Jennifer L. Sanderson

Banded mongooses avoid inbreeding when mating with members of the same natal group.

Inbreeding and inbreeding avoidance are key factors in the evolution of animal societies, influencing dispersal and reproductive strategies which can affect relatedness structure and helping behaviours. In cooperative breeding systems, individuals typically avoid inbreeding through reproductive restraint and/or dispersing to breed outside their natal group. However, where groups contain multiple potential mates of varying relatedness, strategies of kin recognition and mate choice may be favoured. Here, we investigate male mate choice and female control of paternity in the banded mongoose (Mungos mungo), a cooperatively breeding mammal where both sexes are often philopatric and mating between relatives is known to occur. We find evidence suggestive of inbreeding depression in banded mongooses, indicating a benefit to avoiding breeding with relatives. Successfully breeding pairs were less related than expected under random mating, which appeared to be driven by both male choice and female control of paternity. Male banded mongooses actively guard females to gain access to mating opportunities, and this guarding behaviour is preferentially directed towards less closely related females. Guard–female relatedness did not affect the guards probability of gaining reproductive success. However, where mate‐guards are unsuccessful, they lose paternity to males that are less related to the females than themselves. Together, our results suggest that both sexes of banded mongoose use kin discrimination to avoid inbreeding. Although this strategy appears to be rare among cooperative breeders, it may be more prominent in species where relatedness to potential mates is variable, and/or where opportunities for dispersal and mating outside of the group are limited.

Adjustment of costly extra-group paternity according to inbreeding risk in a cooperative mammal

Lay Summary Female-banded mongooses risk their lives to mate with rivals during pack “warfare.” Data from wild banded mongooses reveal that 18% of pups are fathered by males from rival packs. These pups are less likely to be inbred are heavier and have higher survival chances than their within-pack counterparts. However, their mothers risk a lot to mate with extra-pack males; aggressive encounters between packs account for 20% of pup deaths and 12% of adult deaths.

Hormonal mediation of a carry-over effect in a wild cooperative mammal

Summary 1. Recent research has shown that parental investment in one breeding attempt often has a profound negative impact on the level of parental investment in subsequent breeding attempts. However, the mechanistic underpinnings that mediate such carry-over effects are poorly understood. 2. Here, we hypothesise that carry-over effects arise because energetic losses lead to elevated levels of glucocorticoid ‘stress’ hormones which inhibit future investment and thereby maintain energetic homeostasis. We investigate this hypothesis through a detailed investigation of a carry-over effect of (allo-) parental investment in the cooperatively breeding banded mongoose (Mungos mungo). 3. Using a combination of non-invasive hormone monitoring and feeding experiments, we demonstrate (i) that high glucocorticoid concentrations prior to breeding predict reduced alloparental investment; (ii) that energetic losses associated with high alloparental investment lead to an increase in glucocorticoid concentrations during the breeding attempt; and (iii) that elevated glucocorticoid concentrations persist into a time period that is known to affect future investment, although high pup mortality meant that we could not measure effects on subsequent alloparental investment directly. 4. Together, our results provide strong evidence for the hypothesis that carry-over effects on parental investment are mediated by circulating glucocorticoid concentrations. Since an individual’s stress physiology is shaped by early-life and social factors, our findings may help to explain how these factors contribute to individual variation in parental investment and lifetime reproductive success.

Reproductive competition triggers mass eviction in cooperative banded mongooses

In many vertebrate societies, forced eviction of group members is an important determinant of population structure, but little is known about what triggers eviction. Three main explanations are: (i) the reproductive competition hypothesis, (ii) the coercion of cooperation hypothesis, and (iii) the adaptive forced dispersal hypothesis. The last hypothesis proposes that dominant individuals use eviction as an adaptive strategy to propagate copies of their alleles through a highly structured population. We tested these hypotheses as explanations for eviction in cooperatively breeding banded mongooses (Mungos mungo), using a 16-year dataset on life history, behaviour and relatedness. In this species, groups of females, or mixed-sex groups, are periodically evicted en masse. Our evidence suggests that reproductive competition is the main ultimate trigger for eviction for both sexes. We find little evidence that mass eviction is used to coerce helping, or as a mechanism to force dispersal of relatives into the population. Eviction of females changes the landscape of reproductive competition for remaining males, which may explain why males are evicted alongside females. Our results show that the consequences of resolving within-group conflict resonate through groups and populations to affect population structure, with important implications for social evolution.

