Ivana Schoepf

Social flexibility and social evolution in mammals: a case study of the African striped mouse (Rhabdomys pumilio)

Environmental change poses challenges to many organisms. The resilience of a species to such change depends on its ability to respond adaptively. Social flexibility is such an adaptive response, whereby individuals of both sexes change their reproductive tactics facultatively in response to fluctuating environmental conditions, leading to changes in the social system. Social flexibility focuses on individual flexibility, and provides a unique opportunity to study both the ultimate and proximate causes of sociality by comparing between solitary and group‐living individuals of the same population: why do animals form groups and how is group‐living regulated by the environment and the neuro‐endocrine system? These key questions have been studied for the past ten years in the striped mouse Rhabdomys pumilio. High population density favours philopatry and group‐living, while reproductive competition favours dispersal and solitary‐living. Studies of genetic parentage reveal that relative fitness of alternative reproductive tactics depends on the prevailing environment. Tactics have different fitness under constrained ecological conditions, when competitive ability is important. Under conditions with relaxed ecological constraints, alternative tactics can yield equal fitness. Both male and female striped mice display alternative reproductive tactics based on a single strategy, i.e. all individuals follow the same decision rules. These changes are regulated by endocrine mechanisms. Social flexibility is regarded as an adaptation to unpredictably changing environments, selecting for high phenotypic flexibility based on a broad reaction norm, not on genetic polymorphism for specific tactics.

Female home range size is regulated by resource distribution and intraspecific competition: a long-term field study

The size of an individuals home range is an important feature, influencing reproduction and survival, but it can vary considerably among both populations and individuals. The factors accounting for such variation are still poorly understood, and comprehensive long-term field studies considering various environmental factors that influence home range size are rare. We investigated the effects of seasonality, availability of food, cover, number of direct neighbours and the relative individual body mass on home range sizes in 125 adult female striped mice, Rhabdomys pumilio, in South Africa from 2004 to 2008. We used radiotelemetry to estimate home range sizes, trapping to determine the number of direct neighbours, and plant surveys in every home range to determine availability of food and cover. Home ranges were smaller when food quantity was high, many territorial neighbours were present, females had a relatively small body mass and during the nonbreeding season. We conclude that the availability of food resources and intraspecific competition are the main factors influencing home range size in female striped mice. Females enlarged their home ranges when territorial neighbours were few, and there was a significant positive correlation between home range size and quantity of food plants. This indicates that home range size might not reflect the minimal trade-off between access to resources that allow for a females survival and lowest cost for defending and foraging in that area. Instead, we propose a hypothesis for future research that female striped mice occupy areas several times larger than needed to improve their fitness by providing resources for future offspring.

Better off alone! Reproductive competition and ecological constraints determine sociality in the African striped mouse (Rhabdomys pumilio)

1. While the reasons for group-living have been studied for decades, little is known about why individuals become solitary. 2. Several previous experimental studies could demonstrate that group-living can arises as a consequence of ecological constraints. 3. It has been argued that reproductive competition between group members leads to significant costs of group-living, being a main reason of solitary-living. However, so far, no studies tested experimentally whether reproductive competition can explain solitary-living. 4. Using a socially flexible species, the African striped mouse (Rhabdomys pumilio), we tested experimentally in the field whether dispersal and solitary-living are more likely to occur when reproductive competition is present. 5. We investigated ecological constraints, here expressed as a function of population density, by removing groups of striped mice and creating vacant territories. To control for the effect of reproductive competition, which occurs only during the breeding season, we performed experiments during both the breeding and the non-breeding season. This is the first removal experiment performed in a species with communal breeding during the non-breeding season. 6. During the breeding season, when population density was low, more striped mice from experimental groups moved into the vacant territories and became solitary than striped mice from control groups. This is in support of the ecological constraints hypothesis. 7. During the non-breeding season, striped mice remained group-living despite the availability of free territories. Significantly, more striped mice became solitary-living during the breeding than during the non-breeding season. This is the first experimental support for the reproductive competition hypothesis explaining solitary-living. 8. Analysis of the sexual maturity of males showed that males which became solitary had a higher reproductive potential than males that remained group-living. Analysis of the body mass data of females showed that more solitary females reproduced than group-living females. These results indicate that by becoming solitary individuals of both sexes avoided costs of reproductive competition within groups. 9. Our study provides experimental evidence that reproductive competition within groups can lead to dispersal and solitary-living.

