Post-conception reproductive competition in cooperatively breeding common marmosets

Common marmosets are cooperatively breeding monkeys that exhibit high female reproductive skew. Subordinate females usually fail to breed as a consequence of ovulation suppression and inhibition of sexual behavior, and, even when they do breed, typically rear fewer infants than dominants. We evaluated possible mechanisms of post-conception reproductive competition by comparing hormonal profiles across pregnancy, pregnancy outcomes, infant survivorship, and behavior in laboratory-housed families containing one (N=9) or two (N=7) breeding females. Breeding females in plurally breeding groups did not exhibit well-defined dominance relationships and rarely engaged in escalated aggression with one another. No significant differences were found among singly breeding mothers, plurally breeding mothers, and plurally breeding daughters in urinary chorionic gonadotropin or estradiol sulfate concentrations during pregnancy, fetal biparietal diameter, frequency of spontaneous abortion, frequency of stillbirths, number of live-born infants per litter, or infant mortality rates. When females gave birth while another female in the family was pregnant, however, their infants were highly likely to be killed. The perpetrator was definitively identified in only one family, in which a pregnant female killed her daughter's infant. These results are consistent with observations of free-living common marmosets and suggest that breeding females do not regularly influence one another's pregnancy outcomes, but that they may commonly kill each other's infants, especially during their own pregnancy. Our findings further suggest that infanticide by breeding females may have selected for the evolution of reproductive restraint in subordinate female marmosets.     

Sex-specific spatio-temporal variability in reproductive success promotes the evolution of sex-biased dispersal

Inbreeding depression, asymmetries in costs or benefits of dispersal, and the mating system have been identified as potential factors underlying the evolution of sex-biased dispersal. We use individual-based simulations to explore how the mating system and demographic stochasticity influence the evolution of sex-specific dispersal in a metapopulation with females competing over breeding sites, and males over mating opportunities. Comparison of simulation results for random mating with those for a harem system (locally, a single male sires all offspring) reveal that even extreme variance in local male reproductive success (extreme male competition) does not induce male-biased dispersal. The latter evolves if the between-patch variance in reproductive success is larger for males than females. This can emerge due to demographic stochasticity if the habitat patches are small. More generally, members of a group of individuals experiencing higher spatio-temporal variance in fitness expectations may evolve to disperse with greater probability than others.     

Banded mongooses avoid inbreeding when mating with members of the same natal group

Inbreeding and inbreeding avoidance are key factors in the evolution of animal societies, influencing dispersal and reproductive strategies which can affect relatedness structure and helping behaviours. In cooperative breeding systems, individuals typically avoid inbreeding through reproductive restraint and/or dispersing to breed outside their natal group. However, where groups contain multiple potential mates of varying relatedness, strategies of kin recognition and mate choice may be favoured. Here, we investigate male mate choice and female control of paternity in the banded mongoose (Mungos mungo), a cooperatively breeding mammal where both sexes are often philopatric and mating between relatives is known to occur. We find evidence suggestive of inbreeding depression in banded mongooses, indicating a benefit to avoiding breeding with relatives. Successfully breeding pairs were less related than expected under random mating, which appeared to be driven by both male choice and female control of paternity. Male banded mongooses actively guard females to gain access to mating opportunities, and this guarding behaviour is preferentially directed towards less closely related females. Guard–female relatedness did not affect the guard's probability of gaining reproductive success. However, where mate‐guards are unsuccessful, they lose paternity to males that are less related to the females than themselves. Together, our results suggest that both sexes of banded mongoose use kin discrimination to avoid inbreeding. Although this strategy appears to be rare among cooperative breeders, it may be more prominent in species where relatedness to potential mates is variable, and/or where opportunities for dispersal and mating outside of the group are limited.     

