Optimal foraging.

Before visiting your local supermarket, do you write your food shopping list in the order you expect to encounter the items as you walk around, aisle by aisle? This way, you minimise your travel distance, saving time and effort. Many other animals do the same. Baboons (Papio ursinus) plan their foraging journeys to out-of-sight resources, moving in an efficient, goal-directed way, and nectar-collecting bumble bees (Bombus impatiens) use efficient travel routes when foraging on familiar resources.

Untangling the oxidative cost of reproduction: An analysis in wild banded mongooses.

The cost of reproduction plays a central role in evolutionary theory, but the identity of the underlying mechanisms remains a puzzle. Oxidative stress has been hypothesized to be a proximate mechanism that may explain the cost of reproduction. We examine three pathways by which oxidative stress could shape reproduction. The "oxidative cost" hypothesis proposes that reproductive effort generates oxidative stress, while the "oxidative constraint" and "oxidative shielding" hypotheses suggest that mothers mitigate such costs through reducing reproductive effort or by pre-emptively decreasing damage levels, respectively. We tested these three mechanisms using data from a long-term food provisioning experiment on wild female banded mongooses (Mungos mungo). Our results show that maternal supplementation did not influence oxidative stress levels, or the production and survival of offspring. However, we found that two of the oxidative mechanisms co-occur during reproduction. There was evidence of an oxidative challenge associated with reproduction that mothers attempted to mitigate by reducing damage levels during breeding. This mitigation is likely to be of crucial importance, as long-term offspring survival was negatively impacted by maternal oxidative stress. This study demonstrates the value of longitudinal studies of wild animals in order to highlight the interconnected oxidative mechanisms that shape the cost of reproduction.

A double pedigree reveals genetic but not cultural inheritance of cooperative personalities in wild banded mongooses.

Personality traits, such as the propensity to cooperate, are often inherited from parents to offspring, but the pathway of inheritance is unclear. Traits could be inherited via genetic or parental effects, or culturally via social learning from role models. However, these pathways are difficult to disentangle in natural systems as parents are usually the source of all of these effects. Here, we exploit natural 'cross fostering' in wild banded mongooses to investigate the inheritance of cooperative behaviour. Our analysis of 800 adult helpers over 21 years showed low but significant genetic heritability of cooperative personalities in males but not females. Cross fostering revealed little evidence of cultural heritability: offspring reared by particularly cooperative helpers did not become more cooperative themselves. Our results demonstrate that cooperative personalities are not always highly heritable in wild, and that the basis of behavioural traits can vary within a species (here, by sex).

Rhesus macaques build new social connections after a natural disaster.

Climate change is increasing the frequency and intensity of weather-related disasters such as hurricanes, wildfires, floods, and droughts. Understanding resilience and vulnerability to these intense stressors and their aftermath could reveal adaptations to extreme environmental change. In 2017, Puerto Rico suffered its worst natural disaster, Hurricane Maria, which left 3,000 dead and provoked a mental health crisis. Cayo Santiago island, home to a population of rhesus macaques (Macaca mulatta), was devastated by the same storm. We compared social networks of two groups of macaques before and after the hurricane and found an increase in affiliative social connections, driven largely by monkeys most socially isolated before Hurricane Maria. Further analysis revealed monkeys invested in building new relationships rather than strengthening existing ones. Social adaptations to environmental instability might predispose rhesus macaques to success in rapidly changing anthropogenic environments.

Developmental transitions in body color in chacma baboon infants: Implications to estimate age and developmental pace.

OBJECTIVES: In many primates, one of the most noticeable morphological developmental traits is the transition from natal fur and skin color to adult coloration. Studying the chronology and average age at such color transitions can be an easy and noninvasive method to (a) estimate the age of infants whose dates of birth were not observed, and (b) detect interindividual differences in the pace of development for infants with known birth dates. MATERIALS AND METHODS: Using a combination of photographs and field observations from 73 infant chacma baboons (Papio ursinus) of known ages, we (a) scored the skin color of six different body parts from pink to gray, as well as the color of the fur from black to gray; (b) validated our method of age estimation using photographic and field observations on an independent subset of 22 infants with known date of birth; and (c) investigated ecological, social, and individual determinants of age-related variation in skin and fur color. RESULTS: Our results show that transitions in skin color can be used to age infant chacma baboons less than 7 months old with accuracy (median number of days between actual and estimated age = 10, range = 0-86). We also reveal that food availability during the mother's pregnancy, but not during lactation, affects infant color-for-age and therefore acts as a predictor of developmental pace. DISCUSSION: This study highlights the potential of monitoring within- and between-infant variation in color to estimate age when age is unknown, and developmental pace when age is known.

