Significance In social insects, selfish reproduction by workers is suppressed by “policing” behavior, whereby queens and workers identify and destroy worker-laid eggs. An alternative method of policing is to use deterrent threats to prevent offspring production in the first place. Our 7-y field experiment on wild banded mongooses, Mungos mungo, shows that selection to evade the threat of infanticide by older, socially dominant females can explain the evolution of remarkable birth synchrony in this species. The results suggest that reproduction in animal societies can be shaped by threats of punishment that remain hidden until they are triggered experimentally. It follows that coercion may be more widespread than we currently realize.

Abstract The evolution of cooperation in animal and human societies is associated with mechanisms to suppress individual selfishness. In insect societies, queens and workers enforce cooperation by “policing” selfish reproduction by workers. Insect policing typically takes the form of damage limitation after individuals have carried out selfish acts (such as laying eggs). In contrast, human policing is based on the use of threats that deter individuals from acting selfishly in the first place, minimizing the need for damage limitation. Policing by threat could in principle be used to enforce reproductive suppression in animal societies, but testing this idea requires an experimental approach to simulate reproductive transgression and provoke out-of-equilibrium behavior. We carried out an experiment of this kind on a wild population of cooperatively breeding banded mongooses (Mungos mungo) in Uganda. In this species, each group contains multiple female breeders that give birth to a communal litter, usually on the same day. In a 7-y experiment we used contraceptive injections to manipulate the distribution of maternity within groups, triggering hidden threats of infanticide. Our data suggest that older, socially dominant females use the threat of infanticide to deter selfish reproduction by younger females, but that females can escape the threat of infanticide by synchronizing birth to the same day as older females. Our study shows that reproduction in animal societies can be profoundly influenced by threats that remain hidden until they are triggered experimentally. Coercion may thus extend well beyond the systems in which acts of infanticide are common.

The suppression of reproductive competition in animal societies promotes the evolution and maintenance of cooperation because it ensures that helpers or workers can maximize their inclusive fitness only by maximizing the fitness of the group (1, 2). Pioneering work on social Hymenoptera has shown that worker reproduction is suppressed by “policing” behavior, whereby queens and other workers identify and destroy worker-laid eggs (3, 4). This form of insect policing serves primarily to reduce the damaging impact of individually selfish behavior (i.e., egg laying) on the fitness of the group (5). Comparative data suggest that efficient policing can, over evolutionary time, reduce to a low level the proportion of colony workers that develop their ovaries and become reproductively active (4). However, in some systems [e.g., honey bees, common wasp Vespula vulgaris, European wasp Vespula germanica (4)] workers still commit to producing eggs even when these are almost certain to be policed, suggesting that policing does not have a deterrent effect on the reproductive decisions of these individual workers. In contrast, in human societies crime or defection is policed using deterrent threats that raise the perceived costs to individuals of engaging in selfish behavior (6, 7). Individuals can then make an informed decision to refrain from selfish acts if these are likely to trigger punishment, and so the punishments themselves rarely need to be carried out (6⇓⇓⇓–10). While the level of policing and transgression in insect societies is typically assumed to be genetically “hard wired” into the system [that is, determined by obligately expressed “sealed bid” strategies (11⇓⇓–14)], policing by threat requires that individuals are socially sensitive and responsive on a behavioral timescale to the actions (and anticipated actions) of their social partners (10).

The idea that social animals might use threats to police reproduction has been little explored to date because existing models of policing (2, 11, 12, 14⇓–16) do not use “extensive-form” game theory, which is designed to analyze how threats influence strategic behavior (6), and because observational studies on their own cannot detect effective threats (8, 9). To reveal such threats requires an experimental approach to manipulate the status quo and break the social rules that threats are used to enforce (9, 17). In the case of reproductive competition, the influence of threats on the distribution of reproduction (or degree of reproductive skew) within groups can be tested by manipulating skew while keeping group size and composition intact. We carried out an experiment of this kind on banded mongooses, a species in which multiple females in each group contribute offspring to a communal litter (18⇓–20), and much of the postnatal care of offspring is provided by nonbreeding males (21⇓⇓–24).

At our study site in Uganda banded mongooses live in mixed-sex groups of around 20 adults, plus offspring, and groups breed on average four times per year (25). At any one time the study population consists of 10–13 groups. Each group contains a cohort of one to five older, dominant adult females (typically age 4+ y) plus one to eight younger subordinate adult females (typically 1–3 y old). Older females are classed as socially dominant because they aggressively evict younger females from the group when the number of adult females grows large (20); in contrast, younger females do not evict older breeders. Multiple females reproduce in each breeding attempt (mean = 3.4, range 1–12). On average 74% (± 29%; mean ± SE) of dominant females and 49% (± 38%) of subordinate females in each group become pregnant in each breeding attempt (n = 107 attempts). Pregnant females give birth together to a communal litter in an underground den, usually on the same day [i.e., in 64% of 294 communal litters (26)].

