Sociality in African mole-rats : exploring how rainfall affects dispersal and genetic exchange in the Natal mole-rat (Cryptomys hottentotus natalensis)

Abstract

The Natal mole-rat (Cryptomys hottentotus natalensis) is a social subspecies of African mole-rat related to the common mole-rat (Cryptomys hottentotus hottentotus). They inhabit mesic grassland in eastern South Africa from coastal regions to well over 2000m elevation. There have been a few studies on their physiology and reproductive suppression, but their ecology and life history has not been reported in detail. This study used capture-mark recapture methods to investigate life history, population demographics, behaviour, and gene flow in wild Natal mole-rats living at a high elevation site in the southern Drakensberg Mountains. I captured a total of 403 individuals across 52 family groups. Individuals were weighed, measured, sexed, and assigned a reproductive status on capture. Tissue samples were collected for genetic analysis and then they were implanted with a passive integrated transponder for identification at recapture. Groups were captured every six months over the course of 2 years. Both environmental factors and population demographics can have far reaching effects on individual life history, including altering spatial arrangement, behaviour, body condition, and fecundity rates. I found that Natal mole-rats have reduced group sizes (mean 6) compared to the more arid dwelling African mole-rat species. Population wide sex ratios were evenly split between males and females. However, within-group adult sex ratios were skewed towards males, and this skew became more pronounced in larger groups. Sex ratios, group size, and group biomass did not show any seasonal differences. Small litter sizes (1.3), slow population growth rates (0.17), long maturation time (1.2 years) of females indicate a “slow” life history. I found strong sexual dimorphism, with males being larger than females. Male exhibited a faster growth rate compared to females, but growth rates were not affected by group size. This indicates that within-group competition is reduced or absent, likely due to the smaller mean group size or increased availability of food resources. Individual body condition varied between seasons and was affected by group size. During summer body condition increased with increasing group size, highlighting the benefits of collective foraging. But during winter body condition decreased with increasing group size, likely due to low quality of food and a necessity to continue foraging through winter. Interestingly, the body condition in reproductive females increased with group size during winter, when all others decreased. However, their fecundity did not appear to be affected by group size. The expected benefits of helping effects from larger groups may be reduced in Natal mole-rats. 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 ambient temperature, photoperiod, or individual characteristics affects their activity. I used RFID technology to monitor daily activity patterns of wild mole-rats during the summer and winter seasons. I combined the activity data with satellite climate data to investigate how their activity patterns vary between seasons and whether their activity depends on individual characteristics such as body mass, sex and reproductive status. Individual characteristics, including reproductive status, did not affect general activity. This result suggests that reproductive and non-reproductive individuals contribute equally to cooperative behaviours unlike other mole-rats where reproductive individuals exhibit reduced contributions. I found that in winter, individuals were more active during mid-day to coincide with higher soil temperatures, whereas in summer, they showed a bimodal activity pattern during early morning and late afternoon coinciding with cooler soil temperatures. Activity patterns are therefore a behavioural adaptation to avoid extreme burrow temperatures and a mechanism to maintain a stable core body temperature. Thermoregulatory behavioural adaptations appear to be more important than differences in cooperative contributions to Natal mole-rats. I extracted DNA from tissue samples and then used custom designed microsatellite markers to assess spatial grouping and gene flow in the population. Population-level analyses, such as FST, focus on genetic relatedness among social groupings, while relatedness coefficients determine relatedness between individuals in the population. I found that pairwise-relatedness coefficients were surprisingly similar to the arid dwelling Damaraland mole-rat (Fukomys damarensis) in the southern Kalahari, despite assumptions that higher rainfall would provide more dispersal opportunities and higher immigration rates. Population level FST values indicated the presence of male-biased dispersal. Relatedly, females were more related to females in neighbouring family groups than males. The study site had three landscape features which may act as dispersal barriers, such as a road, a river, and a steep rocky hillside. A non-spatial Bayesian clustering analysis determined that these features did not pose major dispersal barriers to mole-rats. I estimated dispersal distances to be between 350 – 400m, with males having slightly higher dispersal distances compared to females. There was no evidence of isolation by distance, and gene flow is well maintained within the study site. In conclusion this study found that Natal mole-rats continue to exhibit delayed dispersal and high levels of within-group relatedness despite increased annual rainfall. Their life history and physiological adaptations allow them to cope with living in an environment with extreme seasonal fluctuations. With the projected increased ambient temperatures due to climate change, mole-rats living at higher altitude may not cope well with very minor deviations from the conditions they have adapted to. I found that body mass appeared reduced compared to 20 years ago, and this decrease may be due to climate change or habitat alteration. The evolution of various physiological traits unique to Natal mole-rats means they may be more susceptible to the effects of climate change than other subterranean rodents. Previous labelling of Natal mole-rats as “less social” should be avoided and there is evidence to support the claim that they are singular cooperative breeders.