Reproductive skew in female common marmosets: what can proximate mechanisms tell us about ultimate causes?

Common marmosets are cooperatively breeding monkeys that exhibit high reproductive skew: most subordinate females fail to reproduce, while others attempt to breed but produce very few surviving infants. An extensive dataset on the mechanisms limiting reproduction in laboratory-housed and free living subordinate females provides unique insights into the causes of reproductive skew. Non-breeding adult females undergo suppression of ovulation and inhibition of sexual behaviour; however, they receive little or no aggression or mating interference by dominants and do not exhibit behavioural or physiological signs of stress. Breeding subordinate females receive comparable amounts of aggression to non-breeding females but are able to conceive, gestate and lactate normally. In groups containing two breeding females,however, both dominant and subordinate breeders kill one another's infants. These findings suggest that preconception reproductive suppression is not imposed on subordinate females by dominants, at a proximate level, but is instead self-imposed by most subordinates, consistent with restraint models of reproductive skew. In contrast to restraint models, however, this self-suppression probably evolved not in response to the threat of eviction by dominant females but in response to the threat of infanticide. Thus,reproductive skew in this species appears to be generated predominantly by subordinate self-restraint, in a proximate sense, but ultimately by dominant control over subordinates' reproductive attempts.     

Reproductive control via eviction (but not the threat of eviction) in banded mongooses

Considerable research has focused on understanding variation in reproductive skew in cooperative animal societies, but the pace of theoretical development has far outstripped empirical testing of the models. One major class of model suggests that dominant individuals can use the threat of eviction to deter subordinate reproduction (the ‘restraint’ model), but this idea remains untested. Here, we use long-term behavioural and genetic data to test the assumptions of the restraint model in banded mongooses (Mungos mungo), a species in which subordinates breed regularly and evictions are common. We found that dominant females suffer reproductive costs when subordinates breed, and respond to these costs by evicting breeding subordinates from the group en masse, in agreement with the assumptions of the model. We found no evidence, however, that subordinate females exercise reproductive restraint to avoid being evicted in the first place. This means that the pattern of reproduction is not the result of a reproductive ‘transaction’ to avert the threat of eviction. We present a simple game theoretical analysis that suggests that eviction threats may often be ineffective to induce pre-emptive restraint among multiple subordinates and predicts that threats of eviction (or departure) will be much more effective in dyadic relationships and linear hierarchies. Transactional models may be more applicable to these systems. Greater focus on testing the assumptions rather than predictions of skew models can lead to a better understanding of how animals control each other''s reproduction, and the extent to which behaviour is shaped by overt acts versus hidden threats.     

Infanticide by subordinates influences reproductive sharing in cooperatively breeding meerkats

In cooperative animal societies, dominant females typically show higher breeding success than subordinates, and are commonly believed to control the extent of reproductive sharing. However, studies of social insect societies reveal that subordinates too can interfere with the breeding attempts of others, with important implications for the distribution of fitness within colonies. Here, we show that subordinate females in a high-skew vertebrate (the meerkat, Suricata suricatta), also exert a substantial influence over the reproductive attempts of others. In meerkat societies, pregnant dominants are known to kill subordinate litters, but we show that pregnant subordinates also kill pups; not only those of other subordinates but the dominant's as well. Litters born to females of any rank were half as likely to survive their first 4 days if a subordinate was pregnant. However, dominant females were more likely than subordinates to give birth when no other females were pregnant, and so lost fewer litters to infanticide than subordinates. This is probably due in part to dominants employing counter-tactics to reduce the incidence of subordinate pregnancy. We discuss the broad implications of subordinates having a degree of control over reproductive sharing for future attempts to understand the distribution of reproduction in animal societies.     

Higher reproductive skew among birds than mammals in cooperatively breeding species

While competition for limited breeding positions is a common feature of group life, species vary widely in the extent to which reproduction is shared among females (‘reproductive skew’). In recent years, there has been considerable debate over the mechanisms that generate variation in reproductive skew, with most evidence suggesting that subordinates breed when dominants are unable to prevent them from doing so. Here, we suggest that viviparity reduces the ability of dominant females to control subordinate reproduction and that, as a result, dominant female birds are more able than their mammal counterparts to prevent subordinates from breeding. Empirical data support this assertion. This perspective may increase our understanding of how cooperative groups form and are stabilized in nature.     

