A long post-reproductive lifespan is a shared trait among genetically distinct killer whale populations

The extended female post-reproductive lifespan found in humans and some toothed whales remains an evolutionary puzzle. Theory predicts demographic patterns resulting in increased female relatedness with age (kinship dynamics) can select for a prolonged post-reproductive lifespan due to the combined costs of inter-generational reproductive conflict and benefits of late-life helping. Here we test this prediction using >40 years of longitudinal demographic data from the sympatric yet genetically distinct killer whale ecotypes: resident and Bigg’s killer whales. The female relatedness with age is predicted to increase in both ecotypes, but with a less steep increase in Bigg’s due to their different social structure. Here, we show that there is a significant post-reproductive lifespan in both ecotypes with >30% of adult female years being lived as post-reproductive, supporting the general prediction that an increase in local relatedness with age predisposes the evolution of a post-reproductive lifespan. Differences in the magnitude of kinship dynamics however, did not influence the timing or duration of the post-reproductive lifespan with females in both ecotypes terminating reproduction before their mid-40s followed by an expected post-reproductive period of ~20 years. Our results highlight the important role of kinship dynamics in the evolution of a long post-reproductive lifespan in long-lived mammals, while further implying that the timing of menopause may be a robust trait that is persistent despite substantial variation in demographic patterns among population.

Asexual and sexual reproduction are two separate developmental pathways in a Termitomyces species

Although mutualistic symbioses per definition are beneficial for interacting species, conflict may arise if partners reproduce independently. We address how this reproductive conflict is regulated in the obligate mutualistic symbiosis between fungus-growing termites and Termitomyces fungi. Even though the termites and their fungal symbiont disperse independently to establish new colonies, dispersal is correlated in time. The fungal symbiont typically forms mushrooms a few weeks after the colony has produced dispersing alates. It is thought that this timing is due to a trade-off between alate and worker production; alate production reduces resources available for worker production. As workers consume the fungus, reduced numbers of workers will allow mushrooms to ‘escape’ from the host colony. Here, we test a specific version of this hypothesis: the typical asexual structures found in all species of Termitomyces —nodules—are immature stages of mushrooms that are normally harvested by the termites at a primordial stage. We refute this hypothesis by showing that nodules and mushroom primordia are macro- and microscopically different structures and by showing that in the absence of workers, primordia do, and nodules do not grow out into mushrooms. It remains to be tested whether termite control of primordia formation or of primordia outgrowth mitigates the reproductive conflict.

Power and punishment influence negotiations over parental care

Asymmetries in power (the ability to influence the outcome of conflict) are ubiquitous in social interactions because interacting individuals are rarely identical. It is well documented that asymmetries in power influence the outcome of reproductive conflict in social groups. Yet power asymmetries have received little attention in the context of negotiations between caring parents, which is surprising given that parents are often markedly different in size. Here we built on an existing negotiation model to examine how power and punishment influence negotiations over care. We incorporated power asymmetry by allowing the more-powerful parent, rank 1, to inflict punishment on the less-powerful parent, rank 2. We then determined when punishment will be favored by selection and how it would affect the negotiated behavioral response of each parent. We found that with power and punishment, a reduction in one parent’s effort results in partial compensation by the other parent. However, the degree of compensation is asymmetric: the rank 2 compensates more than the rank 1. As a result, the fitness of rank 1 increases and the fitness of rank 2 decreases, relative to the original negotiation model. Furthermore, because power and punishment enable one parent to extract greater effort from the other, offspring can do better, that is, receive more total effort, when there is power and punishment involved in negotiations over care. These results reveal how power and punishment alter the outcome of conflict between parents and affect offspring, providing insights into the evolutionary consequences of exerting power in negotiations.

Postreproductive killer whale grandmothers improve the survival of their grandoffspring

Understanding why females of some mammalian species cease ovulation prior to the end of life is a long-standing interdisciplinary and evolutionary challenge. In humans and some species of toothed whales, females can live for decades after stopping reproduction. This unusual life history trait is thought to have evolved, in part, due to the inclusive fitness benefits that postreproductive females gain by helping kin. In humans, grandmothers gain inclusive fitness benefits by increasing their number of surviving grandoffspring, referred to as the grandmother effect. Among toothed whales, the grandmother effect has not been rigorously tested. Here, we test for the grandmother effect in killer whales, by quantifying grandoffspring survival with living or recently deceased reproductive and postreproductive grandmothers, and show that postreproductive grandmothers provide significant survival benefits to their grandoffspring above that provided by reproductive grandmothers. This provides evidence of the grandmother effect in a nonhuman menopausal species. By stopping reproduction, grandmothers avoid reproductive conflict with their daughters, and offer increased benefits to their grandoffspring. The benefits postreproductive grandmothers provide to their grandoffspring are shown to be most important in difficult times where the salmon abundance is low to moderate. The postreproductive grandmother effect we report, together with the known costs of late-life reproduction in killer whales, can help explain the long postreproductive life spans of resident killer whales.