Condition dependence of reproductive strategy and the benefits of polyandry in a viviparous lizard

Species in which males do not contribute to reproduction beyond the provision of sperm offer good opportunities to study the potential genetic benefits that females can obtain from polyandry. Here, we report the results of a study examining the relationships between polyandry and components of female fitness in the common lizard (Lacerta vivipara). We found that polyandrous females produce larger clutches than monandrous females. Polyandrous females also lose fewer offspring during the later stages of gestation and at birth, but we did not find any relationship between polyandry and physical characteristics of viable neonates. Our results were consistent with the predictions of the intrinsic male quality hypothesis, while inbreeding avoidance and genetic incompatibility avoidance might also explain some part of the variation observed in clutch size. Moreover, the benefits of polyandry appeared to depend on female characteristics, as revealed by an interaction between reproductive strategy and female length on reproductive success. Thus, all females did not benefit equally from mating with multiple males, which could explain why polyandry and monandry coexist.     

Living with strangers: direct benefits favour non-kin cooperation in a communally nesting bird

The greater ani (Crotophaga major), a Neotropical cuckoo, exhibits an unusual breeding system in which several socially monogamous pairs lay eggs in a single nest and contribute care to the communal clutch. Cooperative nesting is costly-females compete for reproduction by ejecting each other's eggs-but the potential direct or indirect fitness benefits that might accrue to group members have not been identified. In this study, I used molecular genotyping to quantify patterns of genetic relatedness and individual reproductive success within social groups in a single colour-banded population. Microsatellite analysis of 122 individuals in 49 groups revealed that group members are not genetic relatives. Group size was strongly correlated with individual reproductive success: solitary pairs were extremely rare and never successful, and nests attended by two pairs were significantly more likely to be depredated than were nests attended by three pairs. Egg loss, a consequence of reproductive competition, was greater in large groups and disproportionately affected females that initiated laying. However, early-laying females compensated for egg losses by laying larger clutches, and female group members switched positions in the laying order across nesting attempts. The greater ani, therefore, appears to be one of the few species in which cooperative breeding among unrelated individuals is favoured by direct, shared benefits that outweigh the substantial costs of reproductive competition.     

Determinants of reproductive success in dominant female meerkats

1. In cooperative societies with high reproductive skew, selection on females is likely to operate principally through variation in the probability of acquiring dominant status and variation in reproductive success while dominant. Despite this, few studies of cooperative societies have investigated the factors that influence which females become dominant, and/or their reproductive output while in the dominant position. 2. Here we use long-term data from a wild meerkats population to describe variation in the breeding success of dominant female meerkats Suricata suricatta and investigate its causes. 3. Female meerkats compete intensely for breeding positions, and the probability of acquiring the breeding role depends upon a female's age in relation to competitors and her weight, both at the time of dominance acquisition and early in life. 4. Once dominant, individual differences in breeding success depend principally on the duration of dominance tenure. Females remain for longer in the dominant position if they are heavier than their competitors at the start of dominance, and if the number of adult female competitors at the start is low. 5. Female breeding success is also affected by variation in fecundity and pup survival, both of which increase with group size. After controlling for these effects, female body weight has a positive influence on breeding rate and litter size, while the number of adult female competitors reduces litter survival. 6. These findings suggest that selection for body weight and competitive ability will be high in female meerkats, which may moderate their investment in cooperative activities. We suggest that similar consequences of competition may occur among females in other cooperative societies where the benefits of attaining dominance status are high.     

One for all and breeding for one: Cooperation and competition as a tamarin reproductive strategy

In this paper I examine behavioral strategies used by male and female tamarins to increase individual reproductive opportunities while continuing to maintain a high level of group cohesion and social cooperation. Tamarins of the genus Saguinus are characterized by social groups generally composed of more than one adult of each sex, but a breeding system in which only a single female in each group gives birth. The breeding sovereignty of a single dominant female limits the reproductive opportunities of subordinate females as well as the reproductive opportunities of resident adult males.^1-3 Despite extreme variability in year-to-year reproductive success among members of the same social group, field studies indicate that within-group intrasexual aggression and fighting are rare, and that both breeding and nonbreeding individuals expend time and energy cooperatively caring for young, defending productive feeding sites, and assisting in food harvesting activities.^4-11 In fact, Caine¹² has argued that “co-operation, tolerance, and flexibility” are the primary themes of tamarin social interactions (p. 218). A major question that remains unanswered, however, is how such high levels of cooperation could have evolved in a social system characterized by emigration of both adult males and females from the natal group, polyandrous mating, and intense reproductive competition.     

