The cost of reproduction in a cooperatively breeding mammal : consequences of seasonal variation in rainfall, reproduction, and reproductive suppression

Biological investments, such as reproduction, are influenced by both biotic and abiotic factors and their interactions. The trade-off between reproduction and survival has been well established. Seasonally breeding species, therefore, may exhibit variations in these trade-offs, but there is a dearth of knowledge concerning this. This study investigated the physiological cost of reproduction (measured through oxidative stress) across seasons in the cooperatively breeding highveld mole-rat (Cryptomys hottentotus pretoriae), one of the few seasonal breeding mole-rats. Oxidative stress indicates elevated reactive oxygen species (ROS) levels, which can overwhelm antioxidant defences resulting in damaged proteins, lipids and DNA, which overall can reduce longevity and compromise reproduction. Oxidative markers such as total oxidant status (TOS-measure of total peroxides present), total antioxidant capacity (TAC), oxidative stress index (OSI), and malondialdehyde (MDA) are utilised to measure oxidative stress. In this study, breeding and non-breeding male (NBM) and female mole-rats were captured during the dry season (breeding period) and wet season (non-breeding period). There was an apparent cost of reproduction in the highveld mole-rat; however, the seasonality pattern to the cost of reproduction varied between the sexes. Breeding females (BFs) had significantly higher MDA during the breeding period/dry season in comparison to the non-breeding period/wet season; this is possibly a consequence of bearing and nursing offspring. Contrastingly, breeding males (BMs) showed increased oxidative damage in the non-breeding/wet season compared to the breeding/dry season, possibly due to increased activities of protecting their mating rights for the next breeding/dry season, but this was not significant. Interestingly, during the non-breeding period/wet season, non-breeding females (NBFs) are released from their reproductive suppression, which resulted in increases in TOS and OSI, which again indicated that just the mere ability to be able to breed results in a cost (oxidative stress). Therefore we can speculate that highveld mole-rats exhibited seasonal variation in redox balance brought about by variation in abiotic variables (e.g., rainfall), physiology and behaviour. We conclude that physiological changes associated with reproduction are sufficient to induce significant acute oxidative stress in the plasma of female highveld mole-rats, which become alleviated following transition to the non-breeding season/wet period suggesting a possible hormetic effect.The SARChI chair of Mammalian Behavioural Ecology and Physiology from the DST-NRF South Africa, the National Research Foundation and the University of Pretoria.http://www.frontiersin.org/Physiologyam2022Mammal Research InstituteZoology and Entomolog

Seasonal changes in locomotor activity patterns of wild social Natal mole-rats (Cryptomys hottentotus natalensis)

Differences in individual locomotor activity patterns may be linked to a number of ecological factors, such as changes in ambient temperature or photoperiod. Observations on subterranean mammals suggest that they exhibit diel rhythms despite the lack of visual cues in their underground burrows, but it is unknown how seasonality and individual characteristics affect their activity. In this study we use RFID technology to monitor daily activity patterns of wild, social Natal mole-rats (Cryptomys hottentotus natalensis) during the summer and winter to investigate how their activity varies with season and whether their activity depends on individual characteristics such as body mass, sex and reproductive status. We found that in winter, individuals were more active during the time with the highest soil temperatures, whereas in summer, they showed a bimodal activity pattern during early morning and late afternoon coinciding with cooler soil temperatures. Individual characteristics, including reproductive status, did not affect general activity indicating that reproductive and non-reproductive individuals contribute equally to cooperative behaviors. We suggest that the activity patterns may be a behavioral adaptation to avoid extreme burrow temperatures and a mechanism to maintain a stable core body temperature. We highlight the advantages of RFID technology to study wild small mammal movements.A SARChI Chair of Mammal Behavioral Ecology and Physiology award from the Department of Science and Technology as well as National Research Foundation.http://frontiersin.org/Ecology_and_Evolutiondm2022Mammal Research InstituteZoology and Entomolog

Tissue Oxidative Ecology along an Aridity Gradient in a Mammalian Subterranean Species

