Social rank, fecundity and lifetime reproductive success in wild European rabbits (Oryctolagus cuniculus)

Wild European rabbits of both sexes have separate linear rank orders, which are established and maintained by intensive fights. This paper presents data from a 14-year study (1987-2000) on the population physiology and behavioural ecology of wild rabbits living in a 22,000 m² enclosure and focuses on the relationship between social rank and reproduction in females. Group composition, social ranks, fecundity and reproductive success were known for all females (n=197) from the outset of their first reproductive season at an age of about 300 days until their death. The annual reproductive success of females was influenced to a large extent by their social rank. This depended on two effects of about equal strength: a higher fecundity of high-ranking females and a lower mortality of their offspring between birth and adulthood. The lifetime reproductive success of the females varied greatly. Only about 50% of all females had any reproductive success (range: on to nine adult offspring). The social rank achieved by the females during their first reproductive season substantially influenced their lifetime reproductive success: The mean reproductive lifespan and lifetime fitness of high-ranking females (ranks 1 and 2) was about 60% greater than that of lower-ranking females, although many of the latter also gained dominant positions in subsequent years.     

Sexual selection and reproductive careers in mandrills (Mandrillus sphinx)

In sexually dimorphic, polygynous species, where males provide little parental care and competition between males for access to fertile females is high, sexual selection theory predicts sex differences in age-specific reproductive output and mortality profiles, and greater variance in lifetime reproductive success in males than in females. We examined age-specific reproductive output, mortality patterns and the extent and causes of variation in reproductive success for a semi-free-ranging colony of mandrills (Mandrillus sphinx, Cercopithecidae) in Franceville, Gabon, using long-term (20 year) demographic records and microsatellite parentage analysis. Although differences in the demography and feeding ecology of this closed, provisioned colony, in comparison with wild mandrills, limit interpretation of our results, sex differences in reproductive output and mortality showed the patterns predicted by sexual selection theory. Mortality was higher in males than in females after sexual maturity, and lifespan was significantly shorter in males (mean 14 year) than in females (>22 year). Age at first reproduction was significantly earlier in females (mean 4.2 year) than in males (11.6 year), and male reproductive output declined earlier. All females of breeding age produced offspring; while only 17 of 53 sexually mature males (32%) sired. Males sired a maximum of 41 offspring, versus 17 in females, and variance in male reproductive output was significantly greater than in females at all ages. The most important influence on variation in lifetime reproductive output in both sexes was joint variation between length of the breeding period and reproductive rate, due to lower reproductive rates in younger animals. Finally, social rank significantly influenced reproductive output in both sexes: high-ranking females began their reproductive careers earlier and had a higher subsequent reproductive rate than low-ranking females, while males that achieved top rank during their career sired far more offspring than males that did not.Electronic Supplementary Material Supplementary material is available for this article at     

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     

Variation in offspring sex ratio among individual Weddell seal (<Emphasis Type="Italic">Leptonychotes weddellii</Emphasis>) females of different quality

The Trivers–Willard model predicts that in polygynous species, superior-quality females will maximize their fitness by producing male offspring. Using a sample of 1,780 Weddell seal (Leptonychotes weddellii) pups recorded over 31 years, we investigated relationships between offspring sex ratio and maternal age, reproductive experience, an index of maternal lifetime reproductive output, and annual environmental variations. We found evidence that females with higher index of lifetime reproductive output were more likely to produce male than female offspring but found only weak evidence that large-scale environmental variations influenced sex ratios. Our results suggest that mothers manipulate offspring sex to maximize their own fitness, and inherent maternal quality may influence offspring sex. These findings support the Trivers–Willard sex-allocation model. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

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

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

Harem choice and breeding experience of female southern elephant seals influence offspring survival

