Rebecca Rimbach

The neoteny-helper hypothesis: When to expect and when not to expect endocrine mechanisms to regulate allo-parental care?

Family groups with helpers occur in several species of fish, birds and mammals. In such cooperatively breeding species all group members help with raising the offspring, i.e. parents and offspring from previous litters. While the ecological reasons and ultimate consequences of allo-parental care have been studied in detail, we know little about its physiological regulation. We propose three alternative hypotheses for the endocrine regulation of allo-parental care. 1. The neoteny-helper hypothesis predicts that helpers that did not undergo adolescence yet show helping behavior without any endocrine mechanisms activating it, as helping is the default response towards infant stimuli. The endocrine changes during adolescence would then deactivate helping behavior. 2. The parent-helper hypothesis predicts that helpers undergo the same endocrine changes as parents (increased prolactin and corticosterone levels; decreased testosterone in males but increased estrogen in females). We predict that this hypothesis is especially important in post-adolescent helpers. 3. The helper-specific hypothesis predicts that there are specific endocrine mechanisms that only exist in helpers but not in breeders. We review evidence for these three hypotheses in 23 species of fish, birds, and mammals. We found no evidence for the helper-specific hypothesis but for both other hypotheses. As predicted, this depended on whether helpers were pre- or post-adolescent, but information on whether or not helpers underwent adolescence was often missing. Thus, future studies should investigate whether or not helpers have reached sexual maturity, differentiate between pre- and post-adolescent helpers, and study behavioral changes in helping behavior during adolescence. We conclude that the neurobiological circuits in the brain necessary for allo-parental care might often be the default stage in helpers from cooperative breeding species, which might be deactivated by specific endocrine mechanisms during adolescence, and then would need reactivation for allo-parental and parental care.

Both thyroid hormone levels and resting metabolic rate decrease in African striped mice when food availability decreases

ABSTRACT In response to variation in food availability and ambient temperature (Ta), many animals show seasonal adaptations in their physiology. Laboratory studies showed that thyroid hormones are involved in the regulation of metabolism, and their regulatory function is especially important when the energy balance of an individual is compromised. However, little is known about the relationship between thyroid hormones and metabolism in free-living animals and animals inhabiting seasonal environments. Here, we studied seasonal changes in triiodothyronine (T3) levels, resting metabolic rate (RMR) and two physiological markers of energy balance (blood glucose and ketone bodies) in 61 free-living African striped mice (Rhabdomys pumilio) that live in an semi-arid environment with food shortage during the dry season. We predicted a positive relationship between T3 levels and RMR. Further, we predicted higher T3 levels, blood glucose levels and RMR, but lower ketone body concentrations, during the moist season when food availability is high compared with summer when food availability is low. RMR and T3 levels were negatively related in the moist season but not in the dry season. Both RMR and T3 levels were higher in the moist than in the dry season, and T3 levels increased with increasing food availability. In the dry season, blood glucose levels were lower but ketone body concentrations were higher, indicating a change in substrate use. Seasonal adjustments in RMR and T3 levels permit a reduction of energy expenditure when food is scarce, and reflect an adaptive response to reduced food availability in the dry season. Summary: Seasonal changes occur in the relationship between thyroid hormone levels and resting metabolic rate in free-living African striped mice: a negative relationship exists in the moist season but not the dry season.

Dietary protein influences the life-history characteristics across generations in the African striped mouse Rhabdomys.

The level of dietary protein determines the onset of reproduction, affects offspring growth and maturation, and hence influences life-history traits and fitness. However, to date, the long-term life-history consequences of protein deficiency are not well understood. We studied the transgenerational effects of different levels of dietary protein on the life-history and level of maternal behavior of the striped mouse Rhabdomys dilectus chakae in captivity. Breeding pairs were assigned to three treatments based on the percentage of dietary protein: baseline (BP; 19%); high protein (HP; 24%); and low protein (LP; 10%). Reproductive output and offspring ontogeny was diminished in the LP treatment compared to the other treatments. Transgenerational effects were studied by breeding F2 females raised on the LP or HP diets on the same (HP-HP, LP-LP) or altered diets (HP-LP, LP-HP). The LP-LP treatment had no reproductive success, while reproductive capacity in the remaining treatments was determined mainly by the diet of mothers at breeding. Pups from protein-restricted females (LP, HP-LP) showed post-weaning compensatory growth. Timing of sexual maturity was age-dependent in female and mass-dependent in male offspring. Females fed low protein diets during breeding (LP, HP-LP) displayed lower levels of maternal behavior than females from the other treatments. This study demonstrates that the level of dietary protein influences the life-history of R. d. chakae in predictable ways. The taxon responds to changes in dietary protein at breeding, largely regardless of its nutrition during rearing. Such phenotypic flexibility in life-history parameters allows Rhabdomys to adaptively respond to unpredictable environmental changes.