Differences in social behaviour between group-living and solitary African striped mice, Rhabdomys pumilio

Little is known about the extent to which solitary individuals differ in their social behaviour from group-living ones within the same species. Using the socially flexible African striped mouse, we tested through a series of dyadic encounters in a neutral arena whether group-living mice that later became solitary differed from their philopatric conspecifics. We compared philopatric and solitary mice both before and after dispersal. We predicted striped mice that became solitary would be more aggressive, less amicable and more investigative than individuals that remained group living, and would change their social behaviour after changing from group to solitary living in the same direction (becoming more aggressive, etc.). Dyadic encounters were conducted on 42 group-living individuals and 13 individuals that were first group living and later became solitary. Striped mice that became solitary showed higher levels of aggression and social investigation than their conspecifics that remained group living, differences that were already present before individuals dispersed. Dispersing striped mice showed a negative correlation between amicability and aggression towards opposite-sex individuals, which could be linked to sexual motivation. A second behavioural syndrome in the form of a positive correlation between aggression and social investigation towards same-sex individuals might have indicated that dispersing striped mice were ready to defend their own territory. Our study provides evidence that within the same population and at the same time, individuals that disperse and become solitary differ behaviourally from their group-living conspecifics even before dispersal, and further change their behaviour after dispersal in an evolutionarily adaptive way.

Personality does not constrain social and behavioural flexibility in African striped mice

The development and persistence of personality in nature are counterintuitive because, in heterogeneous environments, personality is expected to limit the degree of behavioural flexibility. Recent work has shown that personality and behavioural flexibility might be linked, but their interaction is not well understood and could be elucidated by studying a socially flexible species. Using well-established tests, we measured the personality traits of activity, boldness, exploration and aggressiveness in free-living striped mice (Rhabdomys pumilio) in South Africa. Specifically, we tested whether personality changes when individuals change their reproductive tactic, either from group-living philopatrics to solitary-living females and roaming males or from non-breeding philopatrics to breeders. Our results showed that striped mice have personalities: Individuals behaved consistently for all the behavioural traits measured both over time and contexts (breeding to non-breeding season). While most of the personality traits measured remained consistent among tactics, they did not predict which tactic an individual would adopt next, suggesting that environmental conditions rather than personality influence tactic switching. Additionally, we found important differences in the consistency of the behaviours measured between males and females, indicating that sexual selection might play a prominent role in the maintenance of personality in this species. Our study demonstrates that some personality traits can be stable over an entire lifetime even in socially flexible species and that personality does not constrain social flexibility.

Personality traits are consistent when measured in the field and in the laboratory in African striped mice (Rhabdomys pumilio)

Personality in free-living individuals has predominantly been measured under standardized laboratory conditions. Such measurements have been then linked to life-history traits, fitness and survival. Yet, it remains unclear how such personality measurements reflect the variation shown by free-living individuals, if the same measurements were taken directly in their natural environment. Here, we used free-living African striped mice to test whether the personality traits of activity, boldness, exploration and aggression are consistent when measured in the laboratory and in the field contexts. First, we established whether personality traits were repeatable and consistent within one context. Next, we compared measurements across the two different contexts. Additionally, we established whether personality traits were correlated with one another in behavioural syndromes and assessed whether the resulting syndromes were consistent across the two contexts. All personality traits in the laboratory were measured using classical personality tests. The same tests were then modified and used to measure personality of the same individuals in the field. All personality traits were highly repeatable and consistent within the same context. In addition, individuals behaved consistently for all the behaviours measured both in the laboratory and in the field. Further, we found that the presence of two correlated context-specific separate latent variables (one for the field and one for the laboratory) underpinned all the behaviours measured, indicating that there is a context-specific syndrome in this species. Overall, our results confirm that measurements of personality traits of wild striped mouse individuals recorded in the laboratory environment are consistent with the traits that the same individuals show under natural conditions.Significance statementAnimal personality research has been mostly focused on measuring traits of wild individuals under standardized laboratory conditions. Most recently, however, such approaches have come under increased scrutiny as it is unclear whether personality measured in the laboratory reflects the variation that the same individuals would show if the same measurements were taken directly in their natural habitat. Here, we used wild African striped mice to test whether the personality traits of activity, boldness, exploration and aggression are consistent when measured in the laboratory and in the field contexts. Using similar protocols, we established whether personality traits were repeatable and consistent within one context and then compared measurements across the two different contexts. We showed that personality measures from standardized laboratory conditions are consistent with field measurements for all personality traits considered.

The pathophysiology of survival in harsh environments.

