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.     

Hormonal correlates of dominance in meerkats (Suricata suricatta)

In cooperatively breeding meerkats (Suricata suricatta), individuals typically live in extended family groups in which the dominant male and female are the primary reproductives, while their offspring delay dispersal, seldom breed, and contribute to the care of subsequent litters. Here we investigate hormonal differences between dominants and subordinates by comparing plasma levels of luteinizing hormone (LH), estradiol and cortisol in females, and testosterone and cortisol in males, while controlling for potential confounding factors. In both sexes, hormone levels are correlated with age. In females, levels of sex hormone also vary with body weight and access to unrelated breeding partners in the same group: subordinates in groups containing unrelated males have higher levels of LH and estradiol than those in groups containing related males only. When these effects are controlled, there are no rank-related differences in circulating levels of LH among females or testosterone among males. However, dominant females show higher levels of circulating estradiol than subordinates. Dominant males and females also have significantly higher cortisol levels than subordinates. Hence, we found no evidence that the lower levels of plasma estradiol in subordinate females were associated with high levels of glucocorticoids. These results indicate that future studies need to control for the potentially confounding effects of age, body weight, and access to unrelated breeding partners before concluding that there are fundamental physiological differences between dominant and subordinate group members.     

Maternal investment during pregnancy in wild meerkats

Maternal investment in offspring development is a major determinant of the survival and future reproductive success of both the mother and her young. Mothers might therefore be expected to adjust their investment according to ecological conditions in order to maximise their lifetime fitness. In cooperatively breeding species, where helpers assist breeders with offspring care, the size of the group may also influence maternal investment strategies because the costs of reproduction are shared between breeders and helpers. Here, we use longitudinal records of body mass and life history traits from a wild population of meerkats (Suricata suricatta) to explore the pattern of growth in pregnant females and investigate how the rate of growth varies with characteristics of the litter, environmental conditions, maternal traits and group size. Gestational growth was slight during the first half of pregnancy but was marked and linear from the midpoint of gestation until birth. The rate of gestational growth in the second half of pregnancy increased with litter size, maternal age and body mass, and was higher for litters conceived during the peak of the breeding season when it is hot and wet. Gestational growth rate was lower in larger groups, especially when litter size was small. These results suggest that there are ecological and physiological constraints on gestational growth in meerkats, and that females may also be able to strategically adjust their prenatal investment in offspring according to the likely fitness costs and benefits of a particular breeding attempt. Mothers in larger groups may benefit from reducing their investment because having more helpers might allow them to lower reproductive costs without decreasing breeding success.     

Onset of plural cooperative breeding in common marmoset families following replacement of the breeding male

Common marmosets, Callithrix jacchus, are usually characterized as singular cooperative breeders, with only a single, dominant female reproducing in each group. Anecdotal reports, however, have described two females breeding concurrently when an unrelated male joins their group. We tested the hypothesis that incorporation of an unrelated adult male into a family systematically leads to the onset of reproductive activity in a daughter and investigated the underlying mechanisms. We collected hormonal and behavioural data from mothers and their eldest daughters before and after the father was removed from the family and either replaced by an unrelated male (N=11) or immediately returned to the family (N=7). Variation between daughters in the occurrence of ovulatory cyclicity was not associated with the presence of an unrelated male but was closely linked to daughters' relationships with their mothers: only anovulatory daughters behaved submissively towards their mothers. Daughters never engaged in sexual behaviour with their fathers, but most did so with unrelated males. Similarly, daughters never conceived in intact natal families but did so in eight of 11 families containing an unrelated male. In six of these families, the mother and daughter bred concurrently. Thus, incorporation of an unrelated adult male into a marmoset family may frequently lead to the onset of plural breeding by activating sexual behaviour in a daughter; however, daughters ovulate only if they are not behaviourally subordinate to their mothers. Therefore, both inbreeding avoidance and rank-related reproductive suppression may constrain reproduction in marmoset daughters and contribute to maintenance of singular breeding.     