Pre- and postnatal dietary protein deficiency influences anxiety, memory and social behaviour in the African striped mouse Rhabdomys dilectus chakae.

Dietary protein deficiency influences the behavioural phenotypes of mammals. We studied whether protein deficiency during gestation and/or post-weaning heightened anxiety, reduced memory recall and influenced competitive ability in the African striped mouse Rhabdomys dilectus chakae. Mice were subjected to five protein diet treatments, which they received continuously, or were raised on one diet to weaning and switched to an alternate diet post-weaning (Day 16): 1) HP-HP: high protein (24%); first letter pair indicates maternal diet and the second pair indicates offspring diet post-weaning; 2) BP-BP: baseline protein (19%); 3) LP-LP: low protein (10%); 4) HP-LP: switched from high to low protein diet; and 5) LP-HP: switched from low protein to high protein diet. From Day 70, when mice were sexually mature, 20 individuals (10 males, 10 females) per treatment were subjected to three successive experiments, in which we tested their anxiety responses in: 1) an open field arena (time spent in the centre of the open field); 2) novel object recognition (time spent exploring a novel object); and 3) social interactions (excluding BP-BP) in age-matched same-sex dyadic encounters (aggressive, amicable and avoidance behaviours). LP-LP and LP-HP treatment mice spent the least amount of time in the centre of the open field, did not demonstrate object preference compared to the other treatments, and were the most aggressive in dyadic encounters. Our study shows that the systemic effects of protein-deficient diets during early life shapes the behavioural phenotype in R. d. chakae, possibly through early organisation of neuro-biological pathways or competition among littermates.

Food Availability Is the Main Driver of Seasonal Changes in Resting Metabolic Rate in African Striped Mice (Rhabdomys pumilio)

Resting metabolic rate (RMR) influences energy allocation to survival, growth, and reproduction, and significant seasonal changes in RMR have been reported. According to one hypothesis, seasonal changes in RMR are mainly attributable to seasonal changes in ambient temperature (Ta) and food availability. Studies on species from the temperate zone indicated that food availability is the main driver. However, whether this is generally true is unknown, because studies from the tropics and subtropics, where most species live, are rare. We studied the African striped mouse (Rhabdomys pumilio) inhabiting a seasonal environment with hot dry seasons with low food availability and cold moist seasons with high food availability. Using 603 RMR measurements of 277 individuals, we investigated the relative importance of food availability and Ta on RMR during selected periods, in which one extrinsic factor varied while the other factor was relatively constant. At similar Ta, residual RMR increased with increasing levels of food availability. In contrast, different Ta did not influence residual RMR at similar levels of food availability. Thus, our study on a subtropical species gives support to the hypothesis, derived from temperate zone species, that food availability mainly drives seasonal changes in RMR.

Active and explorative individuals are often restless and excluded from studies measuring resting metabolic rate: Do alternative metabolic rate measures offer a solution?

