbirds (Tyrannus tyrannus) that bred early in the breeding season would produce male-biased clutches. A significant opportunity for sexual selection also exists in this socially monogamous but cryptically polygamous species, and we predicted that successful extra-pair (EP) sires would be associated with an excess of male offspring. Although population brood sex ratio did not differ from parity, it increased significantly with female body mass and declined with female breeding date, but was independent of the morphology and display (song) behavior (correlates of reproductive success) of social males and EP sires. Male offspring were significantly heavier than female offspring at fledging. Moreover, the probability that male offspring were resighted in subsequent years declined with breeding date, and was greater in replacement clutches, but lower when clutch size was large. Probability of resighting female offspring varied annually, but was independent of all other variables. Given that variance in reproductive success of male kingbirds is much greater than that of females, and that male offspring are more expensive to produce and have a higher probability of recruitment if fledged early in the season, our results support predictions of sex allocation theory: high-quality (heavy) females breeding when conditions were optimal for male recruitment produced an excess of sons.     

Female mate choice,male migration,and the threat of infanticide in ringtailed lemurs

Summary Paternity determination by DNA fingerprinting is reported for a long-term study group of semi-free-ranging ringtailed lemurs (Lemur catta), together with behavioral data collected independently. In 1985, fraternal twin males unfamiliar and unrelated to the resident ringtailed lemurs were introduced to the forest enclosure. Every mature resident male attacked the immigrants frequently across the next 5 months, whereas no female ever did. All observed estrous females showed sexual proceptivity toward the' immigrant males; three solicited copulation exclusively from them. Each female repelled sons, matrilineal brothers, and other resident males from attempting to copulate. Over a 5-year period, four of five females always reproduced with distantly related or unrelated males (Fig. 3). Despite low dominance status throughout the case study, an immigrant sired the off-spring of each female that was proceptive toward only the immigrants, demonstrating that female choice can override male dominance relations to determine reproductive success among male ringtailed lemurs. In the birth season following the 1985–1986 immigration, each of four females targeted one or two particular adult males for consistent attack across the period of infant dependency, beginning days after parturition. Paternity determinations, colony records, and subsequent study of two groups allowed 66 cases of this mode of maternal aggression to be documented. In each, the targeted male had not fathered the protected infant, and almost invariably, he was unrelated to the infant's mother. New mothers attacked every male that immigrated following their infants' conceptions and a few familiar males with whom they had not been seen to copulate during the previous breeding season. Recent attempts by immigrant males to kill infants confirmed the anti-infanticidal function of maternal targeting of males. All results were interpreted together to advance a prospective model of the mating system of ringtailed lemurs. Female avoidance of incest has led to the evolution of natal male dispersal. Subsequently, males should prefer to transfer into groups containing few and/or status-vulnerable males. We predict that, by killing others' infants, males simultaneously increase chances for success in females' next reproductive efforts and terminate current fathers' reproductive eligibility in a group. Basic hypotheses that await testing are that (a) raising an infant through weaning reduces a female's chances for reproductive success the following year and (b) males that demonstrate the capacity to promote the survival of infant offspring are most attractive to females as mates.     

Paternity in naturally-occurring Utetheisa ornatrix (Lepidoptera : Arctiidae) as estimated using enzyme polymorphism

Paternity of offspring in natural populations of insects has received little attention due to the difficulties inherent in following females and sampling each of their mates. Here, an existing statistical technique is modified to estimate paternity based on allozyme variation found in the female and her last mate, thus allowing paternity in nature to be studied by collecting copulating pairs of insects. Using this technique, paternity was investigated in naturally-occurring females of the arctiid moth Utetheisa ornatrix. These females mate promiscuously: upon dissection, they were found to contain up to 13 spermatophores. Statistical paternity estimation revealed considerable variation in the share of offspring sired by the female's last mate: approximately 25% of the males sired all the offspring, while another 25% fathered no offspring; the remainder sired at least some offspring. The proportion of offspring sired by the last male did not correlate with latency to oviposition, the extent of previous mating by the female, or male wing length. Male U. ornatrix are known to make substantial nuptial investments during mating, and this study shows that mating males frequently sire few or no offspring. Thus, male moths stand a chance of being cuckolded.     