Reproductive roles in the cooperatively breeding acorn woodpecker: incest avoidance versus reproductive competition

Incest is rare in the cooperatively breeding acorn woodpecker (Melanerpes formicivorus) despite a polygynandrous mating system in which nearly all group members are close relatives. Here we test the relative importance of avoiding matings between close relatives (incest avoidance) and within-sex competition for breeding opportunities (reproductive competition) in determining the mating system of acorn woodpeckers by examining how reproductive roles change following breeding vacancies. In 83% of cases in which helpers of the same sex were present in the group, reproductive vacancies were resolved when new unrelated immigrants filled the vacancy to the exclusion of resident same-sex helpers, who generally emigrated or did not breed while they remained in the group. Helpers of the opposite sex, especially when male, were significantly more likely to remain in their natal group and in about half the cases inherited and bred following reproductive vacancies. This result was not explainable by reproductive competition, since the number of immigrants was often less than or equal to the number of same-sex helpers in the group. Apparent incest resulted in 5% of cases. The time required to resolve reproductive vacancies was significantly longer for groups with helpers of the same sex as the vacancy. These results confirm that both incest avoidance and reproductive competition are important factors determining reproductive roles within groups of this highly social species.     

Reproductive competition triggers mass eviction in cooperative banded mongooses

In many vertebrate societies, forced eviction of group members is an important determinant of population structure, but little is known about what triggers eviction. Three main explanations are: (i) the reproductive competition hypothesis, (ii) the coercion of cooperation hypothesis, and (iii) the adaptive forced dispersal hypothesis. The last hypothesis proposes that dominant individuals use eviction as an adaptive strategy to propagate copies of their alleles through a highly structured population. We tested these hypotheses as explanations for eviction in cooperatively breeding banded mongooses (Mungos mungo), using a 16-year dataset on life history, behaviour and relatedness. In this species, groups of females, or mixed-sex groups, are periodically evicted en masse. Our evidence suggests that reproductive competition is the main ultimate trigger for eviction for both sexes. We find little evidence that mass eviction is used to coerce helping, or as a mechanism to force dispersal of relatives into the population. Eviction of females changes the landscape of reproductive competition for remaining males, which may explain why males are evicted alongside females. Our results show that the consequences of resolving within-group conflict resonate through groups and populations to affect population structure, with important implications for social evolution.     

A Comparison of the Maternal Care of Females within Prairie Vole (Microtus ochrogaster) Communal Groups

Communal rearing, the shared rearing of offspring by multiple individuals or mothers, may improve the fitness of individuals in group‐living species. To date, many studies have focused on these potential fitness consequences. Fewer studies have emphasized the relative contributions to care of offspring by mothers and non‐breeding alloparents in singularly breeding groups (i.e., one female breeds) and mothers within plurally breeding groups (i.e., more than one female breeds). We compared the care provided by prairie vole (Microtus ochrogaster) mothers and alloparents in singularly breeding groups and mothers in plurally breeding groups. Subjects were littermate siblings in both types of social groups. Specifically, we quantified the amount of time that mothers and alloparents were away from pups during 6 h observational trials and the amount of time that females tactilely stimulated pups (licking and grooming) during 20 min trials. We also compared the quality of milk, measured as total solids, produced by mothers in plurally breeding groups. In singularly breeding groups, mothers spent significantly more time out of the nest but tactilely stimulated pups more than alloparents. In plurally breeding groups, focal mothers (i.e., the first mother to produce a litter) spent significantly more time out of the nest than second mothers (i.e., the second female to produce a litter) but licked and groomed pups an equal amount as second mothers. In plurally breeding groups, focal and second mothers produced milk with a similar concentration of total solids. These results suggest that communal rearing in groups is more beneficial to focal mothers than to other breeding or non‐breeding adult females. We discuss fitness‐based hypotheses that may explain the observed differences in the amount of care provided by mothers and alloparents.     