Female mammals can increase their lifetime fitness through modification of investment potential and by providing better rearing environments with improved breeding experience. We examined the relationships between reproductive fitness and the behavioural decisions that female southern elephant seals (Mirounga leonina) made during the breeding season. We examined whether mother age and breeding experience influenced reproductive success (measured as 1st-year survival probability), and whether there was a change in the choice of harem size with increasing age. Pups produced by young mothers had lower 1st-year survival probability than pups produced by older mothers. A significant increase in mean female mass with age required an analysis of both these effects on offspring survival. There was a significant positive effect of both female age and mass, and the interaction between the two, on 1st-year pup survival. The proportion of young mothers (<5 years old) decreased and the proportion of older mothers (>6 years old) increased with increasing harem size (harems surveyed from 1997 to 2001). Females chose larger harems in which to breed as they aged. Females demonstrated fidelity to breeding areas among successive breeding seasons, with older females displaying greater breeding-site fidelity than younger females. The mean number of previous breeding attempts per female within a harem (breeding experience) increased significantly with increasing harem size. Breeding females returned to breed later in the breeding season as they aged—we hypothesize that young, subordinate females gain a priority advantage by returning earlier. These results lend support to the hypothesis that there are fitness advantages, in terms of offspring survival, that are conferred to females that breed in successively larger harems with age. Potential mechanisms that select for females to improve their breeding conditions include improved mate selection and the avoidance of conspecific harassment in harems.Communicated by F. Trillmich     

The reproductive consequences of male cooperation in the red howler monkey: paternity exclusion in multi-male and single-male troops using genetic markers

Summary Variance in male reproductive success in single and multi-male red howler (Alouatta seniculus) troops was examined through paternity exclusion using genetic markers. Coalitions of relatives were compared to coalitions of non-relatives with regard to duration, stability, and number of offspring expected for each participant based on paternity exclusion results. No evidence of paternity by males living outside of the troop was found. In multi-male troops, only the dominant male was found to father offspring conceived during his tenure. This was the only male observed to mount females. In both troops examined genetically wherein a status change had occurred, paternity changed with status. Coalitions of relatives and potential relatives lasted significantly longer than coalitions of non-relatives, and experienced fewer status changes between males. A direct advantage of forming a coalition for both dominant and subordinate red howler males resulted from the superior competitive ability of coalitions over single males in establishing and maintaining tenure in the limited number of female troops in the population. Although the mating success of a subordinate male in a coalition appears to be extremely low, his chances of achieving membership in a bisexual troop as a single male may be even lower. Since the majority of troops in the population during any given year were multi-male or age-graded male (85%–96%), the number of troops that a single male would be able to invade unaided was very small. A subordinate male may be able to assume dominance, particularly if he is a subadult. In coalitions in which males are related, the subordinate male will further benefit from inclusive fitness. A dominant male that forms a coalition with a relative can expect to have longer reproductive tenure than in a troop with a non-relative, thereby producing more offspring and directly enhancing his fitness. Anecdotal evidence suggests that males choose relatives over non-relatives as coalition partners when possible.     

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.     

Survival and lifetime reproductive success in dispersing and resident red squirrels

Dispersal in red squirrels (Sciurus vulgaris) is not sex-biased and strict philopatry is rare. The immigration pattern suggests that nearly all animals have to disperse away from the natal site and that dispersal in this species is the outcome of local (intrasexual) competition. If this interpretation is correct, we predict that dispersers and residents, of both sexes, should have equal survival rates and lifetime reproductive success. Body mass, longevity, reproductive success and dominance rank of 34 resident offspring (settling within 400 m of the natal range) and 70 immigrants (dispersers) were compared. Immigrants did not weigh less than residents as adults, nor did they have a higher mortality during the pre-setding period. Survival rate, lifetime reproductive success (females) and the proportion of males obtaining a high dominance rank were similar for residents and dispersers, and no sex effect was found on either of the parameters studied. These results are consistent with the hypothesis that local competition determines whether an individual disperses further away or settles close to its birthplace.     

Life history costs and consequences of rapid reproductive maturation in female rhesus macaques

Summary Life history theory suggests that reproduction at one point in time involves costs in terms of energy, reduced survival, or probability of reproduction at a future point in time. ln long-lived iteroparous organisms, initiating reproduction at a relatively young age may exact a cost in terms of reduced survivorship, but an early age of first reproduction could be beneficial if it lengthens the breeding lifespan. Data collected over 30 years from one population of rhesus macaques, Macaca mulatta, were analyzed to determine the fertility and survivorship costs of initiating reproduction at a relatively young age. Low population density and high social status increased the chances of accelerating age at first parturition, but high dominance rank was not associated with greater lifetime reproductive success. Rapid reproductive maturation neither reduced short-term survivorship nor decreased lifespan. Fertility costs arose if young females reared a male, but not female, offspring. The fitness consequences of rapid reproductive maturation depend upon longevity, with age at death having a significantly greater impact on lifetime reproductive success than age at first parturition.Correspondence to: F.B. Bercovitch     