Female banded mongooses could in principle gain an advantage in pup–pup competition by giving birth a few days before other breeders in the group (26). However, when females do give birth asynchronously (i.e., on different days), the offspring of first-birthing females almost always die within the first few days, whereas the offspring of last-birthing females almost always survive (26). This dependence of immediate postnatal survival on the pregnancy status of other breeding females in the group is a signature of female infanticide (27) and tallies with direct observations of female infanticide in this system (26) (Methods). Overall, early-life pup survivorship in asynchronous communal litters is approximately half that of pups in synchronous litters (26), and females that conceive particularly early appear to extend gestation to achieve birth synchrony with other females in their group (28). We hypothesize, therefore, that females synchronize birth to the same day to escape the threat of infanticide, either because birth synchrony removes temporal and spatial cues to maternity in communal litters (18, 28), or because females that have just given birth are mechanistically inhibited from killing offspring (26). We tested our hypothesis by inducing banded mongooses to reproduce out of synchrony using short-acting contraceptives.

Our design consisted of three experiments. In Exp. 1 we suppressed reproduction in all subordinate females and allowed all dominant females to breed (Methods). This experiment tested whether dominant females suffer fitness costs when subordinates also breed, and whether subordinates kill litters when they have not given birth themselves. In Exp. 2 we suppressed all subordinates and all except a single dominant female breeder, thereby mimicking the high skew pattern of reproduction seen in other cooperatively breeding mongooses [e.g., meerkats Suricata suricatta (29), and dwarf mongooses Helogale parvula (30)]. This experiment tested whether single dominant females stand to gain from fully monopolizing reproduction, as assumed by most reproductive skew models (31⇓⇓⇓–35). In Exp. 3 we suppressed all dominant female breeders and left subordinate females to breed. This experiment tested how dominant females exercise reproductive control over subordinate reproduction, and in particular whether dominant females kill litters when they have not given birth themselves. In all cases we compared breeding attempts in which we suppressed females using contraceptive (“EXP” attempts) with control breeding attempts in the same group immediately before and after the treatment (labeled “PRE” and “POST” breeding attempts, respectively). The design of our experiment and the resulting number of dominant and subordinate breeders in PRE, EXP, and POST breeding attempts is illustrated in the top row of Fig. 1.

Fig. 1. Results of the three suppression experiments. (A–C) Number of dominant and subordinate breeders in synchronous breeding attempts before treatment with contraceptive (PRE), the treatment breeding attempt (EXP), and the breeding attempt subsequent to the treatment (POST). (D–F) Individual reproductive success (measured as the number of pups reared to independence) of: (D) dominant females that reproduced in Exp. 1; (E) the single dominant female left untreated in Exp. 2; (F) subordinate females in Exp. 3. (G–I) Probability of whole-litter failure in the first week after birth. Symbols: ∼ P = 0.06, *P < 0.05, **P = 0.012; asterisks refer to statistical tests across all three categories: in D–F, Friedman tests; in G–I, GLMM. Exp. 1: n = 12 breeding attempts in each of PRE, EXP, POST; Exp. 2: n = 8; Exp. 3: n = 9. Bars show SE.

