Social monogamy and the threat of infanticide in larger mammals

Primates, 2008

Owl monkeys (Aotus azarai) are small, territorial, socially monogamous primates that show intense infant care by the adult male in the group. It has been hypothesized that male care may be adaptive because it increases offspring survival and/or reduces the metabolic costs to the female of raising the offspring. Alternatively, males may provide care even when they are not related to the infants to increase future reproductive opportunities. We describe changes in infant care patterns that took place following the eviction of the resident male by a solitary male in an owl monkey population in the Argentinean Chaco. The resident male and mother provided all infant care during the first month of life of the infant, until the male was evicted. During the 3-day male replacement event, care of the infant was shared among the mother, a 4year-old sister, and a 1-year-old brother. The new male began contributing to infant care soon after entering the group, carrying, and interacting socially with the infant in much the same way as any male regularly does. However, despite receiving biparental care from both the original and new resident males, the infant disappeared at the age of four months and was presumed dead. These are the first reports of care by sibling and by non-putative fathers in wild owl monkeys. Given the significant amount time that new pairs of owl monkeys spend before reproducing, it is possible that male care in owl monkeys functions as mating effort as much as or more than parenting effort.

Male reproductive cooperation is rare in nature: expectations from evolutionary theory suggest that males should be competitors for reproductive opportunities and provide little parental care. Counter to this expectation, in cooperatively polyandrous mating systems, multiple adult males mate with a single breeding female and subsequently cooperate to rear her young. This raises the question of the fitness benefits of parental care, as males may be providing care to offspring that are not their own. Here, I use genetic and demographic data from a multiyear field study of Geoffroy’s tamarin, Saguinus geoffroyi, to test predictions of the indirect and direct fitness benefits hypotheses. I found that polyandrous males within a group were related at levels consistent with filial or fraternal relationships (r = 0.36–0.44) and could also share paternity (40% of groups had >2 male sires). Sharing of paternity occurred both within litters and over multiyear associations that remained stable throughout the study period of 2–3 years. However, remaining groups had a single sire, perhaps owing to the ability of males to prevail in sperm competition. These results suggest the joint role of indirect and direct fitness benefits in male–male cooperation in tamarins, in contrast to other cooperatively polyandrous species. The high average relatedness of polyandrous males may be consistent with fraternal cooperative polyandry in this species, as observed in certain human societies, providing a novel example that should enhance comparative studies of the evolution of male–male cooperation in reproduction.

Royal Anthropological Institute - Occasional Paper - Dunbar's Number, 2019

There has been a long history of attempts to explain the evolution of monogamy in mammals in general (Kleiman 1977), and primates in particular (Alexander 1979), partly because of the implications that it may have for the evolution of monogamy in humans. Monogamy is a complex term though, with some species invariably found in pairs (such as owl monkeys), whereas other species can be monogamous, but flexibly take up other mating systems (such as callitrichid monkeys). Humans fit with the latter flexible group, as well as having the additional distinction between their mating system and their marriage system. However, it is fairly well established that monogamy is common in birds (90% of species) (Lack 1968) due to the short time period between mating and egg laying that allows a male to increase his reproductive success through sharing high levels of offspring care (incubating, hatching and rearing), rather than leaving the female he has just mated with to look for other females with whom to mate. The particular reproductive strategy of mammals, with a long gestation period followed by lactation, reduces the opportunities for a male to provide direct care for his offspring, therefore most males move on after mating to seek other fertile females. As a result, monogamy is rare among mammals (5% of species) (Lukas and Clutton-Brock 2013). It is surprising, then, that monogamy is unusually prevalent in one particular mammal order, namely the primates (where 30% of species are monogamous) (Opie, et al. 2013a), with monogamy occurring in all the major primate families (Opie, et al. 2012).