Ecology of domestic dogs (Canis familiaris) as a host for Guinea worm (Dracunculus medinensis) infection in Ethiopia.

The global programme for the eradication of Guinea worm disease, caused by the parasitic nematode Dracunculus medinensis, has been successful in driving down human cases, but infections in non-human animals, particularly domestic dogs (Canis familiaris), now present a major obstacle to further progress. Dog infections have mainly been found in Chad and, to a lesser extent, in Mali and Ethiopia. While humans classically acquire infection by drinking water containing infected copepods, it has been hypothesized that dogs might additionally or alternatively acquire infection via a novel pathway, such as consumption of fish or frogs as possible transport or paratenic hosts. We characterized the ecology of free-ranging dogs living in three villages in Gog woreda, Gambella region, Ethiopia, in April-May 2018. We analysed their exposure to potential sources of Guinea worm infection and investigated risk factors associated with infection histories. The home ranges of 125 dogs and their activity around water sources were described using GPS tracking, and the diets of 119 dogs were described using stable isotope analysis. Unlike in Chad, where Guinea worm infection is most frequent, we found no ecological or behavioural correlates of infection history in dogs in Ethiopia. Unlike in Chad, there was no effect of variation among dogs in their consumption of aquatic vertebrates (fish or frogs) on their infection history, and we found no evidence to support hypotheses for this novel transmission pathway in Ethiopia. Dog owners had apparently increased the frequency of clean water provision to dogs in response to previous infections. Variations in dog ranging behaviour, owner behaviour and the characteristics of natural water bodies all influenced the exposure of dogs to potential sources of infection. This initial study suggests that the classical transmission pathway should be a focus of attention for Guinea worm control in non-human animals in Ethiopia.

Stable isotopes are quantitative indicators of trophic niche.

Hette-Tronquart (2019, Ecol. Lett.) raises three concerns about our interpretation of stable isotope data in Sheppard et al. (2018, Ecol. Lett., 21, 665). We feel that these concerns are based on comparisons that are unreasonable or ignore the ecological context from which the data were collected. Stable isotope ratios provide a quantitative indication of, rather than being exactly equivalent to, trophic niche.

Live long and prosper: durable benefits of early-life care in banded mongooses.

Kin selection theory defines the conditions for which altruism or 'helping' can be favoured by natural selection. Tests of this theory in cooperatively breeding animals have focused on the short-term benefits to the recipients of help, such as improved growth or survival to adulthood. However, research on early-life effects suggests that there may be more durable, lifelong fitness impacts to the recipients of help, which in theory should strengthen selection for helping. Here, we show in cooperatively breeding banded mongooses ( Mungos mungo) that care received in the first 3 months of life has lifelong fitness benefits for both male and female recipients. In this species, adult helpers called 'escorts' form exclusive one-to-one caring relationships with specific pups (not their own offspring), allowing us to isolate the effects of being escorted on later reproduction and survival. Pups that were more closely escorted were heavier at sexual maturity, which was associated with higher lifetime reproductive success for both sexes. Moreover, for female offspring, lifetime reproductive success increased with the level of escorting received per se, over and above any effect on body mass. Our results suggest that early-life social care has durable benefits to offspring of both sexes in this species. Given the well-established developmental effects of early-life care in laboratory animals and humans, we suggest that similar effects are likely to be widespread in social animals more generally. We discuss some of the implications of durable fitness benefits for the evolution of intergenerational helping in cooperative animal societies, including humans. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

Developing differences: early-life effects and evolutionary medicine.

