Sci. Aging Knowl. Environ., 29 May 2002
Vol. 2002, Issue 21, p. pe7
[DOI: 10.1126/sageke.2002.21.pe7]

PERSPECTIVES

The Naked Mole Rat--A New Record for the Oldest Living Rodent

Rochelle Buffenstein, and Jennifer U. M. Jarvis

R. Buffenstein is in the Department of Biology at the City College of the City University of New York, New York, NY 10031, USA. J. U. M. Jarvis is in the Department of Zoology at the University of Cape Town, Private Bag, Rondebosch, Cape Town, 7700 South Africa. E-mail: rbuffen{at}sci.ccny.cuny.edu (R.B.)

http://sageke.sciencemag.org/cgi/content/full/sageke;2002/21/pe7

Key Words: naked mole rat • longevity record • rodent longevity • theories of aging

Introduction

Animals with slow rates of aging are distinctive in that they generally exhibit very little decline in physiological capacity, reproduction rate, or disease resistance as they get older (1-3). Furthermore, animals that exhibit delayed senescence typically live longer than other species of comparable body mass. They therefore represent outlier points on allometric curves, which describe the relationship between maximum life-span and body mass (4). To date, most allometric data on maximal life-span for vertebrates are derived from zoological records and descriptions of captive animals. Although life in captivity is fraught with its own suite of physiologically stressful situations, captive care removes many compounding factors that affect survival in the wild (such as predation, exposure to environmental extremes, and restricted availability of water and nutrients). Thus, the maximal life-spans of captive animals probably reflect inherited ancestral genetic traits of the species (phylogenetic traits) that in turn affect basic cellular processes of aging, rather than mortality induced by external factors (5). Here we describe a male naked mole rat that lived for more than 28 years, primarily in captivity. This life-span represents a new record for rodent longevity.

The Naked Mole Rat and Slow Aging

Naked mole rats (order Rodentia, family Bathyergidae, Heterocephalus glaber) are mouse-sized (about 35 g) rodents that are found only in the hot, dry tropical regions of northeast Africa. The naked mole rat described in this Perspective was collected near Mtito Andei, Kenya, in July/August 1974 and weighed 26 g at that time. In captivity, animals attain an adult mass (>30 g) at about 12 months of age. Naked mole rats weighing 26 g in captivity--where food is provided ad libitum and the energy cost of burrowing is minimal--are about 6 to 12 months old (6). Accordingly, this male was at least 28 years and 2 months old when he died in April 2002. Given the high metabolic cost of locating food underground in an arid environment, it is probable that this animal was smaller at the time of collection than he would have been had he been born and raised in captivity. It is therefore likely that he was at least 6 to 12 months older than the extrapolated minimum captive age. Thus, his life-span surpassed the previous longevity record for a rodent, which was held by a porcupine [Hystrix brachyura, weighing about 11 kg (7)] that lived for 27 years and 4 months (8). This slow rate of aging by a naked mole rat is especially impressive given the relatively small body size of this species (0.002 times that of porcupines and other long-lived rodents).

Throughout the animal kingdom, maximal life-span is proportional to body mass (4), so that large animals live longer than small animals (an observation that applies when different species but not varieties within species are compared to each other). The ratio of observed maximum longevity to that predicted by the animal's body mass is known as the longevity quotient of a species (3). The longevity quotient of naked mole rats is approximately 10, making this indicator one of the highest mammalian values recorded [Fig. 1 and (3, 4)].



View larger version (8K):
[in this window]
[in a new window]
 
Fig. 1. Maximum life-span and longevity quotients for selected rodents based on the allometric equation for predicted life-span [life-span (years) = 5.3 (mass in kg)0.174]. Both maximal life-span and the longevity quotient of naked mole rats are considerably greater than those of rodents (8) commonly used in research on aging.

 
Although our >28-year-old individual appeared frail for the last 6 months of his extraordinary life-span (Fig. 2 and Fig. 3), within the last 2 months of his life he mated successfully. This observation indicates that his reproductive fitness had not declined with age, in contrast to what has been observed for other mammals, such as mice. Like this wild-caught 28-year-old breeding male, females also remain reproductively active well into their old age, although fecundity declines (9). To date, the oldest breeding female in our care was 26 years old when she died. The oldest breeding female to raise pups successfully was 23 years and 8 months when she died, 1 month after producing more than 20 pups and raising two of these offspring. Successful mating at such a late stage in life is comparatively rare in mammals.