Explaining negative kin discrimination in a cooperative mammal society

Significance Kin selection theory predicts that animals will direct altruism toward closer genetic relatives and aggression toward more distantly related individuals. Our 18-y study of wild banded mongooses reveals that, unusually, dominant individuals target females who are more closely related to them for violent eviction from the group. This puzzling result can be explained by selection for unrelated individuals to resist eviction and for related individuals to submit more easily. In support of this idea, we show that kin are targeted for aggression only when individuals are capable of resisting. Our results suggest that, where potential victims can oppose aggression, the usual predictions of kin selection theory can be reversed. Kin selection theory predicts that, where kin discrimination is possible, animals should typically act more favorably toward closer genetic relatives and direct aggression toward less closely related individuals. Contrary to this prediction, we present data from an 18-y study of wild banded mongooses, Mungos mungo, showing that females that are more closely related to dominant individuals are specifically targeted for forcible eviction from the group, often suffering severe injury, and sometimes death, as a result. This pattern cannot be explained by inbreeding avoidance or as a response to more intense local competition among kin. Instead, we use game theory to show that such negative kin discrimination can be explained by selection for unrelated targets to invest more effort in resisting eviction. Consistent with our model, negative kin discrimination is restricted to eviction attempts of older females capable of resistance; dominants exhibit no kin discrimination when attempting to evict younger females, nor do they discriminate between more closely or less closely related young when carrying out infanticidal attacks on vulnerable infants who cannot defend themselves. We suggest that in contexts where recipients of selfish acts are capable of resistance, the usual prediction of positive kin discrimination can be reversed. Kin selection theory, as an explanation for social behavior, can benefit from much greater exploration of sequential social interactions.

Evidence of oxidative shielding of offspring in a wild mammal

Oxidative damage has been proposed as a potential mechanism underlying a life history tradeoff between survival and reproduction. However, evidence that reproduction is associated with increased oxidative damage is equivocal, and some studies have found that breeding females exhibit reduced, rather than elevated, levels of oxidative damage compared to equivalent non-breeders. Recently it was hypothesised that oxidative damage could have negative impacts on developing offspring, and that mothers might down-regulate oxidative damage during reproduction to shield their offspring from such damage. We tested this hypothesis through a longitudinal study of adult survival, reproduction, and oxidative damage in wild banded mongooses (Mungos mungo) in Uganda. High levels of oxidative damage as measured by malondialdehyde (MDA) were associated with reduced survival in both sexes. Levels of protein carbonyls were not linked to survival. Mothers showed reduced levels of MDA during pregnancy, and individuals with higher MDA levels gestated fewer offspring and had lower pup survival. These results suggest that maternal oxidative damage has transgenerational costs, and are consistent with the idea that mothers may attempt to shield their offspring from particularly harmful types of oxidative damage during pregnancy. Further advance in understanding of life history variation would benefit from theory and tests of the potential transgenerational impacts of the mechanisms underlying life history trade-offs.

Variable ecological conditions promote male helping by changing banded mongoose group composition

Lay Summary Male banded mongooses babysit more when rainfall is variable. Banded mongooses live in cooperative family groups and males in particular help raise pups that are not necessarily their own. It has been suggested that ecological conditions affect cooperation, and our study confirms that the variability of conditions is important: Females face higher mortality during years with more variable rainfall, and males may be better off helping their relatives when there are fewer opportunities for mating. Twitter: @HarryHMarshall

Female reproductive competition explains variation in prenatal investment in wild banded mongooses

Female intrasexual competition is intense in cooperatively breeding species where offspring compete locally for resources and helpers. In mammals, females have been proposed to adjust prenatal investment according to the intensity of competition in the postnatal environment (a form of ‘predictive adaptive response’; PAR). We carried out a test of this hypothesis using ultrasound scanning of wild female banded mongooses in Uganda. In this species multiple females give birth together to a communal litter, and all females breed regularly from one year old. Total prenatal investment (size times the number of fetuses) increased with the number of potential female breeders in the group. This relationship was driven by fetus size rather than number. The response to competition was particularly strong in low weight females and when ecological conditions were poor. Increased prenatal investment did not trade off against maternal survival. In fact we found the opposite relationship: females with greater levels of prenatal investment had elevated postnatal maternal survival. Our results support the hypothesis that mammalian prenatal development is responsive to the intensity of postnatal competition. Understanding whether these responses are adaptive requires information on the long-term consequences of prenatal investment for offspring fitness.

Junior scientists are sceptical of sceptics of open access: a reply to Agrawal.

Anurag A. Agrawal [1] recently published a letter in TIPS in which he suggested four points that researchers should consider when choosing to publish open access (OA). Although a critical evaluation of the pros and cons of publishing OA are warranted and important, three other points should also be considered when discussing OA.

Lifetime fitness consequences of early-life ecological hardship in a wild mammal population

Abstract Early‐life ecological conditions have major effects on survival and reproduction. Numerous studies in wild systems show fitness benefits of good quality early‐life ecological conditions (“silver‐spoon” effects). Recently, however, some studies have reported that poor‐quality early‐life ecological conditions are associated with later‐life fitness advantages and that the effect of early‐life conditions can be sex‐specific. Furthermore, few studies have investigated the effect of the variability of early‐life ecological conditions on later‐life fitness. Here, we test how the mean and variability of early‐life ecological conditions affect the longevity and reproduction of males and females using 14 years of data on wild banded mongooses (Mungos mungo). Males that experienced highly variable ecological conditions during development lived longer and had greater lifetime fitness, while those that experienced poor early‐life conditions lived longer but at a cost of reduced fertility. In females, there were no such effects. Our study suggests that exposure to more variable environments in early life can result in lifetime fitness benefits, whereas differences in the mean early‐life conditions experienced mediate a life‐history trade‐off between survival and reproduction. It also demonstrates how early‐life ecological conditions can produce different selection pressures on males and females.