Higher resting metabolic rate in long-lived breeding Ansell’s mole-rats (Fukomys anselli)
© The Author(s). 2017
Received: 19 August 2017
Accepted: 14 September 2017
Published: 22 September 2017
Reproduction is an energetically expensive process that supposedly impairs somatic integrity in the long term, because resources are limited and have to be allocated between reproduction and somatic maintenance, as predicted by the life history trade-off model. The consequence of reduced investment in somatic maintenance is a gradual deterioration of function, i.e. senescence. However, this classical trade-off model gets challenged by an increasing number of contradicting studies. Here we report about an animal model, which adds more complexity to the ongoing debate. Ansell’s mole-rats are long-lived social subterranean rodents with only the founder pair reproducing, while most of their offspring remain in the parental burrow system and do not breed. Despite of a clear reproductive trade-off, breeders live up to twice as long as non-breeders, a unique feature amongst mammals.
We investigated mass-specific resting metabolic rates (msRMR) of breeders and non-breeders to gain information about the physiological basis underlying the reproduction-associated longevity in Ansell’s mole-rats. We assessed the thermoneutral zone (TNZ) for breeders and non-breeders separately by means of indirect calorimetry. We applied generalized linear mixed-effects models for repeated measurements using the msRMR in the respective TNZs.
TNZ differed between reproductive and non-reproductive Ansell’s mole-rats. Contrary to classical aging models, the shorter-lived non-breeders had significantly lower msRMR within the thermoneutral zone compared to breeders.
This is the first study reporting a positive correlation between msRMR and lifespan based on reproductive status. Our finding contradicts common aging theories, but supports recently introduced models which do not necessarily link reproductive trade-offs to lifespan reduction.
Aging is defined as a gradual decline in intrinsic physiological function leading to an increase in morbidity and mortality rate (reviewed in: ). However, the mechanisms behind aging, i.e. senescence processes are still poorly understood. The disposable soma theory is a prevailing model of aging, which is based on a trade-off between energy demanding processes, including growth, somatic maintenance, and reproduction due to limited resource availability . Reproduction is energetically expensive [3–6], and is often considered a central force shaping different life histories . As soon as an animal starts reproducing, energy resources are allocated to reproduction. Consequently, less energy is available for somatic maintenance and protection, leading to a gradual accumulation of somatic damage. This process is thought to be even amplified, because reproduction increases the metabolic rate to cover the increased energy demand . This increase in metabolic rate is predicted to result in oxygen radicals, i.e. reactive oxygen species (ROS), highly reactive byproducts which cause oxidative damage to DNA, lipids and proteins .
However, high energy turnover does not necessarily increase oxidative damage and mortality. Contrary to earlier expectations, correlational and experimental studies published recently show no negative effect of high metabolic rate on lifespan [9–12], or even a positive association . Moreover, in the brown trout, higher metabolic rates were negatively correlated with levels of H2O2, a highly potent ROS. These controversial associations between metabolic rate and oxidative damage and / or lifespan can in parts be ascribed to different experimental setups and tissues studied (reviewed in: [8, 14, 15]). Moreover, some studies indicate that at least reproductive females have an increased ability to protect from oxidative damage, termed oxidative shielding, in order to protect the offspring from prenatal somatic damage (reviewed in: ). Consequently, more research is needed to gather representative data from animals with different life histories, to gain a comprehensive understanding of how life history trade-offs influence lifespan. Here we present the data of a subterranean mammal with a unique life history to contribute to the discussion stated above.
Ansell’s mole-rats (Fukomys anselli) are subterranean rodents of the family Bathyergidae with an extraordinary long lifespan (22 years being the maximum recorded age thus far; own observations). They live in multigenerational families where typically only the founder pair (breeders) reproduces. Most of the offspring (non-breeders) forego reproduction and remain in the natal family. Incestuous mating (i.e. between brothers and sisters) usually does not occur, however, adult non-breeders readily mate with unrelated conspecifics if given a possibility [16, 17]. A clear contradiction to the classic trade-off model has been shown in this species: breeding individuals live up to twice as long as their non-breeding counterparts, a feature which is unique amongst mammals .
Thus far, proximate factors contributing to this bimodal aging pattern are not known. In contrast to naked mole-rats where reproductive behavior of non-breeders is aggressively suppressed by the mother, Ansell’s mole-rats facilitate incest avoidance by individual recognition. Moreover, they exhibit pronounced sociopositive behaviors like grooming and huddling between all family members . Moreover, previous studies showed that daily activity between breeders and non-breeders does not show differences, and social rank does not influence life expectancy [18, 20, 21]. Hence, extrinsic factors like aggression, fighting and higher workload in non-breeders are not likely to influence the lifespan difference in first-place. Thyroid hormone levels, as a possible intrinsic factor, showed no status-dependent difference, as well .
Here, we test the hypothesis that breeders and non-breeders of Ansell’s mole-rats differ in their mass specific resting metabolic rate (msRMR), as a possible approach to understand the bimodal aging pattern.