Experience-based agonistic behavior in female crickets, Gryllus bimaculatus

Fighting behavior in male crickets is already well described, and some of the mechanisms underlying aggression and aggressive motivation have already been revealed. Much less is known about female/female interactions. Here, we report that adult female crickets that had been isolated for several days readily entered into agonistic interactions with conspecific individuals. Characteristic dyadic encounters between isolated females escalated in a stepwise manner and were concluded with the establishment of a dominant/subordinate relationship. For 15 to 30 minutes following an initial fight, former subordinate females showed a dramatic change in agonistic behavior. If they were paired with the former dominant opponent during this interval, a significant majority did not enter into any aggressive interaction but instead actively avoided the opponent. A similar experience-based and time-dependent increase in avoidance was observed when former subordinate females were paired with unfamiliar na?ve opponents. However, when faced with an unfamiliar subordinate individual in the second encounter, no such increase in avoidance behavior was observed. We propose that the observed changes in the behavior of former subordinate females are the consequence of a change in the general state of arousal and of the recognition of dominance status, but not of individual recognition. The fact that former dominant individuals did not show similar experience-based changes in agonistic behavior suggests that dominant/subordinate relationships between pairs of female crickets are maintained mainly by the behavior of subordinate individuals.     

Adaptive size modification by dominant female meerkats

In species of cooperative insects that live in large groups, selection for increased fecundity has led to the evolution of an increased body size among female reproductives, but whether this is also true of cooperative vertebrates is unknown. Among vertebrates, morphological modification of female breeders has only been documented in a single species; in naked mole rats (Heterocephalus glaber), acquisition of alpha status is associated with a significant increase in body size through an elongation of the lumbar vertebrae. Here we provide evidence of morphological modification among breeding females of a cooperative carnivore, the meerkat (Suricata suricatta), and demonstrate that this modification is likely to be adaptive. The same female meerkats were significantly larger when they were dominant than when they were subordinate. This increased body size was not explained by differences in age, foraging efficiency, or investment in offspring care, but may have arisen, in part, through increased levels of hormone that govern bone growth. Increases in body size are likely to result in fitness benefits, for large females delivered larger litters and had heavier offspring, both of which are known to correlate positively with measures of breeding success in meerkats. Our results suggest that the acquisition of alpha status in female meerkats is associated with an adaptive increase in body size and hence that morphological modification of female vertebrates may be more widespread than has been previously supposed.     

Lactation and care for unrelated infants in forest-living ringtailed Lemurs

An adult female ringtailed lemur (Lemur catta) known not to have been pregnant showed spontaneous lactation in response to twin infants born to an unrelated female. The females had met only 7 months earlier, when they and two other unrelated adult females were released from separate locations in a forest enclosure to form a new social group. Three months after release, an adult male from an adjacent enclosure gained access to the new group for 1 day, the day of one female's estrus. No males had access to the females throughout the remainder of the breeding season. Within 2 weeks of the birth of the twins, one of the other adult females began carrying the infants frequently, typically one at a time. All three females were checked for lactation when the infants were two months old. Both their mother and the unrelated adult who had been carrying the infants were producing milk. The third adult female, who never carried either infant, had no milk. The third adult female, who never carried either infant, had no milk. This female, however, like the two maternal females, frequently attacked unfamiliar immigrating adult males when the males approached the infants. Potential implications of these observations concerning the social organization of ringtailed lemurs are discussed.     

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.     

Subordinate Males in Harem Groups of Jamaican Fruit‐Eating Bats (Artibeus jamaicensis): Satellites or Sneaks?

In the caves of Yucatan, Mexico, the Jamaican fruit‐eating bat, Artibeus jamaicensis, forms harems consisting of four to 18 females and a dominant male that defends the group against foreign males. Large groups (>14 females) contain an additional subordinate male. In theory, subordinate males can associate with harem groups either as satellites, if they provide at least some benefits to the dominant male, or as sneaks, if they only impose costs on the dominant male. We assessed the costs and benefits of subordinate males in three removal experiments. In the first experiment, when a dominant male was removed from its group, its role was occupied by the subordinate male (in large groups) or by a foreign male (in small groups). Former subordinate males took less time to gain control of the harems and stayed longer with the groups than foreign males. In the second experiment, when a subordinate male was removed, the rate of visitation by foreign males and the number of agonistic displays by the dominant male both increased. In the third experiment, when the number of females in large groups was reduced, subordinate males spent less time with their groups and the rate of visitation by foreign males increased. However, the frequency of agonistic displays by dominant males towards subordinate males did not change. Dominant males invest large amounts of energy in defending the harems, but obtain direct and immediate benefits from the presence of subordinate males in the form of access to a larger number of females, and suffer no obvious costs. Subordinate males apparently invest little energy in defending the harems, obtain no obvious immediate benefit, but gain long‐term benefits by having priority access to vacant positions left by dominant males. Subordinate males in harem groups of the Jamaican fruit‐eating bat can be considered satellites because their presence brings immediate benefits to the dominant males.     