Baboons adjust secondary sex ratio in response to predictors of sex-specific offspring survival

Summary Most theories of sex ratio adjustment assume that parents will adjust the sex ratio of births (secondary sex ratio) in a manner that maximizes offspring reproductive success (as long as this does not jeopardize parental reproductive success). Survival to maturity is typically the largest component of variance in offspring reproductive success. This should make environmental predictors of sex-specific offspring survival strong predictors of secondary sex ratio adjustment. We tested this survivorship maximization hypothesis for secondary sex ratio adjustment using data from a 17-year demographic study of 315 yellow baboon infants at Mikumi National Park, Tanzania. Sex differences were found in the degree to which several social and ecological conditions affected infant survival to 1 year. Female, but not male, infant survival was inversely correlated with birth order and the proportion of infant females in their birth cohort. Male, but not female, infant survival was inversely correlated with the amount of rainfall early in the year (January) and the proportion of infant males in their birth cohort; male survival also was positively correlated with maternal dominance rank. The consistency and timing of these effects across years suggested that such information was, in fact, available to females around the time of conception. Most importantly, social and ecological conditions that predicted improved survivorship of a given sex also were positively correlated with production of that sex. Early births were female-biased; and low January rainfall was correlated with a male-biased sex ratio, becoming increasingly female-biased as January rainfall increased. However, no sex ratio effects were correlated with maternal rank. Data supported the hypothesis that females adjusted secondary sex ratio in a manner that maximized sex-specific infant survival. This hypothesis also offered a plausible explanation for some of the contradictory data that have arisen from studies of maternal rank effects on sex ratio both within and between species.Correspondence to: S. K. Wasser     

Social monogamy and extra-pair fertilization in an Australian lizard, Tiliqua rugosa

This study investigates social monogamy in the Australian sleepy lizard, Tiliqua rugosa. At a 70-ha site near Mount Mary, South Australia, we radio tracked 55 adult female and 39 adult male lizards during their spring activity periods. Each lizard was observed in 1–5 years. Females were observed with a single male partner on an average of 10.8 days per year, although in 17.3% of cases, females were observed on 2 or fewer days with a male. The most intense pairing period each year was 15 September–15 November when females were with male partners on an average of 36% of observation days. Partnerships lasted an average of 43.3 days each year. After mating in early November, the pairs separated. Observations of females pairing with other males were rare. Most males (82%) were also consistently monogamous, although 7 were observed pairing with 2 females within one season. To investigate paternity, we allowed 21 gravid females to give birth to 42 offspring in the laboratory. We determined genotypes at five polymorphic microsatellite DNA loci for the females, their male partners and their offspring. Four litters (19%) and 6 of the offspring from those litters (14.3%) showed evidence of extra-pair fertilization (EPF). Although the sample sizes are small, females of polygynous males were more likely to experience EPF. Received: 22 February 1998 / Accepted after revision: 23 May 1998     

Paternity and paternal care in the polygynandrous Smith's longspur

In species where females copulate with more than one male during a single breeding attempt, males risk investing in offspring that are not their own. In the polygynandrous Smith's longspur (Calcarius pictus), females copulate sequentially with one to three males for each clutch of eggs and most of these males later assist in feeding the young. Using multilocus DNA profiling, we determined that there was mixed paternity in >75% of broods (n=31) but that few offspring (<1% of 114 nestlings) were sired by males outside the polygynandrous group. Male feeding rate increased significantly with the number of young sired, with males siring four nestlings feeding the brood at double the frequency of males siring only a single nestling. However, male Smith's longspurs appear to show a graded adjustment of paternal care in response to paternity only when other males are available to compensate for reduced care: feeding rate did not vary in relation to paternity when only one male provisioned young at the nest. There was no evidence that males could recognise their own offspring within a brood and feed them preferentially. The number of offspring sired by each male was significantly correlated with the number of days spent copulating with the attending female: on average, a male sired one offspring for every 2 days of copulatory access. If males use their access to females to estimate paternity (and thereby decide on their subsequent level of parental investment), a positive relationship is expected between the amount of female access and the subsequent feeding rate to the nestlings. Nonetheless, male feeding effort was only weakly correlated with female access and more study is needed to determine how males estimate their paternity in a brood. Received: 1 June 1997 / Accepted after revision: 1 April 1998     