Climate change has caused aridification which can alter habitat vegetation, soil and precipitation profiles potentially affecting resident species. Vegetation and soil profiles are important for subterranean mole-rats as increasing aridity causes soils to become harder and geophytes less evenly distributed, and the inter-geophyte distance increases. Mole-rats obtain all water and dietary requirements from geophytes, and thus digging in harder soils may amplify stressors (hyperthermia, dehydration- or exercise-induced damage). This study assessed the oxidative status of the wild common mole-rat along an aridity gradient (arid, semi-arid and mesic). Kidney and liver oxidative markers, including total oxidant status (TOS), total antioxidant capacity (TAC), oxidative stress index (OSI), malondialdehyde (MDA) and superoxide dismutase (SOD) were measured. Liver oxidative status did not demonstrate any significance with the degree of the aridity gradient. Aridity affected the TAC and OSI of the kidney, with individuals in the most arid habitats possessing the highest TAC. The evolution of increased group size to promote survival in African mole-rats in arid habitats may have resulted in the additional benefit of reduced oxidative stress in the kidneys. The SOD activity of the kidneys was higher than that of the liver with lower oxidative damage, suggesting this species pre-emptively protects its kidneys as these are important for water balance and retention

The best of both worlds : no apparent trade-off between immunity and reproduction in two group-living African mole-rat species

Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare.c.6662602.Co-operatively breeding mammals often exhibit a female reproductive skew and suppression of the subordinate non-breeding group members. According to evolutionary theory and the immunity–fertility axis, an inverse relationship between reproductive investment and survival (through immunocompetence) is expected. As such, this study investigated if a trade-off between immunocompetence and reproduction arises in two co-operatively breeding African mole-rat species, namely the Damaraland mole-rat (Fukomys damarensis) and common mole-rat (Cryptomys hottentotus hottentotus), which possess female reproductive division of labour. This study also attempted to investigate the relationship between the immune and endocrine systems in Damaraland mole-rats. There was no trade-off between reproduction and immunocompetence in co-operatively breeding African mole-rat species, and in the case of the Damaraland mole-rats, breeding females (BFs) possessed increased immunocompetence compared with non-breeding females (NBFs). Furthermore, the increased levels of progesterone possessed by Damaraland mole-rat BFs compared with NBFs appear to be correlated to increased immunocompetence. In comparison, BF and NBF common mole-rats possess similar immunocompetence. The species-specific differences in the immunity–fertility axis may be due to variations in the strengths of reproductive suppression in each species.http://rstb.royalsocietypublishing.orghj2024BiochemistryForestry and Agricultural Biotechnology Institute (FABI)GeneticsMicrobiology and Plant PathologyZoology and EntomologySDG-15:Life on lan

Seasonal Changes in Locomotor Activity Patterns of Wild Social Natal Mole-Rats (Cryptomys hottentotus natalensis)

Differences in individual locomotor activity patterns may be linked to a number of ecological factors, such as changes in ambient temperature or photoperiod. Observations on subterranean mammals suggest that they exhibit diel rhythms despite the lack of visual cues in their underground burrows, but it is unknown how seasonality and individual characteristics affect their activity. In this study we use RFID technology to monitor daily activity patterns of wild, social Natal mole-rats (Cryptomys hottentotus natalensis) during the summer and winter to investigate how their activity varies with season and whether their activity depends on individual characteristics such as body mass, sex and reproductive status. We found that in winter, individuals were more active during the time with the highest soil temperatures, whereas in summer, they showed a bimodal activity pattern during early morning and late afternoon coinciding with cooler soil temperatures. Individual characteristics, including reproductive status, did not affect general activity indicating that reproductive and non-reproductive individuals contribute equally to cooperative behaviors. We suggest that the activity patterns may be a behavioral adaptation to avoid extreme burrow temperatures and a mechanism to maintain a stable core body temperature. We highlight the advantages of RFID technology to study wild small mammal movements

Defining the link between oxidative stress, behavioural reproductive suppression and heterothermy in the Natal mole-rat (Cryptomys hottentotus natalensis)