Variation in early-life conditions can trigger developmental switches that lead to predictable individual differences in adult behaviour and physiology. Despite evidence for such early-life effects being widespread both in humans and throughout the animal kingdom, the evolutionary causes and consequences of this developmental plasticity remain unclear. The current issue aims to bring together studies of early-life effects from the fields of both evolutionary ecology and biomedicine to synthesise and advance current knowledge of how information is used during development, the mechanisms involved, and how early-life effects evolved. We hope this will stimulate further research into early-life effects, improving our understanding of why individuals differ and how this might influence their susceptibility to disease. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

Decoupling of Genetic and Cultural Inheritance in a Wild Mammal.

Cultural inheritance, the transmission of socially learned information across generations, is a non-genetic, "second inheritance system" capable of shaping phenotypic variation in humans and many non-human animals [1-3]. Studies of wild animals show that conformity [4, 5] and biases toward copying particular individuals [6, 7] can result in the rapid spread of culturally transmitted behavioral traits and a consequent increase in behavioral homogeneity within groups and populations [8, 9]. These findings support classic models of cultural evolution [10, 11], which predict that many-to-one or one-to-many transmission erodes within-group variance in culturally inherited traits. However, classic theory [10, 11] also predicts that within-group heterogeneity is preserved when offspring each learn from an exclusive role model. We tested this prediction in a wild mammal, the banded mongoose (Mungos mungo), in which offspring are reared by specific adult carers that are not their parents, providing an opportunity to disentangle genetic and cultural inheritance of behavior. We show using stable isotope analysis that young mongooses inherit their adult foraging niche from cultural role models, not from their genetic parents. As predicted by theory, one-to-one cultural transmission prevented blending inheritance and allowed the stable coexistence of distinct behavioral traditions within the same social groups. Our results confirm that cultural inheritance via role models can promote rather than erode behavioral heterogeneity in natural populations.

Intragroup competition predicts individual foraging specialisation in a group-living mammal.

Individual foraging specialisation has important ecological implications, but its causes in group-living species are unclear. One of the major consequences of group living is increased intragroup competition for resources. Foraging theory predicts that with increased competition, individuals should add new prey items to their diet, widening their foraging niche ('optimal foraging hypothesis'). However, classic competition theory suggests the opposite: that increased competition leads to niche partitioning and greater individual foraging specialisation ('niche partitioning hypothesis'). We tested these opposing predictions in wild, group-living banded mongooses (Mungos mungo), using stable isotope analysis of banded mongoose whiskers to quantify individual and group foraging niche. Individual foraging niche size declined with increasing group size, despite all groups having a similar overall niche size. Our findings support the prediction that competition promotes niche partitioning within social groups and suggest that individual foraging specialisation may play an important role in the formation of stable social groupings.

Data collection and storage in long-term ecological and evolutionary studies: The Mongoose 2000 system.

Studying ecological and evolutionary processes in the natural world often requires research projects to follow multiple individuals in the wild over many years. These projects have provided significant advances but may also be hampered by needing to accurately and efficiently collect and store multiple streams of the data from multiple individuals concurrently. The increase in the availability and sophistication of portable computers (smartphones and tablets) and the applications that run on them has the potential to address many of these data collection and storage issues. In this paper we describe the challenges faced by one such long-term, individual-based research project: the Banded Mongoose Research Project in Uganda. We describe a system we have developed called Mongoose 2000 that utilises the potential of apps and portable computers to meet these challenges. We discuss the benefits and limitations of employing such a system in a long-term research project. The app and source code for the Mongoose 2000 system are freely available and we detail how it might be used to aid data collection and storage in other long-term individual-based projects.

Telomere dynamics in wild banded mongooses: Evaluating longitudinal and quasi-longitudinal markers of senescence.

