Abstract
Bat biologists have long known about the exceptional longevity of bats (Order: Chiroptera), which is unusual for mammals of such a small size and a high metabolic rate. Yet relatively few mechanistic studies have focused on this longevity. On average, species of Chiroptera live three times longer than predicted by their body size. In addition, bats have other life history traits that are characteristic of large, long-lived mammals such as few and large offspring and slow growth rates. Bats fit the evolutionary theory of ageing, as their extended longevity is predicted by their ability to escape extrinsic mortality through flight and, in some species, hibernation. They also show tradeoffs between longevity and reproduction, as predicted by the disposable soma theory of ageing. From a physiological perspective, bat longevity reportedly correlates with replicative longevity, low brain calpain activity, and reduced reactive oxygen species production. As long-lived and physiologically interesting organisms, bats may prove to be an informative model system for ageing research.
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References
Anthony ELP (1988) Age determination in bats. In: Kunz TH (ed) Ecological and Behavioral Methods for the Study of Bats, pp 47–58. Smithsonian Institution Press, Washington, DC
Armstrong RB, Ianuzzo CD and Kunz TH (1977) Histochemical and Biochemical properties of flight muscle fibers in the little brown bat, Myotis lucifugus. J Comp Physiol B 119: 141–154
Austad SN (1997) Comparative aging and life histories of mammals. Exp Gerontol 32: 23–38
Austad SN and Fischer KE (1991) Mammalian ageing, metabolism and ecology: evidence from the bats and marsupials. J Gerontol 46: B47–B53
Bahr BA, Vanderklish PW, Ha LT, Tin M, KesslerMand Lynch G (1991) Spectrin breakdown products increase with age in telencephalon of mouse brain. Neurosci Lett 131: 237–240
Barclay RMR (1994) Constraints on reproduction by flying vertebrates: energy and calcium. Am Nat 144: 1021–1031
Barclay RMR (1995) Does energy or calcium availability constrain reproduction by bats? Symp Zool Soc Lond 67: 245–258
Barclay RMR and Harder LD (2003) Life histories of bats: life in the slow lane. In: Kunz TH and Fenton MB (eds) Bat Ecology, pp 209–253. University of Chicago Press, Chicago
Barja G (2002) Rate of generation of oxidative stress-related damage and animal longevity. Free Radic Biol Med 33: 1167–1172
Baudry M, DuBrin R, Beasley L, Leon M and Lynch G (1986) Low levels of calpain activity in Chiroptera brain: implications for mechanisms of aging. Neurobiol Aging 7: 255–258
Blasco MA (2003) Mammalian telomeres and telomerase: why they matter for cancer and aging. Eur J Cell Biol 82: 441–446
Bourliere MD (1958) The comparative biology of aging. J Gerontol 13: 16–24
Brunet-Rossinni AK (2004) Reduced free-radical production and extreme longevity in the little brown bat (Myotis lucifi-gus) versus two non-flying mammals. Mech Ageing Dev 125: 11–20
Charlesworth B (1980) Evolution in Age-Structured Populations. Cambridge University Press, Cambridge, United Kingdom
Choi I-H, Cho Y, Oh YK, Jung N-P and Shin H-C (1998) Behavior and muscle performance in heterothermic bats. Physiol Zool 71: 257–266
Corwin JT and Oberholtzer JC (1997) Fish n' chicks: model recipes for hair-cell regeneration? Neuron 19: 951–954
Cristofalo VJ and Pignolo RJ (1995) Cell culture as a model. In: Masoro EJ (ed) Handbook of Physiology Sect 11: Aging, pp 53–82. American Physiological Society, New York
Croall DE and DeMartino GN (1991) Calcium-activated neutral protease (calpain) system: structure, function, and regulation. Physiol Rev 71: 813–847
Davis WH (1970) Hibernation: ecology and physiological ecology. In: Wimsatt WA (ed) Biology of Bats, pp 265–300. Academic Press, Inc., New York
