Avian Models Of Extremely Slow To Negligible Reproductive Aging

Patterns of reproductive aging vary even more widely among birds than among mammals studied to date. As predicted by evolutionary aging and life-history theory, the slower aging of birds relative to mammals is generally reflected in slower reproductive aging in birds of both sexes (for reviews, see Holmes et al., 2003; Holmes and Ottinger, 2003; 2004). Bird species that mature and reproduce extremely slowly, including seabirds (e.g., albatrosses, terns, and gulls) and large raptors (e.g., condors), tend also to be among the longest-lived, with some species holding longevity records of 50 years or more.

Even shorter-lived wild birds exhibit much slower aging than mammals of equivalent body size. Many small (under 50 grams) passerine songbirds have average life spans of over several years in the wild, and exhibit steady declines in reproductive aging. Reproductive declines in these birds are often more than twice as slow as those of similar-sized captive rodents (McCleery and Perrins, 1988; Newton, 1989; Gustafsson and Part, 1991; Clum, 1995; Newton and Rothery, 1997). For example, the rat-sized (110 g) American Kestrel (maximum recorded life span of over 10 years), a small raptor, shows little reproductive aging for up to 7 years or so.

Wild seabirds, including gulls, albatrosses, fulmars and terns, typically exhibit little or no loss of reproductive fitness even at the end of their natural life spans in nature (>50 yrs for some fulmars), and even when rising mortality rates suggest significant deterioration of other physiological systems. Since few seabirds have been maintained in captivity, it remains unclear how long the postreproductive life spans might be for these species if their natural life spans could be prolonged in captivity. Terns (order Charadriiformes), for example, have an extreme life-history strategy typical of pelagic seabirds, characterized by slow sexual maturation, low lifelong reproduction rates (2-3 chicks fledged per year), long life spans, and very slight to negligible declines in reproductive success after peak fledging success is reached at about 15 yrs (Nisbet et al., 1999; Nisbet, 2002a,b). This kind of very sustained reproductive investment is thought to have evolved only in animal populations with extremely low adult mortality rates (<10 percent per year). The extremely slow to negligible aging typical of seabirds is rare in wild bird or mammal populations, and its physiological basis merits additional study.

Long-lived animals with exceptionally slow reproductive aging likely have physiological or molecular mechanisms for prolonging fertility, and basic reproductive aging processes may differ significantly between long- and short-lived species (Finch, 1990; Austad, 1993; Martin et al., 1996; Austad and Holmes, 1999; vom Saal et al., 1994). With the exception of primates, however, few long-lived animal models have been developed for exploring basic mechanisms of delayed fertility loss. Studies of the physiological correlates of avian reproductive aging have largely been limited to short-lived poultry species (for exceptions, see Clum, 1995; Ottinger et al., 1995; Nisbet et al., 1999, 2002a). We have emphasized the potential of wild bird populations for studies of exceptionally slow—or even negligible—reproductive aging under natural conditions in earlier reviews (Holmes et al., 2003; Holmes and Ottinger, 2003).

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