Telomere length and the rate of telomere shortening have been suggested as particularly useful physiological biomarkers of the processes involved in senescent decline of somatic and reproductive function. However, longitudinal data on changes in telomere length across the lifespan are difficult to obtain, particularly for long-lived animals. Quasi-longitudinal studies have been proposed as a method to gain insight into telomere dynamics in long-lived species. In this method, minimally replicative cells are used as the baseline telomere length against which telomere length in highly replicative cells (which represent the current state) can be compared. Here we test the assumptions and predictions of the quasi-longitudinal approach using longitudinal telomere data in a wild cooperative mammal, the banded mongoose, Mungos mungo. Contrary to our prediction, telomere length (TL) was longer in leukocytes than in ear cartilage. Longitudinally, the TL of ear cartilage shortened with age, but there was no change in the TL of leukocytes, and we also observed many individuals in which TL increased rather than decreased with age. Leukocyte TL but not cartilage TL was a predictor of total lifespan, while neither predicted post-sampling survival. Our data do not support the hypothesis that cross-tissue comparison in TL can act as a quasi-longitudinal marker of senescence. Rather, our results suggest that telomere dynamics in banded mongooses are more complex than is typically assumed, and that longitudinal studies across whole life spans are required to elucidate the link between telomere dynamics and senescence in natural populations.

Biased escorts: offspring sex, not relatedness explains alloparental care patterns in a cooperative breeder.

Kin selection theory predicts that animals should direct costly care where inclusive fitness gains are highest. Individuals may achieve this by directing care at closer relatives, yet evidence for such discrimination in vertebrates is equivocal. We investigated patterns of cooperative care in banded mongooses, where communal litters are raised by adult 'escorts' who form exclusive caring relationships with individual pups. We found no evidence that escorts and pups assort by parentage or relatedness. However, the time males spent escorting increased with increasing relatedness to the other group members, and to the pup they had paired with. Thus, we found no effect of relatedness in partner choice, but (in males) increasing helping effort with relatedness once partner choices had been made. Unexpectedly, the results showed clear assortment by sex, with female carers being more likely to tend to female pups, and male carers to male pups. This sex-specific assortment in helping behaviour has potential lifelong impacts on individual development and may impact the future size and composition of natal groups and dispersing cohorts. Where relatedness between helpers and recipients is already high, individuals may be better off choosing partners using other predictors of the costs and benefits of cooperation, without the need for possibly costly within-group kin discrimination.

Explaining negative kin discrimination in a cooperative mammal society.

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.

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

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.

Lack of aggression and apparent altruism towards intruders in a primitive termite.

In eusocial insects, the ability to discriminate nest-mates from non-nest-mates is widespread and ensures that altruistic actions are directed towards kin and agonistic actions are directed towards non-relatives. Most tests of nest-mate recognition have focused on hymenopterans, and suggest that cooperation typically evolves in tandem with strong antagonism towards non-nest-mates. Here, we present evidence from a phylogenetically and behaviourally basal termite species that workers discriminate members of foreign colonies. However, contrary to our expectations, foreign intruders were the recipients of more rather than less cooperative behaviour and were not subjected to elevated aggression. We suggest that relationships between groups may be much more peaceable in basal termites compared with eusocial hymenoptera, owing to energetic and temporal constraints on colony growth, and the reduced incentive that totipotent workers (who may inherit breeding status) have to contribute to self-sacrificial intergroup conflict.

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

Ecological conditions are expected to have an important influence on individuals' investment in cooperative care. However, the nature of their effects is unclear: both favorable and unfavorable conditions have been found to promote helping behavior. Recent studies provide a possible explanation for these conflicting results by suggesting that increased ecological variability, rather than changes in mean conditions, promote cooperative care. However, no study has tested whether increased ecological variability promotes individual-level helping behavior or the mechanisms involved. We test this hypothesis in a long-term study population of the cooperatively breeding banded mongoose, Mungos mungo, using 14 years of behavioral and meteorological data to explore how the mean and variability of ecological conditions influence individual behavior, body condition, and survival. Female body condition was more sensitive to changes in rainfall leading to poorer female survival and pronounced male-biased group compositions after periods of high rainfall variability. After such periods, older males invested more in helping behavior, potentially because they had fewer mating opportunities. These results provide the first empirical evidence for increased individual helping effort in more variable ecological conditions and suggest this arises because of individual differences in the effect of ecological conditions on body condition and survival, and the knock-on effect on social group composition. Individual differences in sensitivity to environmental variability, and the impacts this has on the internal structure and composition of animal groups, can exert a strong influence on the evolution and maintenance of social behaviors, such as cooperative care.

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.

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.