Fenton MB (1982) Ecolocation, insect hearing, and feeding ecology of insectivorous bats. In: Kunz TH (ed) Ecology of Bats, pp 261–285. Plenum Press, New York
Fransen E, Lemkens N, Van Laer L and Van Camp G (2003) Age-related hearing impairment (ARHI): environmental risk factors and genetic prospects. Exp Gerontol 38: 353–359
Harlow H, Lohuis T, Beck T and Iaizzo P (2001) Muscle strength in overwintering bears. Nature 409: 997
Harman D (1956) Aging: a theory based on free radical radiation chemistry. J Gerontol 11: 298–300
Harvey PH and Zammuto RM (1985) Patterns of mortality and age at first reproduction in natural populations of mammals. Nature 315: 319–320
Hayssen V and Kunz TH (1996) Allometry in litter mass in bats: maternal size, wing morphology, and phylogeny. J Mamm 77: 476–490
Hayssen V, van Tienhoven A and van Tienhoven A (1993) Asdell's Patterns of Mammalian Reproduction. Cornell University Press, Ithaca, New York
Heideman PD (2000) Environmental regulation of reproduction. In: Crichton EG and Krutzsch PH (eds) Reproductive Biology of Bats, pp 469–500. Academic Press, London
Herreid CF (1964) Bat longevity and metabolic rate. Exp Gerontol 1: 1–9
Hill JE and Smith JD (1984) Bats: A Natural History. University of Texas Press, Austin, Texas
Hofman MA (1983) Energy metabolism, brain size and longevity in mammals. Q Rev Biol 58: 495–512
Holden CP and Storey KB (1998) Protein kinase A from bat skeletal muscle: a kinetic study of the enzyme from a hibernating mammal. Arch Biochem Biophys 358: 243–250
Holmes DJ and Austad SN (1994) Fly now, die later: life-history correlates of gliding and flying mammals. J Mamm 75: 224–226
Hudson NJ and Franklin CE (2002) Maintaining muscle mass during extended disuse: aestivating frogs as a model species. J Exp Biol 205: 2297–2303
Johnasson BW (1967) Heart and circulation in hibernators. Mammal Hibern 3: 200–218
Jones KE and MacLarnon A (2001) Bat life histories: testing models of mammalian life-history evolution. Evol Ecol Res 3: 465–476
Jürgens KD and Prothero J (1987) Scaling of maximal lifespan in bats. Comp Biochem Physiol A 88: 361–367
Kallen FC (1977) The cardiovascular system of bats: structure and function. In: Wimsatt WA (ed) Biology of Bats, pp 289–483. Academic Press, Inc., New York
Keegan DJ (1977) Aspects of the assimilation of sugars by Rousettus aegyptiacus. Comp Biochem Physiol A 58: 349–352
Kim MH, Park K, Gwag BJ, Jung N-P, Oh YK, Shin H-C and Choi IH (2000) Seasonal biochemical plasticity of a flight muscle in a bat, Murina leucogaster. Comp Biochem Physiol A 126: 245–250
Kirkegaard M and Jørgensen JM (2000) Continuous hair cell turnover in the inner ear vestibular organs of a mammal, the Daubenton's bat (Myotis daubentonii) Naturwissenschaften 87: 83–86
Kirkwood TBL (1977) Evolution of ageing. Nature 270: 301–304
Kirkwood TBL (1996) Human senescence. BioEssays 18: 1009–1016
Kunz TH (1982) Roosting ecology. In: Kunz TH (ed) Ecology of Bats, pp 1–55. Plenum Press, New York
Kunz TH and Lumsden LF (2003) Ecology of cavity and foliage roosting bats. In: Kunz TH and Fenton MB (eds) Bat Ecology, pp 3–89. University of Chicago Press, Chicago
Kunz TH, Whitaker Jr JO and Wadanoli MD (1995) Dietary energetics of the insectivorous Mexican free-tailed bat (Tadarida brasiliensis) during pregnancy and lactation. Oecologia 103: 407–415
Kurta A and Kunz TH (1987) Size of bats at birth and maternal investment during pregnancy. Symp Zool Soc Lond 57: 79–106
Kurta A, Bell GP, Nagy KA and Kunz TH (1989) Energetics of pregnancy and lactation in free-ranging little brown bats (Myotis lucifugus). Physiol Zool 62: 804–818
LeBlanc K, Lehman CT, Macias MY and Thompson JL (1988) Biomechanical problems and recover of long-term hospitalized patients: anti-gravity effect. J Appl Physiol 73: 92–102
Lee M, Choi I and Park K (2002) Activation of stress signaling molecules in bat brain during arousal from hibernation. J Neurochem 82: 867–873