View larger version (118K):
[in this window]
[in a new window]
 
Fig. 2. The oldest living rodent at age 27 years and 10 months. Note the light colored, parchment-like skin. [Photograph taken by T.P. O'Connor.]

 


View larger version (94K):
[in this window]
[in a new window]
 
Fig. 3. Naked mole rats show visible signs of aging. The animal on the left is 15 years old, whereas the one on right is the 28-year-old male described here, 3 days before he died. Note the darker coloration of the younger mole rat on the left and the parchment-like, less-elastic skin of the 28-year-old male on the right. [Photograph taken by R. Buffenstein]

 
Other features commonly associated with aging in rodents, such as decreased food consumption, decreased metabolic rate, and changes in body composition, have not been observed in elderly naked mole rats (10). Like most aged mammals, however, older naked mole rats are not as active as younger individuals. Older naked mole rats can also be differentiated on sight from younger animals (Fig. 2 and Fig. 4). Their skin is much lighter, thinner, and less elastic than that of younger individuals (Fig. 4); the skin of our oldest individual resembled parchment (Fig. 2 and Fig. 3).



View larger version (67K):
[in this window]
[in a new window]
 
Fig. 4. A six-year-old naked mole rat. Note her darker skin coloration and "younger" looking skin. [Photograph taken by R. Buffenstein]

 
Naked Mole Rats and Theories of Aging

Why do these small rodents live so long? The ecology, physiology, and behavior of naked mole rats, considered within the context of the evolutionary theory of aging (11), the longevity extension theory of social species (12), and the environmentally selected life-span theory (12), provide insight into this question.

Naked mole rats lead a strictly subterranean existence, feeding on roots and tubers (13). Furthermore, these rodents are eusocial in that they live cooperatively in large colonies of up to 300 individuals (14). They exhibit a division of labor that culminates in the presence of a single breeding female. Several litters of different ages are present at one time within the colony (14). The offspring receive extended care, not only from the breeding female who nurses them for about 1 month but also from other members of the colony. These members collect food and carry it to the nest for the offspring. They also feed the young their nutrient-rich feces (15). Most of the offspring continue to live in the colony until they die, although a few individuals, regarded as dispersomorph castes, might leave the colony of their birth to form new colonies (16). Mice and other solitary subterranean mammals, on the other hand, leave the nest shortly after weaning.

The evolutionary theory of aging

The evolutionary theory of aging proposes that aging is the result of the declining power of natural selection to favor advantageous alleles or eliminate deleterious alleles whose phenotypes become evident after sexual maturity (see "Aging Research Grows Up" and Williams Classic Paper). In support of this theory, rates of aging have been found to be directly correlated with extrinsic mortality, so that animals with high extrinsic mortality, which results from living in a dangerous environment, tend to have intrinsically short life-spans. According to the theory, such animals will undergo only weak selection for the maintenance of physiological function as they age, resulting in shorter life-spans, and will evolve life-history traits that facilitate early reproduction. The converse is also predicted to be true: Species that live in safe environments are expected to evolve traits that allow extended periods of reproduction and longer life-spans (3, 11). The life history of naked mole rats supports this theory; their risks of extrinsic mortality are low, and their life-spans are ~10 times longer than that predicted by mass (Fig. 1). These animals lead a protected existence in deep, thermally buffered underground burrows, where they are sheltered from climatic extremes and safeguarded against predation by raptors and mammalian carnivores. Additionally, they are protected against snakes by cooperative defense, whereby several individuals work together to attack an intruder in their burrow system (13).