Social control of reproduction in banded mongooses

Recent theoretical work suggests that the distribution of reproduction, or degree of reproductive skew, in animal societies depends crucially on (1) whether dominant individuals can fully control subordinate reproduction, and (2) how subordinate reproduction affects the fitness of dominants. I investigated these two factors in cooperatively breeding banded mongooses, Mungos mungo. Female packmates entered oestrus together and were closely guarded by dominant males. These males were aggressive to subordinate males who attempted to mate, but females still managed to mate with males other than their mate guard. Older females were guarded and mated a few days before their younger packmates, yet all females usually gave birth on the same day, suggesting that older females may have a longer gestation period. Moreover, older females carried more fetuses. Overall, ca. 83% of adult females conceived in each breeding attempt and 71% carried to term. These results indicate that, among males, dominant individuals did not have full control over the mating attempts of subordinates (since they could not fully control the mating behaviour of the females they guarded), while among females there was little or no attempt to prevent subordinates from breeding (at least, prior to parturition). Two within-group infanticides by males suggested that some control over reproduction may be exercised postpartum. Per capita survivorship of young in the den increased with the number of females who gave birth. Thus, dominant females may benefit from subordinate reproduction, providing a possible explanation for the lack of reproductive suppression among females in this species. Copyright 2000 The Association for the Study of Animal Behaviour.     

Sociality, mating system and reproductive skew in marmots: evidence and hypotheses

Marmot species exhibit a great diversity of social structure, mating systems and reproductive skew. In particular, among the social species (i.e. all except Marmota monax), the yellow-bellied marmot appears quite different from the others. The yellow-bellied marmot is primarily polygynous with an intermediate level of sociality and low reproductive skew among females. In contrast, all other social marmot species are mainly monogamous, highly social and with marked reproductive skew among females. To understand the evolution of this difference in reproductive skew, I examined four possible explanations identified from reproductive skew theory. From the literature, I then reviewed evidence to investigate if marmot species differ in: (1) the ability of dominants to control the reproduction of subordinates; (2) the degree of relatedness between group members; (3) the benefit for subordinates of remaining in the social group; and (4) the benefit for dominants of retaining subordinates. I found that the optimal skew hypothesis may apply for both sets of species. I suggest that yellow-bellied marmot females may benefit from retaining subordinate females and in return have to concede them reproduction. On the contrary, monogamous marmot species may gain by suppressing the reproduction of subordinate females to maximise the efficiency of social thermoregulation, even at the risk of departure of subordinate females from the family group. Finally, I discuss scenarios for the simultaneous evolution of sociality, monogamy and reproductive skew in marmots.     

Failures of reproductive suppression in dwarf mongooses (Helogale parvula): accident or adaptation?

In many communally breeding species, only the dominant femalenormally breeds, while subordinates tolerate reproductive suppression(these are "despotic" species, in the terminology of Brown,1987; Macdonald and Moehlman, 1983; Vehrencamp, 1983). Yet inmany species for which reproductive suppression is the norm(across a wide variety of taxa), subordinates do occasionallybreed. Because reproduction by subordinates is atypical forthese species, it is often regarded as simple failure of thenormal mechanisms of suppression. An alternate hypothesis isthat subordinate pregnancies represent an evolutionary compromisebetween dominant and subordinate, in which dominants concedetheir monopoly on reproduction in order to retain helpers. Weuse data from a long-term study of dwarf mongooses (Helogaleparvula) in Serengeti National Park, Tanzania, to test thishypothesis, using an inclusive fitness model adapted from oneby Vehrencamp (1983). We find that the incidence of subordinatepregnancy closely matches that predicted by the model, suggestingthat the mechanisms that underlie reproductive suppression indwarf mongooses are finely adjusted to the social and demographicenvironment. [Behav Ecol 1991; 2: 7–15]     

Group composition affects male reproductive partitioning in a cooperatively breeding cichlid

Individuals within groups of cooperatively breeding species may partition reproduction, with the dominant pair often taking the largest share. The dominant's ability to reproductively control subordinates may depend on differences in competitive ability, due to, e.g. body size differences, but may also depend on the number of same‐sex competitors inside the group. We tested experimentally whether subordinates reproduce more when these subordinates are large or when a second subordinate of the same sex need to be controlled by the dominants, using the cooperatively breeding cichlid Neolamprologus pulcher. Dominant pairs were assisted by a large and a small unrelated subordinate; sexes of these fish were varied in a full‐factorial design (giving four treatments). Dominant males lost significantly more parentage to the large subordinate male when a small subordinate male was also present, compared to when a small subordinate female was present. However, subordinate paternity was generally low and did not significantly curb total dominant male reproductive output, which was more affected by the sizes and numbers of reproductive females present inside his group. Dominant female maternity, clutch sizes and total output did not depend on the treatments. Subordinate–subordinate reproduction was virtually absent (one out of 874 offspring). Female subordinates were more likely to provide care for their own broods. In contrast, male subordinates did not adjust their level of care to their parentage. Variability in female subordinate alloparental brood care was particularly high, with females showing more care than males in general. We also detected effects of growth rate and food ration on parentage independent of the treatments, most notably: (i) a trade‐off between dominant male growth rate and paternity; (ii) a decrease in dominant male paternity with increasing food ration; (iii) a positive effect of growth rate on paternity in small males. We conclude that dominant males should be sensitive to the number and sizes of subordinate males present in their group, particularly when these subordinates are not helpful or grow fast, and food is plentiful. Dominant females should be less sensitive, because female subordinates do not appear to impose reproductive costs and can be helpful through alloparental brood care.     