Lollar A and Schmidt-French B (1998) Captive Care and Medical Reference for the Rehabilitation of Insectivorous Bats. Bat World Publications, Mineral Wells, Texas
Luan R and Hanák V (2002) A long-term study of a population of Daubenton's bat Myotis daubentonii. Bat Res News 43: 96
Lyman CP (1970) Thermoregulation and metabolism in bats. In: Wimsatt WA (ed) Biology of Bats, pp 301–330. Academic Press, Inc., New York
Masoro EJ (1996) Possible mechanisms underlying the antiaging actions of caloric restriction. Toxicol Pathol 24: 738–741
Medawar PB (1952) An Unsolved Problem in Biology. H.K. Lewis, London
Menaker M (1964) Frequency of spontaneous arousal from hibernation in bats. Nature 203: 540–541
Michelmore AJ, Keegan DJ and Kramer B (1998) Immunocytochemical identification of endocrine cells in the pancreas of the fruit bat, Rousettus aegyptiacus. General Comp Endocrinol 110: 319–325
Moratelli R, Andrade CM and de Armada JLA (2002) A technique to obtain fibroblast cells from skin biopsies of living bats (Chiroptera) for cytogenetic studies. Gen Mol Res 1: 128–130
Neuweiler G (2000) The Biology of Bats. Oxford University Press, New York
Pauziene N, Pauza DH and Stropus R (2000) Morphological study of the heart innervation of bats Myotis daubentoni and Eptesicus serotinus (Microchiroptera: Vespertilionidae) during hibernation. Eur J Morphol 38: 195–205
Pearl R (1928) The Rate of Living. A.A. Knopf, New York
Pettigrew JD (1986) Flying primates? Megabats have the advanced pathway from eye to midbrain. Science 231: 1304–1306
Pettigrew JD (1994) Genomic evolution: flying DNA. Curr Biol 4: 277–280
Pettigrew JD, Jamieson BGM, Robson SK, Hall LS, McAnally KI and Cooper HM (1989) Phylogenetic relations between microbats, megabats and primates (Mammalia: Chiroptera and Primates). Phil Trans Royal Soc Lond B 325: 489–559
Petri B, Neuweiler G and Pääbo S (1995) Mitochondrial diversity and heteroplasmy in two European populations of the large mouse-eared bat, Myotis myotis. Symp Zool Soc Lond 67: 397–403
Petri B, von Haeseler A, and Pääbo S (1996) Extreme sequence heteroplasmy in bat mitochondrial DNA. Biol Chem 377: 661–667
Promislow DEL and Harvey PH (1990) Living fast and dying young: a comparative analysis of life-history variation among mammals. J Zool Lond 220: 417–437
Promislow DEL and Harvey PH (1991) Mortality rates and the evolution of mammal life histories. Acta Oecol 12: 119–137
Racey PA (1982) Ecology of bat reproduction. In: Kunz TH (ed) Ecology of Bats, pp 57–104. Plenum Press, New York
Racey PA and Speakman JR (1987) The energy costs of pregnancy and lactation in heterothermic bats. Symp Zool Soc Lond 57: 107–125
Rachmatulina IK (1992) Major demographic characteristics of populations of certain bats from Azerbaijan. In: Horacek J and Vohralik V (eds) Prague Studies in Mammalogy, pp 127–141. Charles University Press, Prague
Ransome RD (1995) Earlier breeding shortens life in female greater horseshoe bats. Phil Trans Soc Lond B 350: 153–161
Rasweiler JJ (1977) The care and management of bats as laboratory animals. In: Wimsatt WA (ed) Biology of Bats, pp 519–617. Academic Press, Inc., New York
Read AF and Harvey PH (1989) Life-history differences among the eutherian radiations. J Zool Lond 219: 329–353
Röhme D (1981) Evidence for a relationship between longevity of mammalian species and lifespans of normal fibroblasts in vitro and erythrocytes in vivo. Proc Natl Acad Sci USA 78: 5009–5013
Sacher GA (1959) Relation of lifespan to brain weight and body weight in mammals. Ciba Found Coll 5: 115–141
Sacher GA (1977) Life table modification and life prolongation. In: Finch CE and Hayflick L (eds) Handbook of the Biology of Aging, pp 582–638. Van Nostrand Reinhold, New York
Schuknecht HF and Gacek MR (1993) Cochlear pathology in presbycusis. Ann Otol Rhinol Laryngol 102: 1–16