Basic parameters and mean mass-specific resting metabolic rate (msRMR) of Fukomys anselli
Body mass (g)
Range of msRMR (ml O2 × g−1 × h−1)
Mean msRMR (ml O2 × g−1 × h−1)
6.9 ± 2.4
83.9 ± 10.5
1.17 ± 0.13
4.8 ± 2.8
108.8 ± 21.4
0.91 ± 0.17
8.9 ± 3.1
87.2 ± 21.8
1.17 ± 0.20
2.4 ± 1.2
68.2 ± 8.9
0.86 ± 0.21
5.8 ± 4.3
85.6 ± 21.4
1.02 ± 0.23
We first determined the thermoneutral zone (TNZ) for both reproductive states by measuring oxygen consumption (VO2) of Ansell’s mole-rats at 13 different ambient temperatures (Ta) ranging between 10 and 40 °C. For non-reproductive individuals the sample size was 14 at temperatures 10, 15, 20, 25, 26, 28, 30, 32, 33, 34, 35, and 37 °C and 11 at 40 °C. For reproductive animals, the sample size was 12 for temperatures 28, 30, 32, and 33 °C and 4 for temperatures 20, 25, 26, 34, 35, and 37 °C. The tested temperatures did not include extremes for reproductive animals in order to avoid impairments of reproductive animals from established colonies due to hypothermia and/or hyperthermia. Especially high temperatures can be critical, as prolonged exposure of Ansell’s mole-rats to ambient temperatures about 42 °C were shown to be potentially lethal (previous own accidental observations).
with: VO2 = oxygen consumption (ml O2 × min−1), Fri = incurrent flow rate (ml × h−1) FiO2 = oxygen incurrent fractional concentration (%), FeO2 = oxygen excurrent fractional concentration. Data gathered by the oxygen sensor were corrected to standard temperature and pressure conditions (273.15 K, 101.325 kPa). The RMR was calculated as a 10-min mean of lowest oxygen consumption and expressed in ml O2 × h−1. msRMR was then calculated as RMR divided by the individual’s weight and expressed in ml O2 × g−1 × h−1.
Critical temperatures and Jonckheere-Terpstra statistical analysis for reproductive and non-reproductive Fukomys anselli
Upper critical temperature
Temperature range /JT/p
Temperature range /JT/p
Lower critical temperature
Temperature range /JT/p
Temperature range /JT/p
To estimate the effects of various predictors on msRMR (dependent variable) within the TNZ boundaries, data were analyzed with generalized linear mixed-effects models for repeated measurements using the lme4 package  and Gamma distribution was assumed (link identity). First, we extended the null model to include one of the independent variables (square-root transformed body mass, ambient temperature as factor, reproductive status) and tested which of them optimally improved the model using the Akaike information criterion and model comparison by χ2-statistic. Subsequently, we extended this model by inclusion of different variables in the same way as described above and we continued until there was no variable left which would significantly improve the model (forward selection). Finally, interaction model of all significant factors was constructed. Individual identity was treated as a random factor. Since the age of some individuals was not known, the same procedure as described above with an additional factor age was applied to all animals with known age. This analysis showed that age is not a significant factor (results not shown). All calculations and statistical analyses were conducted using R 3.0.2 .
Metabolic rate with respect to reproduction
Low msRMR is a common trait in bathyergid rodents interpreted as an ecophysiological adaptation to the subterranean habitat , and our measurements generally confirm previous studies. However, our finding that long-lived breeders of F. anselli have higher metabolic rates compared to shorter-lived non-breeders is novel. The higher metabolic rate observed in breeders is not surprising per se, since reproduction is energy demanding, especially for lactating females [8, 30, 31], albeit none of the reproductive females were pregnant or lactating during the time of measurements. In Damaraland mole-rats, breeding females also live significantly longer than non-breeding females , but no significant differences in msRMR of female breeders and non-breeding individuals were found. However, changes in daily energy expenditure were observed depending on seasonal changes in rainfall . Higher msRMR in breeders compared to non-breeders of F. anselli are in line with findings in pregnant naked mole-rats, another long-lived bathyergid species (>30 years), which have a higher body temperature compared to their non-breeding counterparts . To the best of our knowledge, metabolic data of reproductive naked mole-rats is not available, but higher body temperature suggests a higher metabolic rate. This assumption is also in line with most mammals, where energy intake and/or daily energy expenditure was shown to be increased in lactating females . This aspect is most interesting since investment in reproduction was long thought to impair somatic maintenance according to the classical trade-off model, but recent findings refer to the trade-off model as being too simplistic . Especially in terms of female reproduction, a meta-analysis from different homeothermic vertebrates by Blount et al.  has shown that in intraspecific comparisons between breeders and non-breeders, breeders had lower levels of oxidative damage in certain tissues. This effect could be attributed to upregulation of antioxidant defense mechanisms, such as glutathione or superoxide dismutase activity, which shows a tissue-dependent upregulation in several species during reproduction [36–39]. This oxidative shielding hypothesis, even if not consistent across different studies (reviewed in: ), suggests a reproduction-induced protection of mothers and offspring. Ansell’s mole-rats are continuously reproducing once they achieve the reproductive status. Oxidative shielding might protect the animals from detrimental pregnancy effects due to a higher energy turnover in female breeders compared to non-breeders. However, the bimodal lifespan in Ansell’s mole-rats is not sex-dependent, indicating a general effect in terms of reproductive status, msRMR, and lifespan rather than just a pregnancy effect restricted to females.