The causes of physiological suppression among female meerkats: a role for subordinate restraint due to the threat of infanticide?

In many animal societies, subordinates exhibit down-regulated reproductive endocrine axes relative to those of dominants, but whether this 'physiological suppression' arises from active interference by dominants or subordinate self-restraint is a matter of debate. Here we investigate the roles that these processes play in precipitating physiological suppression among subordinate female meerkats, Suricata suricatta. We show that, while subordinate females are known to suffer stress-related physiological suppression during periodic temporary evictions by the dominant female, their low estrogen levels while within their groups cannot be readily attributed to chronic stress, as their fecal glucocorticoid metabolite levels during this time are comparable to those of dominants. The low estrogen levels of subordinate females also cannot be explained simply by self-restraint due to factors that could reduce their payoff from maintaining their fertility regardless of the presence of the dominant female (young age, a lack of unrelated mates, poor body condition and limited breeding experience), as substantial rank-related differences in fecal total-estrogen metabolite levels remain when such factors are controlled. We suggest that this residual difference in estrogen levels may reflect a degree of subordinate restraint due in part to the dominant female's ability to kill their young. Accordingly, subordinate female estrogen levels vary in association with temporal variation in the likelihood of infanticide by the dominant. Attempts to identify the causes of physiological suppression should be cautious if rejecting any role for dominant interference in favor of subordinate restraint, as the dominant's capacity to interfere may often be the reason why subordinates exercise restraint.     

Reproductive skew and the threat of eviction: a new perspective

Most recent models of the partitioning of reproduction attempt to explain patterns of skew on the assumption that dominant individuals have complete control over breeding opportunities within the group, but may nevertheless concede a share of direct reproduction to subordinates as an incentive to remain peacefully in the association. Although these models may be applicable to some animal societies, we argue that they fail to provide a comprehensive theory of skew. Instead, we suggest that subordinates may often be able to claim unsanctioned reproduction for themselves, but will be forced to exercise a degree of reproductive restraint lest they incite ejection by the dominant. Reproductive skew, in other words, may reflect the threat of ejection (inducing subordinate restraint) rather than the threat of subordinate departure (inducing reproductive concessions by dominants). We present a simple ESS model of reproductive skew under these circumstances, which demonstrates that a shift in emphasis from reproductive concessions by dominants to reproductive restraint on the part of subordinates, radically alters the predictions of skew models. High group productivity, high relatedness and (when group members are related) strong ecological constraints are all expected to lead to reduced skew (the opposite conclusions to those of previous, concession-based analyses). The reason is that these factors reduce the benefits (or increase the costs) of ejection to the dominant, who therefore does best to tolerate more subordinate reproduction.     

Benefits and Costs of Dominance in the Angelfish Centropyge bicolor

Social groups are often structured by dominance hierarchies in which subordinates consistently defer to dominants. High‐ranking individuals benefit by gaining inequitable access to resources, and often achieve higher reproductive success; but may also suffer costs associated with maintaining dominance. We used a large‐scale field study to investigate the benefits and costs of dominance in the angelfish Centropyge bicolor, a sequential hermaphrodite. Each haremic group contains a single linear body size‐based hierarchy with the male being most dominant, followed by several females in descending size order. Compared to their subordinate females, dominant males clearly benefited from disproportionately high spawning frequencies, but bore costs in lower foraging rates and greater aggressive defence of their large territories. Within the female hierarchy, more dominant individuals benefited from higher spawning frequencies and larger home ranges, but displayed neither higher foraging rates nor spawn order priority. However, dominance in females was also linked to aggressiveness, particularly towards immediate subordinates, suggesting that females were using energetically costly aggression to maintain their high rank. We further showed by experimentally removing dominant females that the linear hierarchy was also a social queue, with subordinates growing to inherit higher rank with its attendant benefits and costs when dominants disappeared. We suggest that in C. bicolor, the primary benefit of high rank is increased reproductive success in terms of current spawning frequency and the prospect of inheriting the male position in the near future, which may be traded off against the cost of aggressively defending rank and territory.     