Simmons NB (2000) Bat phylogeny: an evolutionary context for comparative studies. In: Adams RA and Pedersen SS (eds) Ontogeny, Functional Ecology, and Evolution of Bats, pp 9–58. Cambridge University Press, Cambridge, United Kingdom
Sloane JA, Hinman JD, Lubonia M, Hollander W and Abraham CR (2003) Age-dependent myelin degeneration and proteolysis of oligodendrocyte proteins is associated with the activation of calpain-1 in the rhesus monkey. J Neurochem 84: 157–168
Smith JD and Madkour G (1980) Penial morphology and the question of chiropteran phylogeny. In: Wilson DE and Gardner AL (eds) Proceedings of the Fifth International Bat Research Conference, pp 347–365. Texas Tech Press, Lubbock, Texas
Sohal RS (1986) The rate of living theory: a contemporary interpretation. In: Collatz KG and Sohal RS (eds) Insect Aging: Strategies and Mechanisms, pp 23–44. Springer-Verlag, Berlin
Speakman JR and Thomas DW (2003) Physiological ecology and energetics of bats. In: Kunz TH and Fenton MB (eds) Bat Ecology, pp 209–253. University of Chicago Press, Chicago
St-Pierre J, Buchingham JA, Roebuck SJ and Brand MD (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem 277: 44784–44790
Studier EH and O'Farrell MM (1972) Biology of Myotis thysanodes and M. lucifugus (Chiroptera: Vespertilionidae). I. Thermoregulation. Comp Biochem Physiol A 41: 567–595
Thomas SP (1987) The physiology of bat flight. In: Fenton MN, Racey P and Rayner JMV (eds) Recent Advances in the Study of Bats, pp 75–99. Cambridge University Press, Cambridge, United Kingdom
Thomas SP and Suthers RA (1972) The physiology and energetics of bat flight. J Exp Biol 57: 317–335
Tinker D, Harlow H and Beck T (1998) Protein use and muscle fiber changes in free ranging, hibernating black bears. Physiol Zool 71: 414–424
Tuttle MD and Stevenson D (1982) Growth and survival of bats. In: Kunz TH (ed) Ecology of Bats, pp 105–150. Plenum Press, New York
Vanderklish PW and Bahr BA (2000) The pathogenic activation of calpain: a marker and madiator of cellular toxicity and disease states. Int J Exp Path 81: 323–339
Van den Busche RA, Baker RJ, Huelsenbeck JP and Hillis DM (1998) Base compositional bias and phylogenetic analyses: a test of the 'flying DNA' hypothesis. Mol Phylogen and Evol 10: 408–416
Van der Westhuyzen J (1976) The feeding pattern of the fruit bat Rousettus aegyptiacus. S. Afr J Med Sci 41: 271–278
Wickler S, Hoyt D and Breukelen FV (1991) Disuse atrophy in the hibernating golden mantled ground squirrel, Spermophilus lateralis. Am J Physiol 261: R1214–R1217
Widmaier EP, Gornstein ER, Hennessey JL, Bloss JM, Greenberg JA and Kunz TH (1996) High plasma cholesterol, but low triglycerides and plaque-free arteries, in Mexican free-tailed bats. Am J Physiol 271(Regulatory Integrative Comp Physiol 40): R1101–R1106
Wilkinson GS and Chapman A (1991) Length and sequence variation in evening bat D-loop mtDNA. Genetics 128: 607–617
Wilkinson GS, Mayer F, Kerth G and Petri B (1997) Evolution of repeated sequence arrays in the D-loop region of bat mitochondrial DNA. Genetics 146: 1035–1048
Wilkinson GS and South JM (2002) Life history, ecology and longevity in bats. Aging Cell 1: 124–131
Williams GC (1957) Pleiotropy, natural selection and the evolution of senescence. Evolution 11: 398–411
Wilson, DE (1988) Maintaining bats for captive studies. In: Kunz TH (ed) Ecological and Behavioral Methods for the Study of Bats, pp 247–263
Yacoe ME (1983) Protein metabolism in the pectoralis muscle and liver of hibernating bats, Eptesicus fuscus. J Comp Physiol 152: 137–144)
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Brunet-Rossinni, A.K., Austad, S.N. Ageing Studies on Bats: A Review. Biogerontology 5, 211–222 (2004). https://doi.org/10.1023/B:BGEN.0000038022.65024.d8
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DOI: https://doi.org/10.1023/B:BGEN.0000038022.65024.d8