Longevity extension theory of social species

Extended longevity in naked mole rats might also be an evolved life-history trait that results from living socially in family units (12). Eusociality has evolved independently in several invertebrate groups as well as in the subterranean African mole rat family (17, 18). Both the eusocial insects and naked mole rats have a single breeding female in a colony and exhibit extended longevity. Indeed, termite queens reportedly have maximal life-spans similar to those of naked mole rats [~30 years (12)]. The cost of reproduction is carried by only a few individuals, and most members of a colony are nonreproductive genetically related siblings that bear the brunt of foraging costs. The transfer of genes to the next generation is thus limited to a single breeding female. However, living socially in family units with several overlapping litters and cooperative care of the young enhances the degree to which a beneficial genetic trait is passed from generation to generation by the relatives of individuals (the kin) who express these traits. As such, an individual's fitness (that is, the success of its own genes in the next generation) is not based only on its own reproductive success, but also on all of the effects it has on enhancing the reproductive fitness of relatives that are breeding (a process known as inclusive fitness of kin selection)(18). For example, although a sterile drone in a bee colony clearly has zero personal fitness, its inclusive fitness (the impact it has on ensuring its genes survive) can actually be relatively high, if it devotes its life to providing for its relatives in the beehive (18). These features of kin selection, which are evident in both the eusocial insects and naked mole rats, promote mutually beneficial cooperation that is advantageous to both relatives and the individual itself. Such characteristics contribute to the model of socially induced longevity extension by increasing the survival of both young and reproductively active animals through extended care and complex social behavior.

The environmentally selected life-span theory

The environmentally selected life-span theory posits that animals that live in unpredictable environments where food is sometimes scarce, resource availability is unpredictable, and the location of food is energetically costly will exhibit extended longevity, primarily because of the low metabolic rates exhibited by such animals (12). Again, the life history of naked mole rats supports this hypothesis, because their underground food supply consists of clumped roots and tubers that are unevenly distributed because of unpredictable patchy rainfall (13, 15). Location of food in this dark environment is a blind and energetically costly process, in which animals rely primarily on smell and touch rather than vision (15, 19). Adaptive responses to this irregular food supply that enhance survival include the following: (i) living in large groups that forage cooperatively, (ii) an extremely low resting metabolic rate and basal energy expenditure, and (iii) high digestive efficiencies that maximally extract available nutrients (15). Low metabolic rates might in turn contribute to prolonged longevity by decreasing the amount of accrued oxidative damage within the organism [(2); also see "The Two Faces of Oxygen"].

None of these longevity-oriented theories are mutually exclusive, and no doubt all describe mechanisms that contribute to the extraordinary longevity of this small rodent. The underlying physiological processes that enable the attainment of this exceptional longevity in long-lived species such as the naked mole rat remain unknown and are currently under investigation. Given their extraordinary longevity, naked mole rats are likely to provide useful insights into the biology of aging. Specifically, a 28-year-old naked mole rat will expend approximately seven times more energy (1550 kcal/g) over a lifetime than will similar-sized mice (230 kcal/g). This lifetime energy expenditure is among the highest values known for any mammal (3), suggesting that naked mole rats use cellular mechanisms to reduce the accrual of metabolically induced cellular damage. Genome sequencing and the identification of genes that are differentially expressed relative to other mammalian models of aging will provide useful insights into cellular and physiological mechanisms that are involved in both aging and the retardation thereof. The naked mole rat is therefore a useful animal model for aging research (see Warner Perspective).

