The number of subordinates moderates intrasexual competition among males in cooperatively breeding meerkats

For dominant individuals in cooperatively breeding species, the presence of subordinates is associated with both benefits (i.e. increased reproductive output and other group-living benefits) and costs (i.e. intrasexual competition on reproduction). The biological market theory predicts that dominant individuals are tolerant to same-sex group members when there are only a few subordinates, so as to maximize their own reproductive success. We investigated factors affecting aggression by dominant males and submission by subordinate males for a cooperatively breeding mammal, meerkats, Suricata suricatta. In this species, reproductive conflict occurs between the dominant male and the non-offspring males. As predicted, the number of subordinates in a group was positively associated with the aggression frequency by the dominant male and with the submission frequency by the subordinate males. Relative to the aggression frequency against male offspring, the frequency of aggression against non-offspring males was comparable in small groups, but was higher in large groups. These results indicate that reproductive conflict is present between the dominant male and the non-offspring males but is moderated in groups with small numbers of subordinates. This study provides an empirical data agreeing with the biological market theory in the context of intrasexual competition in cooperatively breeding species.     

Social dominance does not increase oxidative stress in a female dominance hierarchy of an African cichlid fish

In many group living animal species, individuals use aggression to gain and maintain social dominance to secure access to ecological resources and potential mates. While social dominance has many fitness benefits, there are also potential costs associated with frequent agonistic interactions and status display. One potential cost of social dominance is oxidative stress, the imbalance of reactive oxygen species and antioxidant capacity. In the cichlid species Astatotilapia burtoni, dominant males are aggressive, hold a breeding territory, and have an activated reproductive system resulting in larger gonads. Subordinate males are submissive, school with females, and are nonreproductive. Females are submissive under natural conditions, but in a female-only group, a dominance hierarchy will form with dominant females taking on male-typical behaviours including aggression, territory defence, and increased androgen levels. However, in contrast to males, social dominance is not linked to increased activation of the reproductive system in females, allowing us to test whether social dominance alone exposes individuals to increased oxidative stress. We compared dominant and subordinate females in female-only groups in five markers of oxidative stress. Dominant females did not have higher levels of oxidative damage compared to same-sex subordinates. This result contrasted to the trend in males in which dominant males had higher oxidative damage than their subordinate counterparts. Our findings suggest that the oxidative cost of social dominance is limited and support the notion that previously reported associations between high rank and increased oxidative stress is most likely driven by increased investment in reproduction.     

Effects of social status, age, and season on androgen and cortisol levels in wild male golden lion tamarins (Leontopithecus rosalia)

This study examines factors affecting androgen and cortisol levels in wild, male golden lion tamarins (Leontopithecus rosalia). Golden lion tamarins are a cooperatively breeding species in which groups often contain two potentially breeding males. Brothers frequently emigrate together and develop a clear dominance hierarchy, but interactions between them are primarily affiliative. Duos in which the males are not related are less stable. In addition, reproductive skew theory predicts that dominant males will be less likely to share reproduction with related subordinates. As such, we predicted that both androgens and cortisol would be higher in subordinate males unrelated to the dominant male. We also predicted that androgens in breeding males would be higher during the mating season than the birth/infant care season, as per Wingfield's "challenge hypothesis" (1990). Fecal samples were collected from 24 males in 14 social groups and assayed by enzyme immunoassay. Androgen levels were higher in breeding males during the mating season, thus supporting the challenge hypothesis. However, while subordinate males unrelated to the dominant male had significantly lower androgens than any other group, cortisol levels were not correspondingly higher. These results suggest that unrelated subordinate males show measurable reproductive suppression and may use strategies such as infantilization to avert aggression from dominant males.     

Socially induced brain differentiation in a cooperatively breeding songbird

Birds living in social groups establish dominance hierarchies, and taking up the dominant position influences behaviour and physiological parameters. In cooperatively breeding white-browed sparrow weavers (Plocepasser mahali), the transition from subordinate helper to dominant breeder male induces the production of a new type of song. This song contains a large number of new syllables and differs in temporal pattern from duet songs produced by all other group members. Here we show that this change in social status of adult males affects the morphology of a behavioural control circuit, the song control system of songbirds that is composed of large neuron populations. The volume of the song control areas HVC and RA and their gene-expression levels depend on males' social status. Dominant males have several times larger testes than subordinates, which is not reflected in circulating androgen and oestrogen levels. Our findings suggest a remarkable differentiation of adult vertebrate brains in relation to changing social cues.     