American Journal of Physical Anthropology, 2005

Proceedings of the National Academy of Sciences of the United States of America, 2017

Most mammals live in social groups in which members form differentiated social relationships. Individuals may vary in their degree of sociality, and this variation can be associated with differential fitness. In some species, for example, female sociality has a positive effect on infant survival. However, investigations of such cases are still rare, and no previous study has considered how male infanticide might constrain effects of female sociality on infant survival. Infanticide is part of the male reproductive strategy in many mammals, and it has the potential to override, or even reverse, effects of female reproductive strategies, including sociality. Therefore, we investigated the relationships between female sociality, offspring survival, and infanticide risk in wild white-faced capuchin monkeys using long-term data from Santa Rosa, Costa Rica. Female capuchins formed differentiated bonds, and bond strength was predicted by kin relationship, rank difference, and the presence o...

Mating Strategies and Partnerships in Birds, Humans and Other Mammals, 2003

Proceedings of the Royal Society B: Biological Sciences, 2000

Paternal behaviour presumably evolved because male care of young was critical for o¡spring survival. We report ¢eld evidence indicating that paternal behaviour enhances o¡spring survival in a monogamous mammal, the biparental California mouse, Peromyscus californicus. Male removal resulted in lower o¡spring survival in father-absent than in father-present families. New males took up residence with widowed females, but usually after females had stopped lactating, suggesting that the importance of the father is not primarily protection against infanticidal intruders but rather direct care of young.

Infanticide by males has been hypothesized to be a naturally selected behavioral strategy that increases the infanticidal male's reproductive success. The sexual selection hypothesis has been challenged via alternative, nonadaptive hypotheses that dispute its empirical and theoretical bases. Two of the most widely recognized alternatives are the social pathology hypothesis, in which infanticide results from overcrowding or recent human disturbance, and the generalized aggression hypothesis, in which infanticide is an epiphenomenon of increased male aggression. We report the first case of infanticide in wild, seasonally breeding patas monkeys (Erythrocebus patas) living at a low population density in a stable habitat, conditions which do not support the social pathology hypothesis. Its exceptional occurrence is consistent with the sexual selection hypothesis: over a 7-year period the infanticidal male was the only one of 13 resident males that was not present during the actual conception season but was present during the following birth season. Also consistent with this hypothesis, mothers were differentially targeted for male aggression, which increased sevenfold during the days surrounding the infanticide and then decreased to baseline levels after the infanticide. Aggression targeted at mothers does not support the generalized aggression hypothesis. As predicted by the sexual selection hypothesis, females began soliciting mating immediately after the infanticide, despite its occurrence in the nonconceptive season.

Animal Behaviour, 2010

PLoS ONE, 2013

Infanticide can be a major influence upon the social structure of species in which females maintain long-term associations with males. Previous studies have suggested that female mountain gorillas benefit from residing in multimale groups because infanticide occurs when one-male groups disintegrate after the dominant male dies. Here we measure the impact of infanticide on the reproductive success of female mountain gorillas, and we examine whether their dispersal patterns reflect a strategy to avoid infanticide. Using more than 40 years of data from up to 70% of the entire population, we found that only 1.7% of the infants that were born in the study had died from infanticide during group disintegrations. The rarity of such infanticide mainly reflects a low mortality rate of dominant males in one-male groups, and it does not dispel previous observations that infanticide occurs during group disintegrations. After including infanticide from causes other than group disintegrations, infanticide victims represented up to 5.5% of the offspring born during the study, and they accounted for up to 21% of infant mortality. The overall rates of infanticide were 2-3 times higher in one-male groups than multimale groups, but those differences were not statistically significant. Infant mortality, the length of interbirth intervals, and the age of first reproduction were not significantly different between one-male versus multimale groups, so we found no significant fitness benefits for females to prefer multimale groups. In addition, we found limited evidence that female dispersal patterns reflect a preference for multimale groups. If the strength of selection is modest for females to avoid group disintegrations, than any preference for multimale groups may be slow to evolve. Alternatively, variability in male strength might give some one-male groups a lower infanticide risk than some multimale groups, which could explain why both types of groups remain common.