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

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

Socioecological influences on the reproductive success of female mountain gorillas (<Emphasis Type="Italic">Gorilla beringei beringei</Emphasis>)

Over the past few decades, socioecological models have been developed to explain the relationships between the ecological conditions, social systems, and reproductive success of primates. Feeding competition, predation pressures, and risk of infanticide are predicted to influence how female reproductive success (FRS) depends upon their dominance rank, group size, and mate choices. This paper examines how those factors affected the reproductive success of female mountain gorillas (Gorilla beringei beringei) of the Virunga Volcanoes, Rwanda from 1967–2004. Reproductive success was measured through analyses of interbirth intervals, infant survival, and surviving infant birth rates using data from 214 infants born to 67 females. Mountain gorillas were predicted to have “within-group scramble” feeding competition, but we found no evidence of lower FRS in larger groups, even as those groups became two to five times larger than the population average. The gorillas are considered to have negligible “within-group contest” competition, yet higher ranked mothers had shorter interbirth intervals. Infant survival was higher in multimale groups, which was expected because infanticide occurs when the male dies in a one-male group. The combination of those results led to higher surviving birth rates for higher ranking females in multimale groups. Overall, however, the socioecological factors accounted for a relatively small portion of the variance in FRS, as expected for a species that feeds on abundant, evenly distributed foliage.     

Sigma virus and male reproductive success in Drosophila melanogaster

The risk of disease transmission can affect female mating rate, and thus sexual conflict. Furthermore, the interests of a sexually transmitted organism may align or diverge with those of either sex, potentially making the disease agent a third participant in the sexual arms race. In Drosophila melanogaster, where sexual conflict over female mating rate is well established, we investigated how a common, non-lethal virus (sigma virus) might affect this conflict. We gave uninfected females the opportunity to copulate twice in no-choice trials: either with two uninfected males, or with one male infected with sigma virus followed by an uninfected male. We assessed whether females respond behaviorally to male infection, determined whether male infection affects either female or male reproductive success, and measured offspring infection rates. Male infection status did not influence time to copulation, or time to re-mating. However, male infection did affect male reproductive success: first males sired a significantly greater proportion of offspring, as well as more total offspring, when they were infected with sigma virus. Thus viral infection may provide males an advantage in sperm competition, or, possibly, females may preferentially use infected sperm. We found no clear costs of infection in terms of offspring survival. Viral reproductive success (the number of infected offspring) was strongly correlated with male reproductive success. Further studies are needed to demonstrate whether virus-induced changes in reproductive success affect male and female lifetime fitness, and whether virus-induced changes are under male, female, or viral control.     

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.     

Association patterns among male and female spotted hyenas (Crocuta crocuta) reflect male mate choice

Although female animals tend to be choosier than males in selecting mates, sexual selection theory predicts that males should also be choosy when female fecundity varies. Reproductive success among female spotted hyenas varies greatly with social rank. Our goals were therefore to determine whether male hyenas preferentially associate with high-ranking females, and whether male preferences are affected by female reproductive state. Interactions between adult males and females were observed intensively, and association indices calculated for all male-female pairs, over a 7-year period in one population of free-living hyenas. Males initiated most affiliative interactions with females, and males associated most closely with females that were likeliest to be fertile. High- and middle-ranking males associated most closely with high-ranking females, but low-ranking males associated equally closely with females in all rank categories. We used molecular markers to determine the paternity of cubs born during the study period, and found that sires associated more closely with the mothers of those cubs than did non-sires, particularly during the last months before conception. These association data indicate that male spotted hyenas do indeed exhibit selective mate choice, and that they prefer females likeliest to maximize male reproductive success.     

