Sinead English

Weak evidence for anticipatory parental effects in plants and animals

The evolution of adaptive phenotypic plasticity relies on the presence of cues that enable organisms to adjust their phenotype to match local conditions. Although mostly studied with respect to nonsocial cues, it is also possible that parents transmit information about the environment to their offspring. Such ‘anticipatory parental effects’ or ‘adaptive transgenerational plasticity’ can have important consequences for the dynamics and adaptive potential of populations in heterogeneous environments. Yet, it remains unknown how widespread this form of plasticity is. Using a meta‐analysis of experimental studies with a fully factorial design, we show that there is only weak evidence for higher offspring performance when parental and offspring environments are matched compared with when they are mismatched. Estimates of heterogeneity among studies suggest that effects, when they occur, are subtle. Study features, environmental context, life stage and trait categories all failed to explain significant amounts of variation in effect sizes. We discuss theoretical and methodological reasons for the limited evidence for anticipatory parental effects and suggest ways to improve our understanding of the prevalence of this form of plasticity in nature.

Inbreeding and inbreeding depression of early life traits in a cooperative mammal.

Mating between relatives often results in negative fitness consequences or inbreeding depression. However, the expression of inbreeding in populations of wild cooperative mammals and the effects of environmental, maternal and social factors on inbreeding depression in these systems are currently not well understood. This study uses pedigree‐based inbreeding coefficients from a long‐term study of meerkats (Suricata suricatta) in South Africa to reveal that 44% of the population have detectably non‐zero (F > 0) inbreeding coefficients. 15% of these inbred individuals were the result of moderate inbreeding (F ≥ 0.125), although such inbreeding events almost solely occurred when mating individuals had no prior experience of each other. Inbreeding depression was evident for a range of traits: pup mass at emergence from the natal burrow, hind‐foot length, growth until independence and juvenile survival. However, we found no evidence of significant inbreeding depression for skull and forearm length or for pup survival. This research provides a rare investigation into inbreeding in a cooperative mammal, revealing high levels of inbreeding, considerable negative consequences and complex interactions with the social environment.

Consistent individual differences in cooperative behaviour in meerkats (Suricata suricatta).

Although recent models for the evolution of personality, using game theory and life‐history theory, predict that individuals should differ consistently in their cooperative behaviour, consistent individual differences in cooperative behaviour have rarely been documented. In this study, we used a long‐term data set on wild meerkats to quantify the repeatability of two types of cooperative care (babysitting and provisioning) within individuals and examined how repeatability varied across age, sex and status categories. Contributions to babysitting and provisioning were significantly repeatable and positively correlated within individuals, with provisioning more repeatable than babysitting. While repeatability of provisioning was relatively invariant across categories of individuals, repeatability of babysitting increased with age and was higher for subordinates than dominants. These results provide support for theoretical predictions that life‐history trade‐offs favour the evolution of consistent individual differences in cooperative behaviour and raise questions about why some individuals consistently help more than others across a suite of cooperative behaviours.

Escalated conflict in a social hierarchy

Animals that live in cooperative societies form hierarchies in which dominant individuals reap disproportionate benefits from group cooperation. The stability of these societies requires subordinates to accept their inferior status rather than engage in escalated conflict with dominants over rank. Applying the logic of animal contests to these cases predicts that escalated conflict is more likely where subordinates are reproductively suppressed, where group productivity is high, relatedness is low, and where subordinates are relatively strong. We tested these four predictions in the field on co-foundress associations of the paper wasp Polistes dominulus by inducing contests over dominance rank experimentally. Subordinates with lower levels of ovarian development, and those in larger, more productive groups, were more likely to escalate in conflict with their dominant, as predicted. Neither genetic relatedness nor relative body size had significant effects on the probability of escalation. The original dominant emerged as the winner in all except one escalated contest. The results provide the first evidence that reproductive suppression of subordinates increases the threat of escalated conflict, and hence that reproductive sharing can promote stability of the dominant–subordinate relationship.

The information value of non-genetic inheritance in plants and animals

Parents influence the development of their offspring in many ways beyond the transmission of DNA. This includes transfer of epigenetic states, nutrients, antibodies and hormones, and behavioural interactions after birth. While the evolutionary consequences of such non-genetic inheritance are increasingly well understood, less is known about how inheritance mechanisms evolve. Here, we present a simple but versatile model to explore the adaptive evolution of non-genetic inheritance. Our model is based on a switch mechanism that produces alternative phenotypes in response to different inputs, including genes and non-genetic factors transmitted from parents and the environment experienced during development. This framework shows how genetic and non-genetic inheritance mechanisms and environmental conditions can act as cues by carrying correlational information about future selective conditions. Differential use of these cues is manifested as different degrees of genetic, parental or environmental morph determination. We use this framework to evaluate the conditions favouring non-genetic inheritance, as opposed to genetic determination of phenotype or within-generation plasticity, by applying it to two putative examples of adaptive non-genetic inheritance: maternal effects on seed germination in plants and transgenerational phase shift in desert locusts. Our simulation models show how the adaptive value of non-genetic inheritance depends on its mechanism, the pace of environmental change, and life history characteristics.