Spontaneous abortion as a response to reproductive conflict in the banded mongoose

When breeding females compete for limited resources, the intensity of this reproductive conflict can determine whether the fitness benefits of current reproductive effort exceed the potential costs to survival and future fertility. In group-living species, reproductive competition can occur through post-natal competition among the offspring of co-breeding females. Spontaneous abortion could be a response to such competition, allowing females to curtail reproductive expenditure on offspring that are unlikely to survive and to conserve resources for future breeding opportunities. We tested this hypothesis using long-term data on banded mongooses, Mungos mungo , in which multiple females within a group give birth synchronously to a communal litter that is cared for by other group members. As predicted, abortions were more likely during dry periods when food is scarce, and in breeding attempts with more intense reproductive competition. Within breeding events, younger, lighter females carrying smaller fetuses were more likely to abort, particularly those that were also of lower rank. Our results suggest that abortion may be a means by which disadvantaged females conserve resources for future breeding attempts in more benign conditions, and highlight that female reproductive competition may be resolved long before the production of offspring.

Reproductive conflict resolution in cooperative breeders

Female infanticide is common in animal societies where groups comprise multiple co-breeding females. To reduce the risk that their offspring are killed, mothers can synchronize breeding and pool offspring, making it hard for females to avoid killing their own young. However, female reproductive conflict does not invariably result in reproductive synchrony, and we lack a general hypothesis explaining the variation in conflict resolution strategies seen across species. Here, we investigate the fitness consequences of birth timing relative to other females and the prevalence of birth synchrony in cooperatively breeding Kalahari meerkats (Suricata suricatta). We show that, although there would be substantial benefits to females in synchronizing births and reducing their risk of infanticide, birth synchrony is rare. Since precise breeding synchrony has evolved in a related species with similar infanticidal female reproductive conflict, its absence in meerkats requires an evolutionary explanation. We therefore explore the costs and benefits of synchronizing breeding in two theoretical models, each of which contrasts synchrony with an alternative reproductive strategy: (i) breeding opportunistically and accepting fitness losses to infanticide or (ii) suppressing the reproduction of others to prevent infanticide. Our models show that the costs of synchrony constrain its development if subordinates breed infrequently, and that selection instead favors the suppression of subordinate reproduction by the dominant and opportunistic reproduction by subordinates. Together, our results suggest that the resolution of reproductive conflict in animal societies is shaped by differential breeding propensities among female group members, leading to divergent conflict resolution strategies even in closely related species.

Ovary activation does not correlate with pollen and nectar foraging specialization in the bumblebeeBombus impatiens

Social insect foragers may specialize on certain resource types. Specialization on pollen or nectar among honeybee foragers is hypothesized to result from associations between reproductive physiology and sensory tuning that evolved in ancestral solitary bees (the Reproductive Ground-Plan Hypothesis; RGPH). However, the two non-honeybee species studied showed no association between specialization and ovary activation. Here we investigate the bumblebeeB. impatiensbecause it has the most extensively studied pollen/nectar specialization of any bumblebee. We show that ovary size does not differ between pollen specialist, nectar specialist, and generalist foragers, contrary to the predictions of the RGPH. However, we also found mixed support for the second prediction of the RGPH, that sensory sensitivity, measured through proboscis extension response (PER), is greater among pollen foragers. We also found a correlation between foraging activity and ovary size, and foraging activity and relative nectar preference, but no correlation between ovary size and nectar preference. In one colony non-foragers had larger ovaries than foragers, supporting the reproductive conflict and work hypothesis, but in the other colony they did not.

Discrete but variable structure of animal societies leads to the false perception of a social continuum

Animal societies are typically divided into those in which reproduction within a group is monopolized by a single female versus those in which it is shared among multiple females. It remains controversial, however, whether these two forms of social structure represent distinct evolutionary outcomes or endpoints along a continuum of reproductive options. To address this issue and to determine whether vertebrates and insects exhibit the same patterns of variation in social structure, we examined the demographic and reproductive structures of 293 species of wasps, ants, birds and mammals. Using phylogenetically informed comparative analyses, we found strong evidence indicating that not all reproductive arrangements within social groups are viable in nature and that in societies with multiple reproductives, selection favours instead taxon-specific patterns of decrease in the proportion of breeders as a function of group size. These outcomes suggest that the selective routes to sociality differ depending upon whether monopolization of reproduction by one individual is possible and that variation within and among taxonomic groups may lead to the false perception of a continuum of social structures. Thus, the occurrence of very large societies may require either complete reproductive monopolization (monogyny/singular breeding) or the maintenance of a taxon-specific range of values for the proportional decrease in the number of breeders within a group (polygyny/plural breeding), both of which may reduce reproductive conflict among females.