All-offspring dispersal in a tropical mammal with resource defense polygyny

In polygynous mammals, males are usually responsible for gene flow while females are predominantly philopatric. However, there is evidence that in a few mammalian species female offspring may disperse to avoid breeding with their father when male tenure exceeds female age at maturity. We investigated offspring dispersal and local population structure in the Neotropical bat Lophostoma silvicolum. The mating system of this species is resource defense polygyny, with the resource being active termite nests, excavated by single males, which are then joined by females. We combined field observations of 14 harems during 3 years and data about the genetic structure within and between these groups, calculated with one mitochondrial locus and nine nuclear microsatellite loci. The results show that both male and female offspring disperse before maturity. In addition, we estimated life span of excavated termite nests and the duration they were occupied by the same male. Our findings suggest that long male tenure of up to 30 months is indeed a likely cause for the observed dispersal by female offspring that can reach maturity at a low age of 6 months. We suggest that dispersal by offspring of both sexes may occur quite frequently in polygynous tropical bats and thus generally may be more common in mammals than previously assumed.     

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     

Indirect fitness benefits are not related to male dominance in a killifish

Recent theoretical and empirical studies have shown that male dominance is often at odds with female mate preference and that indirect (genetic) benefits of mate choice may not be related to male dominance. We tested whether female preference corresponded to male dominance and whether mating with dominant males conveyed benefits to offspring fitness in a small freshwater fish, the African annual killifish Nothobranchius korthausae (Cyprinodontiformes), a species without parental care. The experimental design used controlled for the effect of male age, possibility of sperm and egg depletion, and accounted for a potential that females express their preference through maternal effects by manipulation of egg mass during ovulation. By sequentially mating females with males of known dominance, we found that female N. korthausae showed no mate preference in terms of egg numbers deposited with respect to male dominance or body size and no congruent mate preference to specific males was detected. However, males sired offspring with consistently higher hatching success and the effect was repeatable across individual females. Thus, some males provided females with indirect benefits related to additive genetic quality (“good genes”) and expressed via increased hatching rate, but this benefit was not related to male dominance status or body size.     

Pre-natal investment in reproduction by female Antarctic fur seals

Summary Maternal investment, in terms of pup birth mass, in gestation by Antarctic fur seals (Arctocephalus gazella) was related to the date of birth in two consecutive years. There were significant differences in birth mass between years and between the sexes within years. Birth mass was used to calculate the mean energetic cost of producing a pup to parturition. The cost for a male pup in 1986 was 173 MJ while it was 191 MJ in 1987. For female pups the cost was 152 and 166 MJ in 1986 and 1987 respectively. Given the probable pattern of foetal growth, this constitutes a minimum of 5–15% of the maternal energy budget in the final months of gestation. Birth mass varied inversely with date of birth, but more strongly for male than for female pups. The sex ratio at birth was unity in both years and this did not vary with time through the birth season. In a subsample of mothers (n=79) which were captured on the day of birth, there was a decline in the body mass and standard length with date of birth. Male birth mass was directly related to maternal mass and maternal condition (mass/length) but there was no significant relationship for females. These results suggest that the growth of male foetuses is limited by maternal resources while female foetuses do not exploit fully maternal resources.     

Extra-pair paternity and tail ornamentation in the barn swallow Hirundo rustica

Females of socially monogamous species may copulate with attractive non-mates to obtain access to the genes of such males, and a preference for attractive copulation partners may result in sexual selection. Extra-pair copulations are common in the socially monogamous barn swallow Hirundorustica, and a 2-year study of paternity using multi-locus DNA fingerprinting demonstrated that 33% of 63 broods and 28% of 261 offspring were sired by extra-pair males. The frequency of extra-pair offspring within broods was highly skewed with the majority of all broods having either no extra-pair offspring or only extra-pair offspring. Individual pairs were consistent in their frequency of extra-pair paternity among broods, and the repeatability of extra-pair paternity of multiple broods of the same female was statistically significant. The proportion of extra-pair offspring was negatively related to the tail length of the male attending the nest. Behavioural observations showed that extra-pair fertilizations were more likely in broods raised by females that had been observed to engage in extra-pair copulations. The frequency of extra-pair offspring was unrelated to the intensity of two male paternity guards, mate guarding and the rate of intra-pair copulations. In an analysis of extra-pair paternity and male parental care in different broods of the same male, male barn swallows fed their offspring relatively less frequently if the brood contained more extra-pair offspring. Therefore, female barn swallows pursue extra-pair copulations with attractive males, which may result in sexual selection, even though extra-pair paternity is costly for females due to the reduction of paternal care by their social mates. Received: 24 January 1997 / Accepted after revision: 2 August 1997