Social queuing in animal societies: a dynamic model of reproductive skew

Previously developed models of reproductive skew have overlooked one of the main reasons why subordinates might remain in a group despite restricted opportunities to breed: the possibility of social queuing, i.e. acquiring dominant status in the future. Here, we present a dynamic ESS model of skew in animal societies that incorporates both immediate and future fitness consequences of the decisions taken by group members, based on their probability of surviving from one season to the next (when post-breeding survival probabilities drop to zero, our analysis reduces to the model produced by Reeve and Ratnieks in 1993, which considered only a single breeding season). This allows us to compare the delayed benefits of philopatry and the immediate opportunities for independent breeding. We show that delayed benefits greatly reduce the need for dominants to offer reproductive concessions to retain subordinates peacefully in the group. Moreover, this effect is strong enough that differences in survival have a much greater impact on the group structure than differences in other parameters, such as relatedness. When the possibility of acceding to dominant status is taken into account, groups where the dominant completely monopolizes reproduction can be stable, even if they consist of unrelated individuals, and even if subordinates have a reasonably high probability of winning a fight for dominance. Finally, we show that stable groups are possible even if association leads to a decrease in current productivity. Subordinates may still stand to gain from group membership under these circumstances, as acquiring breeding positions by queuing may be more efficient than the attempt to establish a new territory. At the same time, the dominant may be unable to exclude unwelcome subordinates, may enjoy increased survival when they are present, or may gain indirect benefits from allowing relatives to stay and queue for dominance. We conclude that reproductive skew in animal groups, ranging from eusocial insect colonies to mating aggregations (leks), will be strongly influenced by the future prospects of group members.     

Costly reproductive competition between females in a monogamous cooperatively breeding bird

In many cooperatively breeding societies, only a few socially dominant individuals in a group breed, reproductive skew is high, and reproductive conflict is common. Surprisingly, the effects of this conflict on dominant reproductive success in vertebrate societies have rarely been investigated, especially in high-skew societies. We examine how subordinate female competition for breeding opportunities affects the reproductive success of dominant females in a monogamous cooperatively breeding bird, the Southern pied babbler (Turdoides bicolor). In this species, successful subordinate reproduction is very rare, despite the fact that groups commonly contain sexually mature female subordinates that could mate with unrelated group males. However, we show that subordinate females compete with dominant females to breed, and do so far more often than expected, based on the infrequency of their success. Attempts by subordinates to obtain a share of breeding impose significant costs on dominant females: chicks fledge from fewer nests, more nests are abandoned before incubation begins, and more eggs are lost. Dominant females appear to attempt to reduce these costs by aggressively suppressing potentially competitive subordinate females. This empirical evidence provides rare insight into the nature of the conflicts between females and the resultant costs to reproductive success in cooperatively breeding societies.     

Competition, breeding success and ageing rates in female meerkats

Competition between females is particularly intense in cooperatively breeding mammals, where one female monopolises reproduction in each group. Chronic competition often affects stress and may therefore have long-term consequences for fitness, but no studies have yet investigated whether intrasexual competition has effects of this kind and, in particular, whether it affects rates of reproductive senescence. Here, we use long-term data from a wild population of meerkats to test whether reproductive success and senescence in dominant females are affected by the degree of intrasexual competition experienced prior to dominance acquisition. Females that experienced greater competition had lower breeding success and higher rates of reproductive senescence. Furthermore, females that were evicted from the group more frequently as subordinates had lower breeding success when dominant. We conclude that the intense intrasexual competition between females in cooperatively breeding groups may carry fitness costs over a longer period than is usually recognised.     

