The hypoxia tolerance of eight related African mole‐rat species rivals that of naked mole‐rats, despite divergent ventilatory and metabolic strategies in severe hypoxia

Abstract

Aims Burrowing mammals tend to be more hypoxia tolerant than non‐burrowing mammals and rely less on increases in ventilation and more on decreases in metabolic rate to tolerate hypoxia. Naked mole‐rats (Heterocephalus glaber, NMRs), eusocial mammals that live in large colonies, are among the most hypoxia‐tolerant mammals, and rely almost solely on decreases in metabolism with little change in ventilation during hypoxia. We hypothesized that the remarkable hypoxia tolerance of NMRs is an evolutionarily conserved trait derived from repeated exposure to severe hypoxia owing to their burrow environment and eusocial colony organization. Methods We used whole‐body plethysmography and indirect calorimetry to measure the hypoxic ventilatory and metabolic responses of eight mole‐rat species closely related to the NMR. Results We found that all eight species examined had a strong tolerance to hypoxia, with most species tolerating 3 kPa O2, Heliophobius emini tolerating 2 kPa O2 and Bathyergus suillus tolerating 5 kPa O2. All species examined employed a combination of increases in ventilation and decreases in metabolism in hypoxia, a response midway between that of the NMR and that of other fossorial species (larger ventilatory responses, lesser reductions in metabolism). We found that eusociality is not fundamental to the physiological response to hypoxia of NMRs as Fukomys damarensis, another eusocial species, was among this group. Conclusions Our data suggest that, while the NMR is unique in the pattern of their physiological response to hypoxia, eight closely related mole‐rat species share the ability to tolerate hypoxia like the current “hypoxia‐tolerant champion,” the NMR.

Naked mole-rat and Damaraland mole-rat exhibit lower respiration in mitochondria, cellular and organismal levels

“…The comparison between these two mole-rats species and other subterranean rodents, other partial fossorial mole-rat species, also shows a reduced BMR by more than 29% [38]. The observed lower BMR might be explained by their fully fossorial lifestyle and eusocial colony organization which likely results in repeated exposure to severe hypoxia [18]. Interestingly, while age-related declines in BMR in disease-free individuals are extensively documented feature in human and laboratory rodent species [57,58], we observed no detectable age-related declines in body mass (Mb) and BMR in DMR or the NMR [41].…”

“…Such observations directly challenge the most prominent life-history trade-off, the cost of reproduction at the expense of somatic maintenance resulting in a negative association between reproductive output and longevity [17]. More impressively, besides their extreme longevity and high reproductive output, both these species also share other characteristics such as hypoxia tolerance [18] and tolerance of oxidative stress [19], features considered evolved traits in response to life below ground for millenia [20]. In spite of the similarities of these exceptional life history traits within this monophyletic clade [21], NMR and DMR exhibit fundamental differences in their evolutionary history: studies suggest they evolved eusociality independently [22,23], and have divergent physiological responses to different stressors [23].…”

The brains of six African mole-rat species show divergent responses to hypoxia

“…Free radicals are also produced upon reoxygenation. However, several mole-rat species such as Spalax galili and Heterocephalus glaber are resistant to decreases in oxygen tension (Larson and Park, 2009;Schülke et al, 2012;Shams et al, 2004), and other species of African mole-rats (Bathyergidae) may also show hypoxia tolerance (Ivy et al, 2020).…”

Environment and exposure

“…Eusocial burrowing animals need hypoxia tolerance to suit their lifestyle preferences. 24 Lastly, Olson et al found that cellular H 2 S is increased during extended hypoxia, probably functioning as a continuously active O 2 -sensing mechanism in several cells. 25 Protection from detrimental environmental influences has, without doubt, contributed to modern man living longer and healthier lives than ever before in human history.…”

“…Insufficient oxygen availability is, however, not exclusively a pathological phenomenon. Eusocial burrowing animals need hypoxia tolerance to suit their lifestyle preferences 24 . Lastly, Olson et al found that cellular H 2 S is increased during extended hypoxia, probably functioning as a continuously active O 2 ‐sensing mechanism in several cells 25 …”