Sub-lethal effects, such as oxidative stress, can be linked to various breeding and thermophysiological strategies, which themselves can be linked to seasonal variability in abiotic factors. In this study, we investigated the subterranean, social living Natal mole-rat (Cryptomys hottentotus natalensis), which, unlike other social mole-rat species, implements heterothermy seasonally in an attempt to avoid exercise-induced hyperthermia and relies solely on behavioural reproductive suppression to maintain reproductive skew in colonies. Subsequently, we investigated how oxidative stress varied between season, sex and breeding status in Natal mole-rats. Oxidative markers included total oxidant status (TOS measure of total peroxides present), total antioxidant capacity (TAC), OSI (oxidative stress index) and malondialdehyde (MDA) to measure oxidative stress. Breeding and non-breeding mole-rats of both sexes were captured during the summer (wet season) and winter (dry season). Seasonal environmental variables (air temperature, soil temperature and soil moisture) had a significant effect on TOS, OSI and MDA, where season affected each sex differently. Unlike other social mole-rat species that use both physiological and behavioural means of reproductive suppression, no oxidative costs to reproduction were present in the Natal mole-rats. Males had significantly higher MDA than females, which was most apparent in summer (wet season). We conclude that the significant oxidative damage in males is a consequence of exercise-induced oxidative stress, exacerbated by increased burrow humidities and poorer heat dissipation abilities as a function of body mass. This study highlights the importance of both breeding and thermophysiological strategies in affecting oxidative stress.SUPPLEMENTARY MATERIAL: FIGURE 1S. Hourly fluctuation in soil temperatures obtained from temperature loggers (ibutton) and the ERA5-Land dataset (ERA5) between Aug15, 2020 and Oct 15, 2020. Temperature loggers were buried ca. 15 cm below the surface to correspond with the soil temperature at 7-28 cm from ERA5.The SARChI chair of Mammalian Behavioural Ecology and Physiology from the DST-NRF South Africa, the National Research Foundation and the University of Pretoria.http://www.elsevier.com/locate/cbpb2023-05-11hj2023Mammal Research InstituteZoology and Entomolog

The endocrine control of reproductive suppression in an aseasonally breeding social subterranean rodent, the Mahali mole-rat (Cryptomys hottentotus mahali)

The following are the supplementary data related to this article. SUPPLEMENTARY FIGURE Fig. 1. Assay validation revealed by parallelism of serial dilutions of spiked plasma pools for Mahali mole-rats, with standard for the prolactin ELISA assay. Relative variation (%) of the slope of respective trendlines were <2% for Mahali mole-rats plasma. OD is the optical density measures the ELISA colour change, which is proportional to the concentration of prolactin.SUPPLEMENTARY TABLES. TABLE S1. Comparison of general linear models tested to explain body mass (g) as a function of season and reproductive status in Mahali mole-rats (Cryptomys hottentotus mahali). Best model fits are ranked by AICc, while model weights are estimates across all models and add up to 1. TABLE S2. Comparison of general linear models tested to explain variation in faecal glucocorticoid metabolite (fGCM, μg/g) concentrations as a function of season and reproductive status in Mahali mole-rats (C. h. mahali). Best model fits are ranked by AICc, while model weights are estimates across all models and add up to 1. TABLE S3. Comparison of generalised linear models tested to explain plasma testosterone concentrations (ng/dl) as a function of season and reproductive status in Mahali mole-rats (C. h. mahali). Best model fits are ranked by AICc, while model weights are estimates across all models and add up to 1. TABLE S4 Comparison of general linear models tested to explain plasma progesterone concentrations (ng/ml) as a function of season and reproductive status in Mahali mole-rat (C. h. mahali) females. Best model fits are ranked by AICc, while model weights are estimates across all models and add up to 1. TABLE S5. Comparison of general linear models tested to explain plasma prolactin concentrations (ng/ml) as a function of season and reproductive status in Mahali mole-rat (C. h. mahali) females. Best model fits are ranked by AICc, while model weights are estimates across all models and add up to 1.Cooperative behaviour, sociality and reproductive suppression in African mole-rats have been extensively studied. Nevertheless, endocrine correlates of some species of social mole-rats have been neglected, and these species may hold the key to understanding the behavioural and physiological complexity that allows the maintenance of social groups in African mole-rats. In this study, we investigated endocrine correlates implicated in the suppression of reproduction and cooperative behaviours, namely glucocorticoids (a stress-related indicator) through faecal glucocorticoid metabolites (fGCMs), plasma testosterone (an indicator of aggression) and plasma prolactin in the Mahali mole-rat (Cryptomys hottentotus mahali) across reproductive classes (breeding females and males, non-breeding females and males) and season (wet and dry). Breeders possessed higher levels of testosterone than non-breeders. In reproductively suppressed non-breeding females, fGCMs were significantly higher than in breeders. Furthermore, an adrenocorticotropic hormone stimulation test (ACTH challenge test) on both male and female non-breeders revealed that female non-breeders show a more significant response to the ACTH challenge than males. At the same time, plasma prolactin levels were equally elevated to similar levels in breeding and non-breeding females. Chronically high levels of prolactin and fGCM are reported to cause reproductive suppression and promote cooperative behaviours in non-breeding animals. Furthermore, there was a negative relationship between plasma prolactin and progesterone in non-breeding females. However, during the wet season, a relaxation of suppression occurs through reduced prolactin which corresponds with elevated levels of plasma progesterone in non-breeding females. Therefore, prolactin is hypothesised to be the primary hormone controlling reproductive suppression and cooperative behaviours in non-breeding females. This study provides new endocrine findings for the maintenance of social suppression in the genus Cryptomys.The SARChI Chair of Mammalian Behavioural Ecology and Physiology from the DST–NRF South Africa, the National Research Foundation and the University of Pretoria.https://www.elsevier.com/locate/yhbehhj2023Mammal Research InstituteZoology and Entomolog

