Policing of reproduction by hidden threats in a cooperative mammal

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.

Explaining negative kin discrimination in a cooperative mammal society

“…We included mean pairwise relatedness to dominants in the group, which we defined as males and females over 3 y of age, as a fixed effect. We use this age criterion for social dominance throughout because, in both males and females, individuals over 3 y of age are more likely to breed, have higher fertility, and appear to be socially dominant (7,10,14,42). In males there is a clear agebased dominance hierarchy, evident during estrus (10,42).…”

“…In males there is a clear agebased dominance hierarchy, evident during estrus (10,42). In females, experimentally suppressing reproduction in older females (>3 y) results in failure of the communal litter, whereas suppressing reproduction in younger females (<3 y) does not (14). Older females also breed more frequently (7,11) and produce larger litters (43).…”

“…To test further whether negative kin discrimination depends on the capacity of recipients to resist, we examined kin discrimination in cases of infanticide of newborn pups. Between 1 and 12 females reproduce in each breeding attempt (14) and birth is highly synchronized, with pregnant females giving birth on exactly the same morning in 63% of cases (15). Experimental and observational evidence suggests that asynchronous litters are often killed by dominant females (14,15) and that in asynchronous litters the death of a litter in the first week after birth can be used as a proxy for infanticide (15,16).…”

“…Between 1 and 12 females reproduce in each breeding attempt (14) and birth is highly synchronized, with pregnant females giving birth on exactly the same morning in 63% of cases (15). Experimental and observational evidence suggests that asynchronous litters are often killed by dominant females (14,15) and that in asynchronous litters the death of a litter in the first week after birth can be used as a proxy for infanticide (15,16). In contrast to the pattern of negative kin discrimination in the eviction of adult females, there was no evidence of kin discrimination in cases of presumed infanticide (GLMM, β ± SE = −0.64 ± 2.00, χ 2 1 = 0.10, P = 0.75; Table S7).…”

Cheating and punishment in cooperative animal societies

“…'Policing' could also be a manifestation of reproductive competition among subordinates in both social insects [68,91,92] and vertebrates [30]. In the bumblebee Bombus terrestris, both queens and workers eat large numbers of worker-laid eggs, and when workers consume eggs they often have activated ovaries, though not always [92].…”