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.     

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.     

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.     

Effects of previous experience on the agonistic behaviour of male crickets, Gryllus bimaculatus

Male solitary animals frequently enter aggressive interactions with conspecific individuals to protect their territory or to gain access to females. After an agonistic encounter, the loser (subordinate individual) changes its behaviour from aggression to avoidance. We investigated agonistic interactions between pairs of male crickets to understand how dominance is established and maintained. Two na?ve males readily entered into agonistic interactions. Fights escalated in a stereotyped manner and were concluded with the establishment of dominance. If individuals were isolated after the first encounter and placed together 15 minutes later, subordinate crickets tended to avoid any further contact with the former dominant opponent. Moreover, subordinate males also avoided unfamiliar dominant and na?ve opponents. They displayed aggressive behaviour only towards unfamiliar subordinate opponents. This suggests that the subordinate male change their behaviour depending on the dominance status of the opponent. Dominant crickets, in contrast, displayed aggressive behaviour towards familiar as well as unfamiliar opponents. If the interval between the first and second encounter was longer than 30 minutes, the former subordinate male showed aggressive behaviour again. However, if the subordinate cricket was paired with the same opponent three consecutive times within 45 minutes, it avoided the former dominant opponent for up to 6 hours following the third encounter. Our results suggest that the maintenance of dominance in male crickets depends largely on the behavioural change of subordinate individuals. Possible mechanisms to maintain dominance are discussed.     

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.     

Male spotted hyenas (Crocuta crocuta) queue for status in social groups dominated by females

A long-term study of immigrant male spotted hyenas (Crocuta crocuta) living in large multimale/multifemale groups (clans) demonstrated that males acquire social status by queuing. Maximumlikelihood estimates of parameters of a stochastic queuingmodel that assessed queuing discipline confirmed that immigrantmales respected the convention that their positions in a queueof typically 15 or more individuals was determined by theirsequence of arrival. Levels of aggression among males were low;males did not attempt to improve their social status throughphysical contests. Size and body mass did not influence malesocial status. The stability of queues was insured by an increasein the rate at which males formed coalitions against othermales as they rose in social status and by coalitions between high-ranked males and dominant females. High-ranked, long-tenuredmales chiefly consorted with ("shadowed") and focused theiraffiliative behavior on females of high reproductive valueand disrupted attempts by subordinate males to associate withthese females. High-ranked males also supported females againstlower-ranked males that harassed them. In contrast, lower-ranked,short-tenured males focused their affiliative behavior on young adult females and rarely shadowed or defended females. Malesthat did not disperse from their natal clan (nondispersers)quickly acquired top rank in the male social hierarchy. Irrespectiveof the social status acquired from their mother when young,nondisperser adult males submitted to all adult females.     

雌性布氏田鼠对雄鼠气味的辨别

通过雌性布氏田导其配偶和陌生雄鼠气味的辨别实验,以及无交配经历的成年雌鼠对社会等级不同的陌生雄鼠气的辨别实验发现,有生育经历的雌鼠对陌生雄鼠气味的探究行为明显多于对配偶气味的控究,但雌鼠在配偶雄鼠气味周围的停留时间、自身修饰行为和何处行为的发生频次和持续地陌生雄鼠,没有交配经历的雌鼠对处于从鼠地位的雄性个体气味探究行为多于对优势雄性的控究,而其他行为表现没有明显差异。表明,雌性布氏田鼠可以利用气味     

Sex differences in the effect of social status on the growth of subordinates in a co-operatively breeding cichlid

Social influences on the growth of the co-operatively breeding cichlid Neolamprologus pulcher were studied by examining the size structure of existing laboratory groups and the responses of males and females to removals of higher-ranked fish, which created larger size differences with more dominant fish. The size differences between adjacently ranked group members were predicted to differ from expected based on random size distributions of group members. Both males and females were predicted to respond to removals by increasing growth rate. In previously established groups, the size difference between dominant and highest-ranked subordinate males was greater than expected based on random group-assembly rules. The size difference between dominant and subordinate females did not differ from the null expectation. Third-ranked subordinate males increased their growth rate upon moving up one place in the dominance hierarchy (after the removal of higher-ranking fish) relative to fish that did not change rank. Contrary to predictions, however, females did not increase growth upon increasing rank.     