Frontiers in Ecology and Evolution, 2018

Background: We still do not understand the key drivers or prevalence of genetic monogamy in mammals despite the amount of attention that the evolution of mammalian monogamy has received. There have been numerous reviews of the hypotheses proposed to explain monogamy, some of which focused on animals in general, while others focused on particular classes like birds or mammals, or on specific orders within a class. Because monogamy is rare in mammals overall but relatively common in some of the orders in which it has been observed (e.g., Primates, Macroscelidea, and Carnivora), mammals provide a unique taxon in which to study the evolution and maintenance of monogamy However, the term "monogamy" encompasses related but separate phenomena; i.e., social monogamy (pair-living by opposite-sex conspecifics) and genetic monogamy or reproductive monogamy (mating exclusivity). A recent review of mammalian monogamy reported that 226 species (9%) in 9 orders (35%) were socially monogamous, although socially monogamous mammals are not necessarily genetically monogamous. Methods: Since factors that predispose socially monogamous mammals to be genetically monogamous are still subject to debate, we conducted meta-analyses using model selection to determine the relative importance of several life history, demographic, and environmental factors in predicting genetic monogamy. Results: We found sufficient data to include 41 species in our analysis, about 2x more than have been included in previous analyses of mammalian genetic monogamy. We found that living as part of a socially monogamous pair vs. in a group was the best predictor of genetic monogamy, either by itself or in combination with high levels of paternal care. A male-biased sex ratio and low population density were inversely related to the number of pairs that were genetically monogamous, but not to the production of intra-pair young or litters. Conclusion: Our results agree with the results of some previous analyses but suggest that more than one factor may be important in driving genetic monogamy in mammals.

PLoS ONE, 2012

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.

Behavioral Ecology and Sociobiology, 2014

Fundamental reproductive interests dictate that females generally benefit most from mate selectivity and males from mate quantity. This can create conflict between the sexes and result in sexual coercion: male use of aggression to garner mating success at a cost to females. Potential fitness costs of sexual coercion, however, can be difficult to measure. Here we demonstrate benefits to males and costs to females of female defense polygyny in wild hamadryas baboons, cercopithecoid primates in which females are coercively transferred among social units by males, restricting both female choice and bonding among female kin. Of all coercive transfers (takeovers) of females with young infants, 67% were followed by infant mortality, which was significantly more likely to occur after takeovers than at other times. As expected, infant mortality decreased time to subsequent conception but lengthened intervals between surviving infants. Following infant survival, whether a female had experienced a takeover after the previous birth was a significant predictor of subsequent interbirth interval, with interbirth intervals of females remaining with the same male between births being significantly shorter than those of females incurring takeovers between births. Together these results reveal that takeovers increase the chance of infant mortality while delaying subsequent conception. Male-driven female defense polygyny in this species is thus costly to females in two ways. These results demonstrate that reproductive strategies benefitting males can evolve despite substantial costs to females. These costs may be mitigated over the long term, however, by female counterstrategies and protective behavior by males.

Frontiers in Ecology and Evolution, 2022

Explanations for the evolution of social monogamy in mammals typically emphasise one of two possibilities: females are overdispersed (such that males cannot defend access to more than one female at a time) or males provide a service to the female. However, the first claim has never been formally tested. I test it directly at three levels using populationlevel data from primates and ungulates. First, I show that the females of monogamous genera do not have territories that are significantly larger, either absolutely or relatively, than those of polygynous genera. Second, using two indices of territorial defendability, I show that, given their typical day journey lengths, males of most monogamous species could easily defend an area large enough to allow them to monopolise as many as 5-10 females if they ranged solitarily. Finally, I use a model of male mate searching strategies to show that the opportunity cost incurred by pairbonded males is typically 5-10 times the reproductive success they actually obtain by being obligately monogamous. This suggests that the selection pressure dissuading them from pursuing a roving male strategy must be very considerable. At present, the evidence is undecided as to whether mitigating predation or infanticide risk is the primary function, but estimates of their impacts suggest that both are in fact plausible.

Evolution, 1980