When is incomplete epigenetic resetting in germ cells favoured by natural selection

Resetting of epigenetic marks, such as DNA methylation, in germ cells or early embryos is not always complete. Epigenetic states may therefore persist, decay or accumulate across generations. In spite of mounting empirical evidence for incomplete resetting, it is currently poorly understood whether it simply reflects stochastic noise or plays an adaptive role in phenotype determination. Here, we use a simple model to show that incomplete resetting can be adaptive in heterogeneous environments. Transmission of acquired epigenetic states prevents mismatched phenotypes when the environment changes infrequently relative to generation time and when maternal and environmental cues are unreliable. We discuss how these results may help to interpret the emerging data on transgenerational epigenetic inheritance in plants and animals.

Cooperative personalities and social niche specialization in female meerkats.

The social niche specialization hypothesis predicts that group‐living animals should specialize in particular social roles to avoid social conflict, resulting in alternative life‐history strategies for different roles. Social niche specialization, coupled with role‐specific life‐history trade‐offs, should thus generate between‐individual differences in behaviour that persist through time, or distinct personalities, as individuals specialize in particular nonoverlapping social roles. We tested for support for the social niche specialization hypothesis in cooperative personality traits in wild female meerkats (Suricata suricatta) that compete for access to dominant social roles. As cooperation is costly and dominance is acquired by heavier females, we predicted that females that ultimately acquired dominant roles would show noncooperative personality types early in life and before and after role acquisition. Although we found large individual differences in repeatable cooperative behaviours, there was no indication that individuals that ultimately acquired dominance differed from unsuccessful individuals in their cooperative behaviour. Early‐life behaviour did not predict social role acquisition later in life, nor was cooperative behaviour before and after role acquisition correlated in the same individuals. We suggest that female meerkats do not show social niche specialization resulting in cooperative personalities, but that they exhibit an adaptive response in personality at role acquisition.

Calling in the gap: competition or cooperation in littermates' begging behaviour?

Offspring are frequently raised alongside their siblings and are provisioned early in life by adults. Adult provisioning is stimulated by offspring begging, but it is unclear how each offspring should beg, given the begging behaviour of their siblings. It has previously been suggested that siblings may compete directly through begging for a fixed level of provisioning, or that siblings may cooperate in their begging in order to jointly elevate the level of provisioning by adults. We studied the begging behaviour of meerkat Suricata suricatta pups, explored how it changed as the begging behaviour of their littermates altered, and asked how the adults responded to group-level changes in begging. We found conflicting evidence for classic models of competitive and cooperative begging. Pups reared in larger litters begged at higher rates, yet experimentally increasing begging levels within groups caused individual begging rates to decrease. Pups decreased begging rates when close to other begging pups, and pups spaced further apart were fed more. Adults increased their overall level of provisioning as group levels of begging increased, but per capita provisioning decreased. Adults preferred to provision speakers playing back recordings of two pups begging alternately to recordings of the same two pups begging simultaneously. Therefore, we suggest that meerkat pups avoid some of the costs of direct competition imposed by an escalation of begging as other pups beg, by begging in gaps between the bouts of others or avoiding littermates. Such behaviour is also preferred by provisioning adults, thus providing additional benefits to the pups.

Costly reproductive competition between females in a monogamous cooperatively breeding bird

In many cooperatively breeding societies, only a few socially dominant individuals in a group breed, reproductive skew is high, and reproductive conflict is common. Surprisingly, the effects of this conflict on dominant reproductive success in vertebrate societies have rarely been investigated, especially in high-skew societies. We examine how subordinate female competition for breeding opportunities affects the reproductive success of dominant females in a monogamous cooperatively breeding bird, the Southern pied babbler (Turdoides bicolor). In this species, successful subordinate reproduction is very rare, despite the fact that groups commonly contain sexually mature female subordinates that could mate with unrelated group males. However, we show that subordinate females compete with dominant females to breed, and do so far more often than expected, based on the infrequency of their success. Attempts by subordinates to obtain a share of breeding impose significant costs on dominant females: chicks fledge from fewer nests, more nests are abandoned before incubation begins, and more eggs are lost. Dominant females appear to attempt to reduce these costs by aggressively suppressing potentially competitive subordinate females. This empirical evidence provides rare insight into the nature of the conflicts between females and the resultant costs to reproductive success in cooperatively breeding societies.

Competitive growth in a cooperative mammal

In many animal societies where hierarchies govern access to reproduction, the social rank of individuals is related to their age and weight and slow-growing animals may lose their place in breeding queues to younger ‘challengers’ that grow faster. The threat of being displaced might be expected to favour the evolution of competitive growth strategies, where individuals increase their own rate of growth in response to increases in the growth of potential rivals. Although growth rates have been shown to vary in relation to changes in the social environment in several vertebrates including fish and mammals, it is not yet known whether individuals increase their growth rates in response to increases in the growth of particular reproductive rivals. Here we show that, in wild Kalahari meerkats (Suricata suricatta), subordinates of both sexes respond to experimentally induced increases in the growth of same-sex rivals by raising their own growth rate and food intake. In addition, when individuals acquire dominant status, they show a secondary period of accelerated growth whose magnitude increases if the difference between their own weight and that of the heaviest subordinate of the same sex in their group is small. Our results show that individuals adjust their growth to the size of their closest competitor and raise the possibility that similar plastic responses to the risk of competition may occur in other social mammals, including domestic animals and primates.