New insights into morphological adaptation in common mole‐rats (<i>Cryptomys hottentotus hottentotus</i>) along an aridity gradient

Morphological adaptation is the change in the form of an organism that benefits the individual in its current habitat. Mole‐rats (family Bathyergidae), despite being subterranean, are impacted by both local and broad‐scale environmental conditions that occur above ground. Common mole‐rats (Cryptomys hottentotus hottentotus) present an ideal mammalian model system for the study of morphological variation in response to ecology, as this species is found along an aridity gradient and thus can be sampled from geographically non‐overlapping populations of the same species along an environmental longitudinal cline. Using the mass of five internal organs, ten skeletal measurements and 3D morphometric analyses of skulls, we assessed the morphology of wild non‐breeding individuals from five common mole‐rat populations in South Africa. We found that the body mass and mean relative mass of the spleen and kidneys in arid populations was larger, and individuals from arid regions possessed shorter legs and larger inter‐shoulder widths compared to individuals from mesic regions. Additionally, arid populations demonstrated greater skull depth, and shape change of features such as angular processes of the lower jaw than mesic individuals, indicating that these distinct geographic populations show differences corresponding to the aridity gradient, potentially in response to environmental factors such as the variation in food sources found between different habitats, in addition to different soil compositions found in the different regions. Arid populations potentially require a stronger jaw and neck musculature associated with mastication to chew xeric‐adapted plants and to dig through hard soil types, whereas mesic populations excavate through soft, looser soil and may make use of their front limbs to aid the movement of soils when digging. Aridity influences the morphology of this species and could indicate the impact of environmental changes on speciation and mammalian skull morphology

Tissue Oxidative Ecology along an Aridity Gradient in a Mammalian Subterranean Species

Climate change has caused aridification which can alter habitat vegetation, soil and precipitation profiles potentially affecting resident species. Vegetation and soil profiles are important for subterranean mole-rats as increasing aridity causes soils to become harder and geophytes less evenly distributed, and the inter-geophyte distance increases. Mole-rats obtain all water and dietary requirements from geophytes, and thus digging in harder soils may amplify stressors (hyperthermia, dehydration- or exercise-induced damage). This study assessed the oxidative status of the wild common mole-rat along an aridity gradient (arid, semi-arid and mesic). Kidney and liver oxidative markers, including total oxidant status (TOS), total antioxidant capacity (TAC), oxidative stress index (OSI), malondialdehyde (MDA) and superoxide dismutase (SOD) were measured. Liver oxidative status did not demonstrate any significance with the degree of the aridity gradient. Aridity affected the TAC and OSI of the kidney, with individuals in the most arid habitats possessing the highest TAC. The evolution of increased group size to promote survival in African mole-rats in arid habitats may have resulted in the additional benefit of reduced oxidative stress in the kidneys. The SOD activity of the kidneys was higher than that of the liver with lower oxidative damage, suggesting this species pre-emptively protects its kidneys as these are important for water balance and retention