Brood parasitism,relatedness and sociality: a kinship role in female reproductive tactics

Conspecific brood parasitism (CBP) is a reproductive tactic in which parasitic females lay eggs in nests of other females of the same species that then raise the joint brood. Parasites benefit by increased reproduction, without costs of parental care for the parasitic eggs. CBP occurs in many egg‐laying animals, among birds most often in species with large clutches and self‐feeding young: two major factors facilitating successful parasitism. CBP is particularly common in waterfowl (Anatidae), a group with female‐biased natal philopatry and locally related females. Theory suggests that relatedness between host and parasite can lead to inclusive fitness benefits for both, but if host costs are high, parasites should instead target unrelated females. Pairwise relatedness (r) in host–parasite (h‐p) pairs of females has been estimated using molecular genetic methods in seven waterfowl (10 studies). In many h‐p pairs, the two females were unrelated (with low r, near the local population mean). However, close relatives (r = 0.5) were over‐represented in h‐p pairs, which in all 10 studies had higher mean relatedness than other females. In one species where this was studied, h‐p relatedness was higher than between nesting close neighbours, and hosts parasitized by non‐relatives aggressively rejected other females. In another species, birth nest‐mates (mother–daughters, sisters) associated in the breeding area as adults, and became h‐p pairs more often than expected by chance. These and other results point to recognition of birth nest‐mates and perhaps other close relatives. For small to medium host clutch sizes, addition of a few parasitic eggs need not reduce host offspring success. Estimates in two species suggest that hosts can then gain inclusive fitness if parasitized by relatives. Other evidence of female cooperation is incubation by old eider Somateria mollissima females of clutches laid by their relatives, and merging and joint care of broods of young. Merging females tended to be more closely related. Eiders associate with kin in many situations, and in some geese and swans, related females may associate over many years. Recent genetic evidence shows that also New World quails (Odontophoridae) have female‐biased natal philopatry, CBP and brood merging, inviting further study and comparison with waterfowl. Kin‐related parasitism also occurs in some insects, with revealing parallels and differences compared to birds. In hemipteran bugs, receiving extra eggs is beneficial for hosts by diluting offspring predation. In eggplant lace bugs Gargaphia solani, host and parasite are closely related, and kin selection favours egg donation to related females. Further studies of kinship in CBP, brood merging and other contexts can test if some of these species are socially more advanced than presently known.     

Dispersal, eviction, and conflict in meerkats (Suricata suricatta): an evolutionarily stable strategy model

Decisions regarding immigration and emigration are crucial to understanding group dynamics in social animals, but dispersal is rarely treated in models of optimal behavior. We developed a model of evolutionarily stable dispersal and eviction strategies for a cooperative mammal, the meerkat Suricata suricatta. Using rank and group size as state variables, we determined state-specific probabilities that subordinate females would disperse and contrasted these with probabilities of eviction by the dominant female, based on the long-term fitness consequences of these behaviors but incorporating the potential for error. We examined whether long-term fitness considerations explain group size regulation in meerkats; whether long-term fitness considerations can lead to conflict between dominant and subordinate female group members; and under what circumstances those conflicts were likely to lead to stability, dispersal, or eviction. Our results indicated that long-term fitness considerations can explain group size regulation in meerkats. Group size distributions expected from predicted dispersal and eviction strategies matched empirical distributions most closely when emigrant survival was approximately that determined from the field study. Long-term fitness considerations may lead to conflicts between dominant and subordinate female meerkats, and eviction is the most likely result of these conflicts. Our model is computationally intensive but provides a general framework for incorporating future changes in the size of multimember cooperative breeding groups.     

Sex differences in the drivers of reproductive skew in a cooperative breeder

Many cooperatively breeding societies are characterized by high reproductive skew, such that some socially dominant individuals breed, while socially subordinate individuals provide help. Inbreeding avoidance serves as a source of reproductive skew in many high‐skew societies, but few empirical studies have examined sources of skew operating alongside inbreeding avoidance or compared individual attempts to reproduce (reproductive competition) with individual reproductive success. Here, we use long‐term genetic and observational data to examine factors affecting reproductive skew in the high‐skew cooperatively breeding southern pied babbler (Turdoides bicolor). When subordinates can breed, skew remains high, suggesting factors additional to inbreeding avoidance drive skew. Subordinate females are more likely to compete to breed when older or when ecological constraints on dispersal are high, but heavy subordinate females are more likely to successfully breed. Subordinate males are more likely to compete when they are older, during high ecological constraints, or when they are related to the dominant male, but only the presence of within‐group unrelated subordinate females predicts subordinate male breeding success. Reproductive skew is not driven by reproductive effort, but by forces such as intrinsic physical limitations and intrasexual conflict (for females) or female mate choice, male mate‐guarding and potentially reproductive restraint (for males). Ecological conditions or “outside options” affect the occurrence of reproductive conflict, supporting predictions of recent synthetic skew models. Inbreeding avoidance together with competition for access to reproduction may generate high skew in animal societies, and disparate processes may be operating to maintain male vs. female reproductive skew in the same species.     