It has often been proposed that bolder, more explorative or more active individuals also have a higher resting metabolic rate (RMR), indicating metabolic costs of these personality types. However, such individuals might often be restless and thus excluded from RMR datasets, leading to a significant sampling bias. We tested (1) whether such a bias occurs when animals are measured for a relatively common but short time period of 3h, and if so, (2) whether alternative measures of metabolic rate, that allow the incorporation of non-resting individuals, would reveal associations between metabolism and personality. For this, we studied free-living individuals of the African striped mouse (Rhabdomys pumilio) both during the moist season (N=25 individuals) with high food availability and the dry season (N=48 individuals) with low food availability. We assessed variation in the latency to explore a novel object, and the time spent active and time spent in the centre of a neutral arena. We examined links between personality and (i) RMR and (ii) four alternative metabolic rate (MR) metrics: average MR, highest MR, lowest MR and span of MR. Twenty-nine percent of the measured individuals had to be excluded from our RMR study because they remained restless during respirometry trials. Striped mice showed a behavioural syndrome where fast explorers also spent more time in centre and more time active than slow explorers. Individuals that did not rest during respirometry trials were faster explorers and in the moist season, they were also more active and spent more time in the centre than individuals that rested. We found no relationship between RMR and the behavioural syndrome, which might be due to the exclusion of individuals with a certain behavioural type, leaving a subset of compliant individuals. In the moist season, we found positive relationships between the behavioural syndrome and span of MR and lowest MR. In the dry season, low food availability may mask links between the behavioural syndrome and alternative MR measures due to reduced overall activity in striped mice. Our study demonstrated the importance to consider personality when measuring RMR and suggests that some alternative MRs may be useful to examine relationships between metabolism and personality when it is impossible to measure individuals over extended time periods.

Correction: Both thyroid hormone levels and resting metabolic rate decrease in African striped mice when food availability decreases (doi: 10.1242/jeb.151449)

There was an error published in J. Exp. Biol. (2017) 220 , [837-843][1] ([doi: 10.1242/jeb.151449][2]). A mistake was made by the authors in the calculation of RMR values. The corrected Results section, tables and figures follow and we indicate where the significance of relationships changed. There

Seasonal variation in energy expenditure in a rodent inhabiting a winter-rainfall desert

Animals that spend more energy than they obtain risk entering allostatic overload, reducing survival and fitness. They are predicted to adjust their daily energy expenditure (DEE) during periods of food scarcity. Adjustments of DEE to changes in food availability have been well-studied in species in temperate zones during winter, but less so in species enduring seasonal droughts. Likely mechanisms regulating DEE involve adjustments of activity and maintenance metabolism. Species that experience seasonal droughts and changes in food availability, like the African striped mouse (Rhabdomys pumilio), are appropriate model organisms to study the regulation of seasonal changes of DEE. We quantified DEE using the ‘doubly labelled water’ method, measured resting metabolic rate (RMR), and concomitantly determined activity levels using all-day focal observations of 69 free-living striped mice in the cold moist season with high food availability and the hot dry season with low food availability. Striped mice decreased their DEE in the food scarce dry season using multiple mechanisms, especially reductions in RMR, and reduced overall physical activity. This was further facilitated passively by reduced thermoregulatory costs. Our study demonstrates that animals reduce DEE via active and passive mechanisms in food-restricted environments, and highlights that several environmental factors should be considered simultaneously when aiming to understand how animals cope with harsh environments.

Protein deficiency decreases stereotypic behavior frequency and prevalence and activity in the striped mouse Rhabdomys dilectus chakae

Diverse motivational triggers, including diet, elicit stereotypic behavior. We investigated whether diets comprised of different protein levels but similar levels of energy were associated with the occurrence of locomotor stereotypies in the striped mouse Rhabdomys dilectus chakae. In a first experiment, 20 stereotypic and 20 non-stereotypic (10 subjects per sex and per group) juvenile (40 days old) subjects were placed on baseline (BP), high (HP) or low protein (LP) diet treatments (120 subjects in total). All subjects initially identified as stereotypic displayed stereotypic behavior in the BP and HP treatments on Days 60-63 and Days 80-83 compared to 35% and 12.5% of LP subjects, respectively. Moreover, LP subjects displayed lower levels of activity and stereotypic behavior than BP and HP subjects. Those identified as non-stereotypic never displayed stereotypy. In a second experiment, 48 individuals, bred and reared on LP and whose parents were stereotypic, were assigned to either HP (13 males, 12 females) or LP (12 males, 11 females) treatments at 50 days of age for 30 days. Stereotypy was three times less likely to occur in the LP than the HP treatment, and activity was greater in LP-HP individuals than LP-LP individuals. In both experiments, LP individuals had the lowest body mass. Striped mice adjusted their behaviors in response to dietary protein levels. Protein deficiency reduced activity and stereotypic behavior and prevalence, possibly related to an energy or neurological deficit.