May 29, 2002

  1. C. E. Finch, Longevity, Senescence and the Genome (Univ. of Chicago Press, Chicago, IL, 1990).
  2. R. E. Ricklefs, Evolutionary theories of aging: confirmation of a fundamental prediction, with implications for the genetic basis and evolution of life span. Am. Nat. 152, 24-44 (1998).
  3. S. N. Austad, Why We Age: What Science Is Discovering about the Body's Journey Through Life (Wiley, New York, 1997).
  4. J. Prothero, K. D. Jurgens, Scaling of maximal life span in mammals: a review. Basic Life Sci. 42, 49-74 (1987).[Medline]
  5. R. A. Miller, Kleemeier Award Lecture: Are there genes for aging? J. Gerontol. A Biol. Sci. Med. Sci. 54, B297-B307 (1999).[Medline]
  6. J. O'Riain, J. U. M. Jarvis, The dynamics of growth in naked mole-rats--the effects of litter order and changes in social structure. J. Zool. 246, 49-60 (1998). [CrossRef]
  7. S. B. Parker, Grzimek's Encylopedia of Mammals, vol. 4 (McGraw-Hill, New York, 1990).
  8. J. R. Carey, D. S. Judge, Longevity records: life spans of mammals, birds, amphibians, reptiles and fish. Odense Univ. Monogr. Popul. Aging 8, 1-241 (2000).
  9. P. W. Sherman, J. U. M. Jarvis, Extraordinary life spans of naked mole-rats (Heterocephalus glaber). J. Zool., in press.
  10. T. P. O'Connor, A. Lee, J. U. M. Jarvis, R. Buffenstein, Prolonged longevity in naked mole-rats: Age-related changes in metabolism, body composition and gastrointestinal function. Comp. Biochem. Physiol., in press.
  11. M. R. Rose, Evolutionary Biology of Aging (Oxford Univ. Press, Oxford, 1991).
  12. J. R. Carey, D. S. Judge, Life span extension in humans is self-reinforcing: a general theory of longevity. Popul. Dev. Rev. 27, 411-436 (2001).[CrossRef]
  13. R. A. Brett, in The Biology of the Naked Mole-Rat, P. W. Sherman, J. U. M. Jarvis, R. D. Alexander, Eds. (Princeton Univ. Press, Princeton, NJ, 1991), pp. 137-184.
  14. J. U. M. Jarvis, Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212, 571-573 (1981).[Abstract/Free Full Text]
  15. R. Buffenstein, in The Biology of Subterranean Rodents, E. Lacey, J. Patton, G. Cameron, Eds. (Univ. of Chicago Press, Chicago, IL, 2000), pp. 62-110.
  16. M. J. O'Riain, J. U. M. Jarvis, R. Alexander, R. Buffenstein, C. Peeters, Morphological castes in a vertebrate. Proc. Natl. Acad. Sci. U.S.A. 97, 13194-13197 (2000).[Abstract/Free Full Text]
  17. R. D. Alexander, K. M. Noonan, B. J. Crespi, in The Biology of the Naked Mole-Rat, P. W. Sherman, J. U. M. Jarvis, R. D. Alexander, Eds. (Princeton Univ. Press, Princeton, NJ, 1991), pp. 3-44.
  18. E. O. Wilson, Sociobiology, The New Synthesis (Harvard Univ. Press, Cambridge, MA, 2000).
  19. B. G. Lovegrove, The cost of burrowing by the social mole-rats (Bathyergidae) Cryptomys damarensis and Heterocephalus glaber: The role of soil moisture. Physiol. Zool. 62, 449-469 (1989).




THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Naked mole-rat transcriptome signatures of socially-suppressed sexual maturation and links of reproduction to aging.
M. Bens, K. Szafranski, S. Holtze, A. Sahm, M. Groth, H. A. Kestler, T. B. Hildebrandt, and M. Platzer (2019)
bioRxiv
   Abstract »    Full Text »    PDF »
Matrilineal Transmission of Familial Excess Longevity (mtFEL): Effects on Cause-specific Mortality in Utah, 1904 - 2002.
E. OBrien, R. M. Cawthon, K. R. Smith, and R. A. Kerber (2019)
bioRxiv
   Abstract »    Full Text »    PDF »
Hypersensitivity to contact inhibition provides a clue to cancer resistance of naked mole-rat.
A. Seluanov, C. Hine, J. Azpurua, M. Feigenson, M. Bozzella, Z. Mao, K. C. Catania, and V. Gorbunova (2009)
PNAS 106, 19352-19357
   Abstract »    Full Text »    PDF »
How to learn new and interesting things from model systems based on "exotic" biological species.
J. M. Sedivy (2009)
PNAS 106, 19207-19208
   Full Text »    PDF »
Protein stability and resistance to oxidative stress are determinants of longevity in the longest-living rodent, the naked mole-rat.
V. I. Perez, R. Buffenstein, V. Masamsetti, S. Leonard, A. B. Salmon, J. Mele, B. Andziak, T. Yang, Y. Edrey, B. Friguet, et al. (2009)
PNAS 106, 3059-3064
   Abstract »    Full Text »    PDF »




Science of Aging Knowledge Environment. ISSN 1539-6150