Reproductive sharing in relation to group and colony-level attributes in a cooperative breeding fish

The degree to which group members share reproduction is dictated by both within-group (e.g. group size and composition) and between-group (e.g. density and position of neighbours) characteristics. While many studies have investigated reproductive patterns within social groups, few have simultaneously explored how within-group and between-group social structure influence these patterns. Here, we investigated how group size and composition, along with territory density and location within the colony, influenced parentage in 36 wild groups of a colonial, cooperatively breeding fish Neolamprologus pulcher. Dominant males sired 76% of offspring in their group, whereas dominant females mothered 82% of offspring in their group. Subordinate reproduction was frequent, occurring in 47% of sampled groups. Subordinate males gained more paternity in groups located in high-density areas and in groups with many subordinate males. Dominant males and females in large groups and in groups with many reproductively mature subordinates had higher rates of parentage loss, but only at the colony edge. Our study provides, to our knowledge, the first comprehensive quantification of reproductive sharing among groups of wild N. pulcher, a model species for the study of cooperation and social behaviour. Further, we demonstrate that the frequency of extra-pair parentage differs across small social and spatial scales.     

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.     

Small Subordinate Male Advantage in the Zebrafish

Dominance is an important determinant of reproductive success in many species, and size is usually an indicator of dominance status, with larger, dominant individuals physically and physiologically preventing smaller subordinates from mating. However, small size may be advantageous in some mating contexts because enhanced manoeuvrability enables males to get closer to females during mating. Here, we determined the paternity success and testes size of dominant and subordinate male zebrafish (Danio rerio), in pairs that controlled for social status. There was no statistical difference in both body size and testes size between dominant and subordinate males. Dominant males sired significantly more offspring than subordinates, but when subordinates were small, they had a greater share of the paternity than larger subordinates. Small male advantage may be one mechanism by which variation in body size is maintained in this species.     

Paternity and dominance loss in male breeders: the cost of helpers in a cooperatively breeding mammal

Paternity insurance and dominance tenure length are two important components of male reproductive success, particularly in species where reproduction is highly skewed towards a few individuals. Identifying the factors affecting these two components is crucial to better understand the pattern of variation in reproductive success among males. In social species, the social context (i.e. group size and composition) is likely to influence the ability of males to secure dominance and to monopolize reproduction. Most studies have analyzed the factors affecting paternity insurance and dominance tenure separately. We use a long term data set on Alpine marmots to investigate the effect of the number of subordinate males on both paternity insurance and tenure of dominant males. We show that individuals which are unable to monopolize reproduction in their family groups in the presence of many subordinate males are likely to lose dominance the following year. We also report that dominant males lose body mass in the year they lose both paternity and dominance. Our results suggest that controlling many subordinate males is energetically costly for dominant males, and those unable to support this cost lose the control over both reproduction and dominance. A large number of subordinate males in social groups is therefore costly for dominant males in terms of fitness.     

Beyond aggression: Androgen-receptor blockade modulates social interaction in wild meerkats

In male vertebrates, androgens are inextricably linked to reproduction, social dominance, and aggression, often at the cost of paternal investment or prosociality. Testosterone is invoked to explain rank-related reproductive differences, but its role within a status class, particularly among subordinates, is underappreciated. Recent evidence, especially for monogamous and cooperatively breeding species, suggests broader androgenic mediation of adult social interaction. We explored the actions of androgens in subordinate, male members of a cooperatively breeding species, the meerkat (Suricata suricatta). Although male meerkats show no rank-related testosterone differences, subordinate helpers rarely reproduce. We blocked androgen receptors, in the field, by treating subordinate males with the antiandrogen, flutamide. We monitored androgen concentrations (via baseline serum and time-sequential fecal sampling) and recorded behavior within their groups (via focal observation). Relative to controls, flutamide-treated animals initiated less and received more high-intensity aggression (biting, threatening, feeding competition), engaged in more prosocial behavior (social sniffing, grooming, huddling), and less frequently initiated play or assumed a ‘dominant’ role during play, revealing significant androgenic effects across a broad range of social behavior. By contrast, guarding or vigilance and measures of olfactory and vocal communication in subordinate males appeared unaffected by flutamide treatment. Thus, androgens in male meerkat helpers are aligned with the traditional trade-off between promoting reproductive and aggressive behavior at a cost to affiliation. Our findings, based on rare endocrine manipulation in wild mammals, show a more pervasive role for androgens in adult social behavior than is often recognized, with possible relevance for understanding tradeoffs in cooperative systems.     