The mechanisms underlying the higher msRMR in male Ansell’s mole-rat breeders which do not lactate cannot be derived from the present results. Even so, it could be argued that reproduction in monogamous species includes parental care in male and female, thus it could be that a closer look at monogamous male breeders reveals a higher energy turnover during the reproductive phase as well. Furthermore, breeders are sexually active throughout the year, which could increase the overall msRMR in these individuals.
Higher msRMR in long-lived breeders is not in line with classical aging theories
Oxidative stress as a main factor contributing to life history trade-offs is getting challenged by increasing contradictory studies . Hence, higher msRMR in breeders is in line with those studies, which did not find any correlation  or even support a positive correlation between RMR and lifespan [11, 13, 40–43]. In a large comparative study by de Magalhães et al. , data from 300 mammalian species were analyzed, but after correcting for body mass and phylogeny, no influence of metabolic rate on lifespan, at least in eutherians, could be found. On the other hand, the developmental schedule of a species, i.e. age of sexual maturity and postnatal growth rate, were both correlated with longevity. Mole-rats have a relatively long gestational period of about 3 months (100 days), slow postnatal growth rates, and reach sexual maturity at about 1 year of age [44, 45]. These features are in line with developmental schedule-associated implications reported in de Magalhães et al. . Although these developmental features might account for overall longevity in mole-rats, the distinct intraspecific lifespan difference between breeding and non-breeding Ansell’s mole-rats is still a special case which must be discussed in light of studies that support a positive correlation between msRMR and lifespan .
The uncoupling-to-survive hypothesis  complements simplistic theories of senescence by explaining apparent exceptions. It suggests that elevated oxygen consumption, a measure for msRMR in the present study, could be also observed due to uncoupling of proton flux in the mitochondria. This process, also referred to as inducible proton-leak, is facilitated by uncoupling proteins and increases RMR. On the other hand, inducible proton-leak is known to reduce ROS production by reducing mitochondrial membrane potentials . Hence the higher msRMR measured in breeders of Ansell’s mole-rats could be due to higher rates of mitochondrial uncoupling compared to non-breeders. Several studies found higher rates of uncoupling in those laboratory mice that lived longer compared to other individuals with shorter lifespans [13, 41, 42]. A recent study even showed that mitochondrial H2O2 levels (which is a ROS) were negatively correlated to the metabolic rate in the brown trout . However, in case of mole-rats this model should be considered carefully, since in naked mole-rats, surprisingly high levels of oxidative damage to DNA, lipids and proteins were found, which contrasts with the proposed benefit of mitochondrial uncoupling . Nevertheless, it would be interesting to establish a protocol to investigate mitochondrial ROS in F. anselli in future studies. Mitochondrial uncoupling should be taken into account as a possible proximate mechanism contributing to the bimodal lifespan of F. anselli, but the adaptive background of such a selective protective mechanism on species level is still puzzling. It may be that the upregulation of protective, or in general, repair mechanisms are just a side effect of sexual activity in this species. For instance, long-lasting pair bonding could lead to higher oxytocin levels, known to decrease stress hormones and promote immunity (reviewed in ). Hence, further research should illuminate the linkage between different physiological processes, and how the different processes impacts an animal’s lifespan.
Bathyergid species with their exceptionally long lifespan are already interesting animal models in current aging research, but this is the first study to report a positive correlation between msRMR and lifespan based on reproductive status. The bimodal lifespan of our animal model, the Ansell’s mole-rat, provides an exceptional opportunity to investigate protective mechanisms such as oxidative shielding on species level without the usual shortcomings related to experimental manipulation of the study animals. In general, our finding stresses the complexity of currently discussed aging mechanisms.
We thank João Pedro de Magalhães and two anonymous reviewers for fruitful comments on the manuscript.
Availability of data and materials
The raw data is available at https://www.uni-due.de/imperia/md/images/fb10_bio/allgemeine_zoologie/schielke-et-al_raw-data.xlsx.
SB and HB conceived the project. CKMS performed all metabolic measurements with the help of JO who set-up the equipment. JO, SB and YH evaluated the data and conducted the statistical tests. JO prepared the figures. All authors contributed to the draft and improvement of the manuscript and reviewed the final version. All authors read and approved the final manuscript.
All experiments were approved by the North Rhine-Westphalia State Environment Agency (permit no. AZ: 87-51.04.2010.A359/01) and have been performed in accordance with their guidelines and regulations.
Consent for publication
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