Methods Study Population. The research was carried out under a permit from Uganda Wildlife Authority and Uganda National Council for Science and Technology, and all methods approved by the ethical review panel of the University of Exeter. Data were collected from 11 groups of banded mongooses, living on and around Mweya Peninsula in Queen Elizabeth National Park Uganda (0°12′S; 29°53′E), between November 2005 and January 2013. Descriptions of habitat, climate, and study population are provided elsewhere (18). All individuals were marked with color-coded plastic collars or unique shave marks, and groups were visited every 3 d to determine group composition (or daily when birth was imminent). Infanticide typically occurs in the den, so is rarely observed in our population. Between November 1995 and April 2008 we observed within-group infanticide on 24 occasions, all within 1 wk of birth (26). In 16 of these cases dead pups were observed at or close to the natal den, with bite marks and wounds to the head or body, but we could not identify the group members that may have inflicted these wounds. In the remaining eight cases one or more adults were observed eating dead pups; in all cases these “pup eaters” included one or more dominant females. Evictions were defined as cases when adult individuals left their group for at least 1 d as a consequence of aggression from other group members (21). Individuals that were observed away from their group with no signs of aggression who did not return were recorded as having dispersed. Contraceptive Treatment. Experimental reproductive suppression in females was achieved using subcutaneous injection of synthetic progesterone (5 mg/kg medroxyprogesterone acetate; brand name Depo-provera) immediately after the birth of a communal litter (mean 5.33 ± 3.46 d after birth), and hence before postpartum estrus. Females were caught and anesthetized using the methods described in ref. 51. This procedure allowed us to successfully block reproduction for a single breeding attempt in 115 females (52 dominants and 63 subordinates) in 29 EXP breeding attempts (Exp. 1, n = 12 experiments in 8 groups conducted between 2006 and 2010; Exp. 2, n = 8 experiments in 6 groups conducted between 2006 and 2010; Exp. 3, n = 9 experiments in 5 groups conducted between 2008 and 2012). Adult females received an average of 1.8 treatments over the 7 y of study (range 1–5). By the time that pups in the EXP breeding attempts were born (10–11 wk postestrus) there was no significant difference between treated females (n = 5) and untreated females (n = 8) in progesterone [mean ± SE = 265.5 ± 123.3 ng/g (treated) and 124.9 ± 15.8 ng/g (untreated); t test: t 12 = −1.13, P = 0.32] or estrogen [median = 30.3, interquartile range 25.8–45.4 ng/g (treated) and median = 41.2, interquartile range 18.5–53.3 ng/g (untreated); Mann–Whitney U test: U = 18, P = 0.83] levels, as measured from fecal metabolites. For details of fecal sample collection and hormone analyses, see the SI Text. On average 50 (± 10%) of treated females conceived in the breeding attempt following the treatment litter, which did not differ significantly from the number of untreated females who conceived (57 ± 11%; GLMM: χ2 2 = 0.45, P = 0.50, controlling for a significant influence of dominance status; χ2 2 = 5.49, P = 0.019, n = 106 females in 17 experimental breeding attempts). Statistical Analysis. All statistical analyses were conducted in Genstat 14 (VSN International). To investigate the influence of the experimental treatment on female reproductive success, we used genetic analysis to determine the number of pups born to each female that survived to independence at 3 mo. Maternity was assigned with ≥95% confidence using a panel of 20 microsatellites following the methodology reported in ref. 52. Because female reproductive success was not normally distributed, we conducted a Friedman’s test to assess the effect of treatment (PRE, EXP, POST). Each experiment was assigned a unique identity number, which was included as a blocking factor to ensure experimental litters were compared with the appropriate control litters. To assess whether treatment influenced whether or not litters failed in the first week after birth, we fitted the probability of litter failure (1 = failed, 0 = survived) as the binomial response term in a GLMM. Litters were assumed to have failed if the group left no babysitters for more than 3 d (26). Group size (all group members >3 mo of age) and rainfall 60 d before birth (in millimeters) were fitted as covariates in all GLMMs and experimental number was included as a random term. To investigate whether the presence of older pups influences pup survival to 3 mo, we used a GLMM and fitted whether or not each pup survived as the binomial response term (1 = survived, 0 = died). Whether or not older pups were present in the group was fitted as the main term of interest and other factors likely to influence pup survival were included as fixed effects: group size, rainfall in the 3 mo after birth (in millimeters), pup sex, and litter size. Group and litter were fitted as random effects. This analysis was conducted on 160 pups from 121 litters in 11 groups. To investigate whether the presence of older pups influences pup weight at 3 mo, we weighed pups between 90 and 100 d of age by encouraging them to step onto an electronic weighing balance. The mean weight of 237 pups from 75 litters in 8 groups was fitted as the response term in a LMM, which included the same fixed effects and random terms as outlined above.

Acknowledgments We thank the Uganda Wildlife Authority for permission to conduct our research; the Wardens of Queen Elizabeth National Park for logistical support; Francis Mwanguhya, Solomon Kyabulima, Kenneth Mesigwe, Robert Businge, Corsin Müller, Neil Jordan, Bonnie Metherell, Roman Furrer, Jennifer Sanderson, and David Jansen for help in the field; Sue Walker and Rebecca Purcell at Chester Zoo Endocrinology Unit for help with hormonal analyses; and Nick Davies, Jeremy Field, Kevin Foster, Andy Young, and three anonymous referees for comments on the manuscript. This study was funded by the Natural Environment Research Council of the United Kingdom and The Royal Society.

Footnotes Author contributions: M.A.C. and S.J.H. designed research; M.A.C., H.J.N., and S.J.H. performed research; H.J.N. and S.J.H. analyzed data; M.A.C. and R.A.J. wrote the model; and M.A.C., R.A.J., and S.J.H. wrote the paper.

The authors declare no conflict of interest.

↵*This Direct Submission article had a prearranged editor.

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