Social Opportunity Rapidly Regulates Expression of CRF and CRF Receptors in the Brain during Social Ascent of a Teleost Fish,Astatotilapia burtoni

In social animals, hierarchical rank governs food availability, territorial rights and breeding access. Rank order can change rapidly and typically depends on dynamic aggressive interactions. Since the neuromodulator corticotrophin releasing factor (CRF) integrates internal and external cues to regulate the hypothalamic-pituitary adrenal (HPA) axis, we analyzed the CRF system during social encounters related to status. We used a particularly suitable animal model, African cichlid fish, Astatotilapia burtoni, whose social status regulates reproduction. When presented with an opportunity to rise in rank, subordinate A. burtoni males rapidly change coloration, behavior, and their physiology to support a new role as dominant, reproductively active fish. Although changes in gonadotropin-releasing hormone (GnRH1), the key reproductive molecular actor, have been analyzed during social ascent, little is known about the roles of CRF and the HPA axis during transitions. Experimentally enabling males to ascend in social rank, we measured changes in plasma cortisol and the CRF system in specific brain regions 15 minutes after onset of social ascent. Plasma cortisol levels in ascending fish were lower than subordinate conspecifics, but similar to levels in dominant animals. In the preoptic area (POA), where GnRH1 cells are located, and in the pituitary gland, CRF and CRF₁ receptor mRNA levels are rapidly down regulated in ascending males compared to subordinates. In the Vc/Vl, a forebrain region where CRF cell bodies are located, mRNA coding for both CRFR₁ and CRFR₂ receptors is lower in ascending fish compared to stable subordinate conspecifics. The rapid time course of these changes (within minutes) suggests that the CRF system is involved in the physiological changes associated with shifts in social status. Since CRF typically has inhibitory effects on the neuroendocrine reproductive axis in vertebrates, this attenuation of CRF activity may allow rapid activation of the reproductive axis and facilitate the transition to dominance.     

Subordinate male cichlids retain reproductive competence during social suppression

Subordinate males, which are excluded from reproduction often save energy by reducing their investment in sperm production. However, if their position in a dominance hierarchy changes suddenly they should also rapidly attain fertilization capability. Here, we asked how social suppression and ascension to dominance influences sperm quality, spermatogenesis and reproductive competence in the cichlid Astatotilapia burtoni, where reproduction is tightly coupled to social status. Dominant territorial (T) males are reproductively active while subordinate non-territorial (NT) males are suppressed, but given the opportunity, NT males will perform dominance behaviours within minutes and attain T male testes size within days. Using the thymidine analogue 5-bromo-2-deoxyuridine (BrdU) to label germ cell proliferation, we found that the spermatogenic cycle takes approximately 11-12 days, and social status had no effect on proliferation, suggesting that spermatogenesis continues during reproductive suppression. Although sperm velocity did not differ among social states, NT males had reduced sperm motility. Remarkably, males ascending in status showed sperm motility equivalent to T males within 24 h. Males also successfully reproduced within hours of social opportunity, despite four to five weeks of suppression and reduced testis size. Our data suggest that NT males maintain reproductive potential during suppression possibly as a strategy to rapidly improve reproductive fitness upon social opportunity.     

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.     

Influence of reproductive season and rank on fecal glucocorticoid levels in free-ranging male Verreaux's sifakas (Propithecus verreauxi)

Studies in anthropoid primates and other mammals suggest that reproductive season, rank, reproductive skew, aggression received, and social support are the major factors influencing glucocorticoid output. In which way these are also affecting adrenal function in lemurid primates has been studied rarely. Here, we examine the influence of reproductive season and rank on glucocorticoid output in male sifakas (Propithecus verreauxi), a species characterized by high breeding seasonality, a hierarchy among males and extreme reproductive skew towards dominant males. We established a fecal assay for non-invasively monitoring adrenal activity and collected 315 fecal samples during the reproductive and birth season from 10 male sifakas living in 5 groups in Western Madagascar. We found a significant effect of season on glucocorticoid output, with males exhibiting higher fecal glucocorticoid levels during the reproductive compared to the birth season in conjunction with an increase in overall aggression rates during the former period. Moreover, our data indicate a significant effect of rank on adrenocortical activity with dominant males exhibiting higher glucocorticoid levels than subordinate males in the reproductive season. However, dominant males did not differ significantly in rates of initiated or received aggression and rates of affiliative behavior from subordinates but showed significantly lower rates of submission. Given their highly formalized dominance relationships, we conclude that higher glucocorticoid output in dominant males during the 4-month reproductive season is likely related to higher energetic demands necessary to cope with the challenges of male reproduction rather than to physical demands of increased fighting frequency to maintain dominance status. High rank in sifakas may thus carry high costs, which, however, may be outweighed by monopolization of almost all paternities. In sum, our data generally support the findings on the relationship between environmental and social factors and glucocorticoid output found in non-lemurid primates.     