Effect of the Presence of Subordinates on Dominant Female Behaviour and Fitness in Hierarchies of the Dwarf Angelfish Centropyge bicolor

In many hierarchical animal societies, dominant individuals control group membership owing to their power to evict subordinates. In such groups, the presence of subordinates, and therefore group stability, is continually dependent on subordinates being tolerated by dominants. The dominant decision to tolerate or evict is, in turn, dependent on the costs and benefits to dominants of subordinate presence. We investigated the effect of subordinate presence on dominants in the female dominance hierarchy of the dwarf angelfish Centropyge bicolor, using both observations of natural groups and experimental removals of subordinates. We found that the presence of subordinates had no effect on dominant access to resources, as measured by dominant foraging rates and home range areas, nor on dominant fitness, as measured by growth rates and spawning frequencies. Our results suggest that the presence of subordinates has a neutral effect on the current fitness of dominants, so that dominants have no great incentive to evict subordinates. We discuss the possibility that tolerance of subordinates might be further explained by considering future fitness, as dominant females in these haremic protogynous angelfish stand to inherit the male position, whereupon subordinate females change from potential competition to useful mates.     

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.     

Sibling rivalry: training effects, emergence of dominance and incomplete control

Within-brood or -litter dominance provides fitness-related benefits if dominant siblings selfishly skew access to food provided by parents in their favour. Models of facultative siblicide assume that dominants exert complete control over their subordinate sibling's access to food and that control is maintained, irrespective of the subordinate's hunger level. By contrast, a recent functional hypothesis suggests that subordinates should contest access to food when the cost of not doing so is high. Here, we show that within spotted hyena (Crocuta crocuta) twin litters, dominants most effectively skew access to maternal milk in their favour when their aggression prompts a highly submissive response. When hungry, subordinates were less submissive in response to aggression, thereby decreasing lost suckling time and increasing suckling time lost by dominants. In a species where adult females socially dominate adult males, juvenile females were more often dominant than males in mixed-sex litters, and subordinate sisters used more effective counter-tactics against dominant brothers than subordinate brothers against dominant sisters. Our results provide, to our knowledge, the first evidence in a mammal that dominant offspring in twin litters do not exert complete control over their sibling's access to resources (milk), and that sibling dominance relationships are influenced by sibling sex and training effects.     

Behavioural tactics of breeders in cooperative meerkats

In eusocial invertebrates, queens commonly show morphological and behavioural modifications to their role as the principal breeders in their colonies. With the exception of naked mole-rats, Heterocephalus glaber, morphological modification of breeders has yet to be shown in cooperative vertebrates, but the behaviour of dominant individuals may be modified so as to maximize reproductive success. We studied the cooperative behaviour of dominant and subordinate adults in meerkats, Suricata suricatta, and found that the decision rules governing the contributions of dominant breeders differed from those of subordinate helpers. Dominant breeders contributed less than adult helpers to babysitting and pup feeding, but raised their individual contributions to pup care to a greater extent when helper:pup ratios were low. In contrast to subordinates, dominant breeders did not increase their contributions when they foraged successfully. Finally, while subordinates of both sexes assisted in rearing the young when dominants bred, dominant females contributed little when subordinates attempted to breed, and male helpers (but not females) reduced their contributions to the care of pups. Our results suggest that the division of labour between breeders and helpers in meerkats is intermediate between that of facultatively cooperative species, where parents are principally responsible for rearing young, and that of specialized eusocial species, which show a well-defined division of labour between breeders and workers.     

A commitment model of reproductive inhibition in cooperatively breeding groups

Cooperatively breeding groups include individuals that giveup some current reproductive opportunities while remaining ina group. In some cases, these individuals are physiologicallyor morphologically unable to reproduce. Empirical and theoreticalevidence suggest that this inability often does not result fromstress or manipulation by dominants against the interests ofsubordinates. I argue that such reproductive inhibition canrepresent a commitment not to reproduce in exchange for a reductionin costs imposed by dominants. I present a model that allowssubordinates to choose whether to inhibit their own reproduction("self-inhibition") and accept no direct reproduction whilein the group or to remain flexible and attempt to take a shareof group productivity. If dominants assess the reproductivestatus of subordinates and punish those that reproduce, thismodel predicts self-inhibition when group members are closelyrelated, opportunities for independent breeding are poor, assessmentof reproductive status and eviction are costly, and the chanceof being detected when cheating is high. However, dominantsare less likely to assess the reproductive status of subordinatesthat are closely related, resulting in a narrow window of relatednessin which self-inhibition is favored. Counterintuitively, thiswindow is wider when flexible subordinates would be able totake a large share of group production. Although the model assumesthat dominants are able to reliably detect commitment, it isgenerally robust against mistakes in the form of dominants failingto assess uncommitted subordinates, or even low frequenciesof deception by flexible subordinates.     

