Aging Research on Bats

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Few studies have examined bat longevity, and due to continually improving lifespan data, it is not surprising that some of these studies have reached contradictory conclusions. Some of the earliest work that considered the question of why bats live so long was a comparative survey of lifespans by Bourliere (1958). Addressing the question from the standpoint of the rate of living theory (Pearl, 1928; Sacher, 1959), Bourliere described the extreme longevity of bats as a simple consequence of reduced metabolism during hibernation. This explanation, of course, neglects the long lifespan of homeothermic bats, which do not hibernate. In fact, Herreid (1964) and Austad and Fischer (1991) found no difference in maximum lifespan between hibernating and tropical bats. Jurgens and Prothero (1987) found that after accounting for torpor and hibernation, lifetime energy consumption and body mass predict maximum lifespan reasonably well in hibernating species, but fail to do so in nonhibernating species. The most recent survey study on bat longevity, which included an extensively updated dataset, found that the average longevity of hibernating species is about 6 years longer than that of nonhibernating species (Wilkinson and South, 2002).

Hibernation does appear to contribute to lifespan extension by concealing bats from predators, protecting them from inclement weather, and retarding physiological deterioration (Barclay and Harder, 2003). However, it does not account for the fact that all known bat longevity records exceed those of similar sized nonflying mammals, including those that hibernate (Austad and Fischer, 1991). In its original formulation, the rate of living theory predicts the existence of a constant mass-specific lifetime energy expenditure for all mammals (Sacher, 1959). Bats exceed the lifetime energy expenditure of nonflying placental mammals by two-fold (Austad and Fischer, 1991), contradicting the rate of living theory. Another formulation of the rate of living theory describes an inverse correlation between maximum lifespan and metabolic rate or body size. Austad and Fischer (1991) calculated that on average bats live over three times longer than expected based on body size, again contradicting the rate of living theory. There is ambiguous evidence regarding a possible correlation between body mass and longevity within the order Chiroptera. Two studies found no correlation (Austad and Fischer, 1991; Jones and MacLarnon, 2001), yet a third found a correlation when using a phylogentic analysis method which accounts for relationships among the species analyzed (Wilkinson and South, 2002).

From an evolutionary perspective, the exceptional longevity of bats is consistent with the evolutionary theory and the disposable soma theory of aging. The evolutionary theory of aging attributes senescence to the decreasing strength of natural selection with increasing age (Williams, 1957). This predicts that organisms that excel at escaping extrinsic mortality such as starvation, predation, disease, and accidents evolve to be long lived. Bats have terrestrial and aerial predators (e.g., snakes, opossums, owls, hawks) and are vulnerable to climate; however, the exposure is low relative to nonflying mammals. Like birds, which also exhibit exceptionally long lifespan, bats are able to escape predation by flying, and many species will migrate or adjust body temperature and metabolic rate to avoid adverse food and weather conditions (Wilkinson and South, 2002; Barclay and Harder, 2003).

The disposable soma theory of aging describes an inevitable evolutionary tradeoff between using limited resources and energy for somatic maintenance or to increase reproductive output (Kirkwood, 1977). An organism that experiences high extrinsic mortality is likely to die prior to the next reproductive season and would do well to invest in high and quick reproductive output instead of in somatic maintenance. The opposite would be true for an organism that experiences low extrinsic mortality as it can spread out reproductive output over a longer lifespan. Bat species with high reproductive rates and early sexual maturation exhibit shorter longevity (Rachmatulina, 1992; Wilkinson and South, 2002). Even within a species, females who delay breeding to a later age have higher survival rates than females who breed early in life (Ransome, 1995).

Very little is known about the physiological and molecular mechanisms underpinning the exceptional longevity of bats. Rohme (1981) included a bat (Vespertilio murinus) in a comparative study, which found a positive correlation between organism maximum lifespan and replicative lifespan of fibroblasts cultured from eight mammalian species. The involvement of cellular replica-tive lifespan in aging is still disputed (Cristofalo and Pignolo, 1995), and several laboratories are in the process of evaluating this correlation using fibroblast cell cultures from other species of bats (Brunet-Rossinni and Austad, 2004).

Baudry et al. (1986) examined a potential correlation between calpain activity and species maximum lifespan. The calpains are a family of calcium-dependent cystein proteases that have been implicated in age-related pathologies of kidneys, heart, and brain tissue deterioration, as calpain activity increases with age likely due to impaired inhibitory mechanisms. Based on a negative correlation between calpain activity and brain size, and a positive correlation between brain size and maximum longevity, Baudry et al. hypothesized that brain calpain activity should be inversely correlated with maximum longevity. By quantifying degraded proteins in the presence of calcium, the study compared calpain activity in brain tissues of two bat species to that of mice and found significantly lower calpain activity in the bat tissues. It should be noted, however, that bat brain size is not consistent with the reputed correlation between lifespan and brain size.

A more recent study tested the free radical theory of aging (Harman, 1956) as an explanation for the extreme longevity of bats. In a comparative study, Brunet-Rossinni (2004) measured mitochondrial hydrogen peroxide production in heart, kidney and brain tissue of the little brown bat, Myotis lucifugus, the short-tailed shrew, Blarina brevicauda, and the white-footed mouse, Pero-myscus leucopus. Hydrogen peroxide production per unit of oxygen consumed was significantly lower in the bat tissues than in the two nonflying mammals. Brunet-Rossinni also measured activity of superoxide dismutase, a key enzyme in the antioxidant defense system of mammalian tissues. Activity of this enzyme did not differ between the three species. Though not an all-inclusive assessment of antioxidant defenses, this study suggests that free radical production is a better predictor of bat longevity than metabolic rate and antioxidant activity. Similar results have been found in birds and other mammals (Herrero and Barja, 1998; Ku, et al., 1993).

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