Male reproductive suppression in the cooperatively breeding fish Neolamprologus pulcher

In most cooperative breeders, dominants suppress the reproductionof subordinates. However, two previous studies of Neolamprologuspulcher, a cooperatively breeding cichlid fish, have suggestedthat socially subordinate helper males sneak fertilizationsfrom dominant breeding males. If such sneaking does occur, boththeoretical work and empirical studies of other fish speciessuggest that sperm competition will select for increased reproductiveinvestment by sneaker males, relative to more dominant males.To address these issues, we quantified gonadal investment andsperm characteristics of 41 N. pulcher male breeders and 62male helpers from 55 groups in Lake Tanganyika. Gonadal investmentfollowed patterns consistent with reproductive suppression,with breeders having considerably larger testes masses thanhelpers. Breeders also had faster and longer swimming spermand a higher percentage of motile sperm compared to helpers.However, sperm characteristics of large helpers were similarto those of breeders, but these same helpers had lower testesmasses. Thus, large helpers had sperm that were physiologicallyequivalent to that of breeders, but their relatively small gonadsimply that they were reproductively suppressed.     

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.     

Masculinized dominant females in a cooperatively breeding species

The molecular mechanisms underlying complex social behaviours such as dominance are largely unknown. Studying the cooperatively breeding African cichlid Neolamprologus pulcher, we show that dominant females were similar to dominant males in dominance behaviour, high testosterone levels and brain arginine vasotocin expression (a neuropeptide involved in vertebrate territorial, reproductive and social behaviours) compared to subordinate helpers, but had lower levels of 11-ketotestosterone than males. Furthermore, brain gene expression profiles of dominant females were most similar to those of the males (independent of social rank). Dominant breeder females are masculinized at the molecular and hormonal level while being at the same time reproductively competent, suggesting a modular organization of molecular and endocrine functions, allowing for sex-specific regulation.     

Females of an African cichlid fish display male-typical social dominance behavior and elevated androgens in the absence of males

Social environment can affect the expression of sex-typical behavior in both males and females. Males of the African cichlid species Astatotilapia burtoni have long served as a model system to study the neural, endocrine, and molecular basis of socially plastic dominance behavior. Here we show that in all-female communities of A. burtoni, some individuals acquire a male-typical dominance phenotype, including aggressive territorial defense, distinctive color patterns, and courtship behavior. Furthermore, dominant females have higher levels of circulating androgens than either subordinate females or females in mixed-sex communities. These male-typical traits do not involve sex change, nor do the social phenotypes in all-female communities differ in relative ovarian size, suggesting that factors other than gonadal physiology underlie much of the observed variation. In contrast to the well-studied situation in males, dominant and subordinate females do not differ in the rate of somatic growth. Dominant females are not any more likely than subordinates to spawn with an introduced male, although they do so sooner. These results extend the well known extraordinary behavioral plasticity of A. burtoni to the females of this species and provide a foundation for uncovering the neural and molecular basis of social dominance behavior while controlling for factors such as sex, gonadal state and growth.     

Gender Differences in the Costs that Subordinate Group Members Impose on Dominant Males in a Cooperative Breeder

In group-living species, a dominant male's ability to monopolize reproduction, and the cost of doing so, are expected to vary with a group's gender composition. We used spawning observations of a group-living cichlid, Neolamprologus pulcher , to test this expectation. We constructed groups that contained a dominant breeding pair and either two male subordinates, one male and one female subordinate or two female subordinates. Parasitic spawning by male subordinates was more common in groups with two male subordinates than in groups with one male and one female subordinate. Female subordinates were never observed laying eggs in dominant females' clutches, but three female subordinates laid independent clutches. During spawning, frequencies of dominant male aggression towards male and female subordinates were similar. Dominant males were less aggressive during non-reproductive periods. The declines were greater for female subordinates, such that, during non-reproductive periods, dominant males were more aggressive towards male subordinates. Aggression towards each subordinate was also affected by the second subordinate's gender; the direction of that effect differed for large and small subordinates. Male subordinates approached breeding shelters less often than female subordinates, and both male and female subordinates approached shelters more frequently when the second subordinate was male. Collectively, these patterns suggest: (1) that male subordinates impose higher costs on dominant males than female subordinates do and (2) that the presence of a second male subordinate imposes additional costs beyond those of the first male subordinate. We discuss the implications of these effects for dominant and subordinate group members.