Reproductive competition promotes the evolution of female weaponry

Secondary sexual traits in females are a relatively rare phenomenon. Empirical studies have focused on the role of male mate choice in their evolution; however, recently it has been suggested that secondary sexual traits in females are more likely to be under selection via reproductive competition. We investigated female competition and the influence of female phenotype on fitness in Onthophagus sagittarius, a species of dung beetle that exhibits female-specific horns. We compared reproductive fitness when females were breeding in competition versus breeding alone and found that competition for breeding resources reduced fitness for all females, but that smaller individuals suffered a greater fitness reduction than larger individuals. When females were matched for body size, those with the longest horns gained higher reproductive fitness. The fitness function was positive and linear, favouring increased horn expression. Thus, we present evidence that female body size and horn size in O. sagittarius are under directional selection via competition for reproductive resources. Our study is a rare example of female contest competition selecting for female weaponry.     

Mechanisms and reproductive consequences of breeding dispersal in a specialist predator under temporally varying food conditions

Individual variation in breeding dispersal has extensive ecological and evolutionary consequences, but the factors driving individual dispersal behaviour and their fitness consequences remain poorly understood. Our data on dispersal events of a rodent‐specialist predator, the Eurasian kestrel Falco tinnunculus, over 20 years in western Finland offers a unique opportunity to explore the mechanisms underlying breeding dispersal behaviour and its reproductive consequences in a wild bird population. Sex, age, body condition and previous breeding success affected breeding dispersal. Dispersal distances were longer in females than in males as well as longer in yearlings than in older individuals. Body condition was positively correlated to breeding dispersal distances, particularly for females. The lowest dispersal distances were recorded for intermediate brood sizes in the year preceding dispersal. Our results highlight sex‐ and environment‐specific consequences of breeding dispersal on reproductive performance. During increase phases of the three‐year vole cycles, males dispersing further had lower reproductive performance after dispersal, whereas in females, long breeding dispersal distances were associated with increased breeding success under all environmental conditions. These results suggest benefits associated to breeding dispersal in females, potentially related to large spatio‐temporal variation in main food abundance and intensity of intra‐specific competition. Breeding dispersal of males was costly during increasing food abundance, indicating the potential fitness benefits of environmental familiarity in this migratory species. Overall, our results indicate that both individual traits and environmental factors interact to shape breeding dispersal strategies in wide‐ranging predator populations under fluctuating food conditions.     

Group size,composition, and reproductive success in wild common marmosets (Callithrix jacchus)

Data from published sources about size and composition of wild common marmoset groups (Callithrix jacchus) were analyzed to see if the number of juveniles in a group is closely related to the number of other group members. Mean group size was 8.7 members including 4.4 adults (1.8 females, 2.5 males), 2.9 subadults, and 1.4 juveniles. The number of juveniles was significantly positively correlated to the number of adult males. Groups with one or two adult males had significantly fewer juveniles (mean: 1:1 juveniles) than groups containing more than two adult males (mean: 2.0 juveniles). Apart from a different number of subadults, results showed obvious similarities between common marmosets and tamarins of the genus Saguinus in size and composition of subgroups of adults as well as the key role of adult males in mediating the reproductive success of a breeding female. Common marmoset females seem to gain direct fitness benefits in increased reproductive success from the presence of a larger number of adult males. Whether or not other group members get fitness benefits depends on the reproductive strategy of adult males (monogamy vs. polyandry), their kinship, and on the genetic relationship of nonbreeders to the offspring of the breeding female. © 1995 Wiley-Liss, Inc.