An individual’s ability to survive harsh conditions might depend on its available energy, and also on its health, which is expected to decline as conditions deteriorate. Yet, we know little about how health and energy expenditure are shaped by harsh environmental conditions in free-living vertebrates. Here, we studied how African striped mice (Rhabdomys pumilio) that survived summer droughts differed in their energy expenditure and health from non-survivors. Specifically, we tested whether: (1) survivors’ and non-survivors’ health and energy expenditure differed before environmental conditions declined; (2) non-survivors were in poorer health and had greater energy expenditure than survivors when conditions were harshest; (3) non-survivors’ health deteriorated more than that of survivors as conditions deteriorated; and (4) survivors recovered once conditions improved. Survivors and non-survivors’ health was assessed using VetsScan ABAXIS, while energy expenditure was measured as resting metabolic rate (RMR). Before conditions declined, non-survivors had lower energy stores and higher globulin levels than survivors. As conditions became harsher, survivors’ and non-survivors’ health deteriorated but only non-survivors showed signs of permanent pathology (increased glucose and decreased globulin). Once conditions improved, survivors’ health improved but was not fully restored (increased alanine aminotransferase and decreased globulin). Furthermore, while survivors and non-survivors had similar RMR before conditions became harsh; their levels diverged considerably when conditions deteriorated, with survivors having a decreased RMR and non-survivors having an increased RMR. Our results show that an individual’s health before facing an environmental challenge and the way it regulates its RMR influences its ability to maintain homeostasis when conditions become more taxing.

Basal blood glucose concentration in free-living striped mice is influenced by food availability, ambient temperature and social tactic

Vertebrates obtain most of their energy through food, which they store mainly as body fat or glycogen, with glucose being the main energy source circulating in the blood. Basal blood glucose concentration (bBGC) is expected to remain in a narrow homeostatic range. We studied the extent to which bBGC in free-living African striped mice (Rhabdomys pumilio) is influenced by ecological factors with a bearing on energy regulation, i.e. food availability, abiotic environmental variation and social tactic. Striped mice typically form extended family groups that huddle together at night, reducing energetic costs of thermoregulation, but solitary individuals also occur in the population. We analysed 2827 blood samples from 1008 individuals of seven different social categories that experienced considerable variation in food supply and abiotic condition. Blood samples were taken from mice in the morning after the overnight fast and before foraging. bBGC increased significantly with food plant abundance and decreased significantly with minimum daily ambient temperature. Solitary striped mice had significantly higher bBGC than group-living striped mice. Our results suggest that adaptive responses of bBGC occur and we found large natural variation, indicating that bBGC spans a far greater homeostatic range than previously thought.

Trade-offs between reproduction and health in free-ranging African striped mice

Energy is limited and must be allocated among competing life-history traits. Reproduction is considered one of the most energetically demanding life-history stages. Therefore, the amount of energy an individual invests in reproduction might carry fitness costs through reduced energy allocation to other activities such as health maintenance. We investigated whether reproduction impacts health in the seasonally breeding African striped mouse (Rhabdomys pumilio). We measured health in individuals that reproduced (breeders) and individuals that did not reproduce (their adult offspring) and tested whether: (1) breeders’ health before reproduction was similar to that of their offspring (representing a baseline); (2) breeders’ health deteriorated after reproduction; (3) breeders’ health after reproduction was worse than that of their offspring. We collected blood samples from 12 breeding females and 11 breeding males both at the onset and at the end of the breeding season and from 12 adult daughters and 11 adult sons that did not reproduce at the end of the breeding season. Health was assessed using serum biochemistry analysis with VetScan Abaxis. Breeders differed considerably in their health before and after reproduction, particularly in parameters associated with digestion (lower amylase in males), metabolism (lower albumin, alkaline phosphatase, creatinine and glucose), osmoregulation (lower potassium and phosphorous in females) and immunity (higher globulin and altered alanine aminotransferase). Our results suggest that with the onset of breeding striped mice shifted their energy allocation from maintaining health to reproduction, indicating that investment into reproduction carries significant health costs.

Boldness: are open field and startle tests measuring the same personality trait?

Boldness, the willingness of individuals to engage in risky behaviour, is one of the most studied personality traits. It has been measured using a variety of tests; however, measuring a behaviour using different assays may lead to a jingle fallacy. The few studies that have attempted to determine whether these different assays are comparable have produced mixed results. A lack of repeatability between boldness measures under standardized and natural conditions may be the source of this variation. Here, we tested whether risk-taking behaviour of free-living African striped mice, Rhabdomys pumilio, measured in a laboratory using open field tests is comparable with measures of risk-taking behaviour from startle tests. These measures were then compared with measures of risk-taking behaviour obtained from equivalent open field and startle tests performed on the same individuals under natural conditions. During open field tests, we assessed the time an individual spent away from the wall of the arena (in the laboratory) or from its nest (in nature). During startle tests, we measured the latency to re-emerge from either a protective box (in the laboratory) or a nest (under natural conditions) after an individual was scared away. Our results showed that risk-taking behaviour measured using the open field and the startle tests were repeatable within the same context (tested twice per assay) and across contexts (laboratory, nature). However, open field measures of risk-taking behaviour were not correlated with startle measures, supporting the idea that the two tests are assaying different personality traits. The variations in the outcome observed in the two assays probably resulted from the presentation of threatening stimuli in the startle test. We propose that, at least in striped mice, the startle test is more suitable for measuring anxiety than boldness.