The Cost of Reproduction in a Cooperatively Breeding Mammal: Consequences of Seasonal Variation in Rainfall, Reproduction, and Reproductive Suppression

Abstract

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 Evolution and Ecology of Oxidative and Antioxidant Status: A Comparative Approach in African Mole-Rats

“…The social mole-rats were captured and transported as outlined for solitary mole-rats. A subset of animals ( Table 1 ) was sampled within 72 h of being in captivity (similar to other studies [ 79 , 94 ]). An additional subset was maintained under laboratory conditions for more than six months before sampling.…”

“…All animals used in this study were considered adults and reproductively inactive (non-breeders) {see Bennett and Faulkes [125] on how reproductive status was determined} (Table 1). The use of non-breeders avoids complications between breeder and non-breeder comparisons associated with oxidative stress due to reproduction [74,79] and the effects of reproductive suppression differences [74,79,[98][99][100][101][102][103][104][105][106]125,126] (Supplementary File S1).…”

“…Therefore, this study sought to investigate the comparison of the redox status between family members of Bathyergidae due to their unique physiology, life-history, and reproductive system as well as the current understanding of their oxidative ecology ( Supplementary File S1 ) [ 22 , 51 , 55 , 71 , 74 , 76 , 77 , 78 , 79 , 80 , 81 , 82 , 83 , 84 , 85 , 86 , 87 , 88 , 89 , 90 , 91 , 92 , 93 , 94 , 95 , 96 , 97 , 98 , 99 , 100 , 101 , 102 , 103 , 104 , 105 , 106 , 107 , 108 , 109 , 110 , 111 , 112 , 113 ]. The current study included eight different subspecies and species of African mole-rats, namely the NMR, the DMR, the highveld mole-rat ( Cryptomys hottentotus pretoriae ) (CHP), the common mole-rat ( C. h. hottentotus ) (CHH), the Natal mole-rat ( C. h. natalensis ) (CHN), the Cape mole-rat (Georychus capensis ) (GC), and the Cape Dune mole-rat ( Bathyergus suillus ) (BS) […”

“…We further opted to utilise the same markers analysed from the same laboratory, as markers measured from different laboratories are rarely comparable [ 57 ]. Also, due to the confounding effects known in social mole-rats species, namely a reproductive division of labour [ 74 , 79 ], we used only the non-breeding colony members of social mole-rats and solitary mole-rats individuals outside their breeding season for the current study. We realise that the markers investigated do not include DNA damage, an important aspect associated with ageing [ 24 , 28 , 122 ]; however, this study was undertaken as an initial overview of oxidative stress and ageing in this unique rodent family.…”

Social stress is unlikely to play a major role in reproductive suppression of female subordinate naked mole-rats and Damaraland mole-rats

“…Medger [1] also eluded to the variation in the longevity between breeders and subordinates in social mole-rat species, which is a point of interest for many researchers [23][24][25][26][27][28]. Medger [1] suggested that the lower oxidative damage found in breeding females of the Damaraland mole-rat contributes to their longer lifespan [29] but does not mention that the opposite trend is seen in naked mole-rats [28].…”