Lifetime and intergenerational fitness consequences of harmful male interactions for female lizards

Male mating behaviors harmful to females have been described in a wide range of species. However, the direct and indirect fitness consequences of harmful male behaviors have been rarely quantified for females and their offspring, especially for long-lived organisms under natural conditions. Here, lifetime and intergenerational consequences of harmful male interactions were investigated in female common lizards (Lacerta vivipara) using field experiments. We exposed females to male harm by changing the population sex ratio from a normal female-biased to an experimental male-biased sex ratio during the first experimental year. Thereafter, females and their first generation of offspring were monitored during two additional years in a common garden with a female-biased sex ratio. We found strong immediate fitness costs and lower lifetime reproductive success in females subjected to increased male exposure. The immediate fitness costs were partly mitigated by direct compensatory responses after exposure to male excess, but not by indirect benefits through offspring growth, offspring survival, or mating success of offspring. These results support recent empirical findings showing that the direct costs of mating are not outweighed by indirect benefits.     

Maternal dominance rank and lifetime survivorship of male and female rhesus monkeys

Summary The longitudinal survivorship of a group of free-ranging male and female rhesus monkeys from La Parguera, Puerto Rico, was analyzed. Males had lower age-specific survivorship than females. There were no differences in the survivorship of daughters of high- and low-ranking mothers and there was no correlation between total number of offspring born and maternal rank for females. However, the sons of low-ranking mothers had lower survivorship than the sons of high-ranking females. This sex-related difference in survivorship, in conjunction with other evidence, indicates that the average lifetime reproduction of sons of low-ranking females is lower than that of daughters and vice versa for offspring of high-ranking females.     

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 control of reproductive skew in cooperatively breeding brown jays (<Emphasis Type="Italic">Cyanocorax morio</Emphasis>)

Brown jays (Cyanocorax morio) are long-lived, social corvids that live in large, stable, territorial groups (mean = 10 individuals). In this study, I determined the distribution of reproductive success within groups using multi-locus DNA fingerprinting. Breeding females produced virtually all (99%) of the young within their own nests. Reproduction within groups was highly skewed towards a single primary female, although long term data indicate that secondary females (female breeders that were usually younger and subordinate to the primary female) were sometimes successful. The high reproductive skew observed for females was associated with primary female aggression. Successful reproduction by secondary females may have been due to parental facilitation or the inability of primary females to completely suppress secondary females. Multiple paternity occurred in 31–43% of broods and extra-group paternity occurred in a minimum of 22% of broods. Patterns of paternity also varied between years, since females often switched or included new genetic mates. Although male consorts of nesting females fathered relatively few offspring (20%), they still had a higher chance of fathering offspring than any other single group male. Reproduction was less skewed for males than females as a result of female mating patterns. Female reproductive patterns are consistent with some of the predictions and assumptions from optimal skew models, while male reproductive patterns are not. The factors affecting skew in species with complex social systems such as incomplete control by breeders over subordinate reproduction, female control of paternity, and resource inheritance have not been well incorporated into reproductive skew models.Communicated by: J. Dickinson     

Reproductive success in the Caribbean octocoral Briareum asbestinum

For most sessile marine invertebrates the number of offspring produced by an individual is often determined indirectly from counts of eggs present, with the assumption that all or most become viable offspring. Few field data on the actual number of offspring produced per individual (reproductive success) have been reported. We examined reproductive success in the octocoral, Briareum asbestinum (Pallas), by measuring embryo densities on 40 female colonies on two reefs (Pinnacles and House reefs) in the San Blas Islands, Panama from 1986 to 1988. The percentage of female colonies with mature eggs which subsequently released embryos was low, ranging from 46.6% in 1986 to 5.0% in 1988. Reproductive success was significantly different between reefs. Pinnacles reef had significantly more successful colonies (those releasing embryos) than House reef in all three years and significantly higher embryo densities in 1986 and 1987. There was a significant positive correlation between female reproductive success and the density and proximity of nearby males in both 1986 and 1987. In addition, fertile female branches placed 25 cm away from male branches produced significantly more embryos than female branches placed 50 cm away. In 1988 two groups of female branches were placed at distances of <50 cm and 5 m from four large male colonies at Pinnacles reef. Of the 20 female branches placed 5 m from the males none released embryos while 35% (7 of 20 branches) of the branches <50cm from males released embryos. These data indicate that simple counts of mature eggs present within female colonics prior to the reproductive season provide a poor estimate of reproductive success in B. ashestinum and that female reproductive success is positively influenced by the close proximity of males.