Female eviction, abortion, and infanticide in banded mongooses (Mungos mungo): implications for social control of reproduction and synchronized parturition

Most cooperatively breeding species exhibit high reproductiveskew, where reproduction within the social group is monopolizedby a dominant pair. In many of these species, social controlof reproduction is the mechanism driving reproductive skew:individuals within the social group actively reduce the reproductivesuccess of others. In species where females do not suppressconception in other females, alternative routes to skewing thesocial group's reproductive output include inducing abortionin rivals, evicting them, or killing their young. This studyexamines instances of female eviction, abortion, and infanticidein a cooperatively breeding species with low preparturitionreproductive skew, the banded mongoose (Mungos mungo). Althoughinstances of these behaviors are rare in this species, aspectsof their occurrence have implications for social control ofreproduction. Abortion can be induced by the stress of beingevicted. The readmittance of females that abort suggests thatreducing communal litter size is a possible selective pressurefor eviction. This is supported by the occurrence of evictionevents in groups with relatively high numbers of reproductivefemales and by the eviction of young reproductive females. Thetiming of abortion events suggests that synchronization of parturitionwith other females in the group is a major selective pressure.Infanticide could represent the selective pressure for synchronizedparturition. Alternatively, synchronization may minimize competitiveasymmetry between pups born to different females. This paperalso describes incidences where a female aborts or gives birthto her litter over different days in order to synchronize parturition:behavior previously unrecorded in mammals.     

Assessing the cost of helping: the roles of body condition and oxidative balance in the Seychelles warbler (Acrocephalus sechellensis)

In cooperatively breeding species, helping close relatives may provide important fitness benefits. However, helping can be energetically expensive and may result in increased generation of reactive oxygen species. Consequently, an oxidant/antioxidant imbalance can lead to higher oxidative stress susceptibility. Given the potential costs of helping, it may be that only individuals with a sufficiently good body condition and/or stable oxidative balance can afford to help. Knowledge about relationships between social status and oxidative balance in cooperatively breeding systems is still limited. Studying these relationships is important for understanding the costs of helping and physiological pressures of reproduction. Here we evaluate the relationship between helping behaviour, body condition and oxidative balance in a wild population of the cooperatively breeding Seychelles warbler (Acrocephalus sechellensis). In this species, some subordinate individuals help dominant birds with the rearing of young, while others refrain from any assistance. We assessed body condition and oxidative parameters of birds of different social status caught during different breeding stages. We found that, prior to breeding, female subordinates that did not subsequently help (non-helpers) had significantly lower body condition and higher ROMs (reactive oxygen metabolites) than helpers and dominants. During the later stages of breeding, body condition was low in dominants and helpers, but high in non-helpers. Differences in oxidative balance between individuals of different social status were found only during nest care: Dominant males occupied with guarding behaviours tended to have relatively high oxidative stress susceptibility. Furthermore, dominant and helper females showed elevated antioxidant capacity (measured as OXY) in the weeks just prior to egg-laying, possibly representing a change in their reproductive physiology. The results imply that an individuals' oxidative balance may be influenced by factors related to reproduction, which can differ with sex and--within cooperative breeding systems--social status.     

Buffered development: resilience after aggressive subordination in infancy

Do aggressive dominance and subordination in vertebrate broods and litters affect development? We examined 1,167 fledglings from two-chick broods of the blue-footed booby (Sula nebouxii), a species in which the first-hatched chick dominates with violent attacks throughout the nestling period and subordinates suffer lower fledging success, but if both broodmates survive, they grow to the same size. There was little evidence that dominant fledglings were more likely to recruit into the breeding population than were subordinate fledglings, and there was no evidence that dominant and subordinate recruits differed in their age, date, brood size, or nest success at first reproduction or in their summed brood sizes or total nest success over the first 5 yr or first 10 yr of life. Compared with dominants, subordinate fledglings were less prejudiced by late hatching and established clutches earlier over the first 10 yr, and subordinate recruits had 33% larger broods over the first 5 yr. However, in broods where both chicks fledged, accumulated reproductive success for chicks up to age 5 yr was similar for dominants and subordinates. Exercising dominance throughout infancy apparently does not fortify a chick for the future and may incur a long-term cost, and suffering violent subordination throughout infancy has little or no prejudicial effect and may even steel a chick for adult life.