Demography of male reproductive queues in cooperatively breeding superb fairy-wrens Malurus cyaneus

1. Subordinate helpers in cooperative societies may gain both immediate and future benefits, including paternity and territorial inheritance. However, if such opportunities correlate with rank in the queue, it is unclear why such queues should be stable. 2. In cooperatively breeding superb fairy-wrens Malurus cyaneus, only males are generally philopatric, and form stable hierarchical queues for the dominant position. 3. Male opportunities for reproduction are influenced both by their dominance status within the group, and their relatedness to the breeding female. For young queuing subordinates, the breeding female is typically their mother. Because of incest avoidance, reproduction is possible only through extra-group mating, even if the dominant position is achieved while the mother is still on the territory. If the mother dies while the helper is still a subordinate, he can seek matings both outside the group, and with the unrelated replacement female within the group. Finally, males can achieve the dominant position and pair with an unrelated female by inheritance, dispersal to a neighbouring vacancy, or by forming a liaison with an immigrant subordinate female that causes fission of the natal territory. 4. On average males spent more time living with unrelated females than with their mother. Subordinate males gained no survival advantages when living with their mother rather than an unrelated female, contrary to the prediction that parents facilitate the survival of their offspring. 5. Dominants and subordinates also had similar survival. Mortality accelerated over time, probably because older males invest more in extra-group courtship display. 6. Fairy-wren queues are likely to be stable because older birds are superior, and because extra-pair mating provides direct benefits to subordinates.     

Male endocrine responses to females: Effects of social cues in cynomolgus macaques

This study tested the hypothesis that the hormonal responses of male macaques to sexually receptive females are mediated by specific socioenvironmental cues. Twelve, socially living male Macaca fascicularis were exposed to two-ovariectomized, estrogen-primed females under pair test, peer group, and peer group without dominant male conditions. Preexposure to postexposure changes in serum cortisol levels and testosterone levels were examined in relation to male dominance rank, age, and conditions of access to stimulus females. The males displayed significantly lower cortisol increases and greater testosterone increases with females under peer group than pair test conditions. Dominant males displayed greater testosterone increases than subordinate males under peer group conditions. The testosterone levels of subordinate males were greatly enhanced by removing the dominant male from each group. Adult males displayed greater cortisol responsivity to changes in conditions of access to females than did subadult males. Subadult males displayed greater testosterone responsivity to removal of the dominant male from the group than did adult males. It is concluded that specific social cues can greatly influence the endocrine responses of males to receptive females, and further, that there may be optimal socioenvironmental parameters for eliciting testosterone increases in male primates.     

The energetics of lactation in cooperatively breeding meerkats Suricata suricatta

Species may become obligate cooperative breeders when parents are unable to raise their offspring unassisted. We measured the daily energy expenditure of mothers, helpers and offspring during peak lactation in cooperatively breeding meerkats Suricata suricatta using the doubly labelled water technique. Lactating mothers expended more energy per day than allo-lactating subordinate females, non-lactating females or suckling offspring. Metabolizable energy intakes of lactating mothers were calculated from isotope-based estimates of offspring milk energy intake, and were not significantly different from the previously suggested maximal limit for mammals. Allo-lactating females were the only category of animals that lost weight during the period of study, probably because they spent more time babysitting than non-lactating females. Daily energy expenditure (DEE) of lactating mothers increased with litter size but decreased with the number of helpers. Calculations show that for every 10 helpers, even in the absence of allo-lactators, mothers are able to reduce their DEE during peak lactation by an amount equivalent to the energy cost of one pup. These results indicate that helpers have beneficial energetic consequences for lactating mothers in an obligate cooperatively breeding mammal.