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AMER. ZOOL., 35:307-317 (1995) The Evolution of Avian Senescence Patterns: Implications for Understanding Primary Aging Processes1 DONNA J. HOLMES AND STEVEN N. AUSTAD Department of Biological Sciences, University of Idaho, Moscow, Idaho 83843 The long life spans of birds relative to those of mammals are intriguing to biogerontologists, particularly in light of birds' high body temperatures, high blood glucose levels, and high metabolic rates—all of which should theoretically increase their biochemical liability for rapid aging. The comparative longevity of birds and other flying homeotherms is consistent with evolutionary senescence theory, which posits that species with low mortality rates from predation or accident will be released from selection for rapid maturity and early reproduction, and will exhibit retarded aging. Comparative analyses of avian life history parameters to date, although not as extensive as those for mammals, broadly support an association between low mortality rates, slow reproduction, and long lifespan. The diversity of bird life histories suggests the importance of developing a diversity of avian models for studies of aging mechanisms, both proximate and ultimate, and for using wild as well as domestic representatives. Birds studied in the laboratory thus far show many of the same manifestations of aging as mammals, including humans, and many ornithologists are beginning to document actuarial evidence consistent with aging in their study populations. We encourage greater communication and collaboration among comparative gerontologists and ornithologists, in the hope that the study of aging in birds will lead to an integrated understanding of physiological aging processes well grounded in an evolutionary paradigm. SYNOPSIS. tion and glycation of proteins and nucleic (Monnier, 1990; Monnier et al., 1991; The class Aves, comprised of some 9,000 species, is characterized by diverse life his- H o l m e s and Austad, 1995). The exceptional tones and patterns of reproduction. As a longevity of birds as a group suggests they group, however, birds are very long-lived have evolved special mechanisms to protect for their body size relative to mammals. a g a i n s t m o r e r a P i d a&in& t h e comparative This is particularly remarkable to gerontol- evidence is largely consistent with the idea ogists and other students of comparative t h a t t h i s lorf™y is associated with the vertebrate life spans. Since birds have much adaptation offlight,and the ability to escape higher metabolic rates and body tempera- mortality from predation and accident, In man tures, on average, than mammals, as well y o f the , longest-lived bird species, ate as higher levels of blood glucose, theoreti- l maturity and delayed reproduction precally they should sustain proportionately cede slow aging. Although aging in wild accelerated damage from processes hypoth- populations remains to be studied intenesized to be responsible for the physiolog- sively, birds in general represent a wealth ical deterioration which characterizes o f m o d e l s y stem! > f o r understanding the senescence-including free-radical genera- evolution of retarded aging, including that of reproductive systems, and the primary physiological correlates of senescence and longevity. In 'FromtteSymposiumReproductiveAginginAvian * « r e V * W ' W e h ° P e t 0 ^ ^P .^ t h e INTRODUCTION acids 5^c/«Presentedatthe2istlnternationalOrnithology groundwork for a well-integrated avian Congress, Vienna, Austria in August, 1994. biogerontology combining proximate and 307 308 D. J. HOLMES AND S. N. AUSTAD ultimate perspectives on the study of senescence. We begin by recalling the prediction, from evolutionary senescence theory, that flightedness should promote the evolution of long life span and slow aging in homeothermic vertebrates. Second, we summarize comparative evidence gathered to date addressing this prediction. A third section is devoted to what is actually known now about avian aging processes. The fourth briefly introduces ornithologists to physiological processes hypothesized by experimental gerontologists to be responsible for senescence in vertebrates, and the possible relevance of these to avian aging. Fifth and last, we suggest ways in which ornithology can contribute to a comprehensive comparative biology of aging, or "evolutionary gerontology." THE EVOLUTIONARY PERSPECTIVE ON FLIGHT, AGING, AND LONGEVITY Some tenets of senescence theory Senescence can be denned as age-related physiological changes adversely affecting an organism's fitness and reproduction, and increasing its risk of mortality (Finch, 1990; Rose, 1991). Evolutionary senescence theory includes as its central tenet the idea that age-specific schedules of reproduction and mortality—including mortality attributable to senescence—are shaped by natural selection (Williams, 1957; Hamilton, 1966; Charlesworth, 1980; Rose, 1991; Partridge and Barton, 1993). Two mechanisms for the evolution of senescence are particularly relevant to the discussion of avian aging. The first is antagonistic pleiotropy, in which senescence evolves when traits advantageous to organisms relatively early in life (such as those promoting reproductive success) are favored by natural selection despite deleterious effects later on (Williams, 1957). The second mechanism is mutation accumulation. Since natural selection ultimately can only act on characters affecting reproduction, the power of selection against deleterious genes wanes as organisms age and become postreproductive, allowing for the accumulation of harmful mutations (Haldane, 1941; Medawar, 1952; Partridge and Barton, 1993). The expression of these genes is posited as another way in which senescence could be manifest in animals in nature. Flight and the evolution of longevity Senescence theory predicts that, all else being equal, stable populations of organisms subject to high mortality rates from predation or accident will evolve life histories characterized by high fecundity, short life spans, and relatively rapid aging (Medawar, 1952; Williams, 1957; Edney and Gill, 1967; Charlesworth, 1980; Partridge and Barton, 1993). On the other hand, organisms protected from such hazards should be characterized by slower reproduction, longer life spans, and delayed senescence. Nearly 40 years ago Williams (1957), followed later by Charlesworth (1980, 1990), suggested that the evolution of flight, which presumably protects birds from mortality, accounts in large part for the apparently slow aging in this class relative to non-flying homeotherms. He noted succinctly that one of the critical tests of senescence theory would be empirical comparison of aging rates in flightless versus flying birds and mammals. COMPARATIVE EVIDENCE OF ASSOCIATIONS BETWEEN FLIGHT, LOW MORTALITY RATES, SLOW AGING AND SLOW REPRODUCTION Comparative analyses are largely consistent with Williams' prediction of a correlation between flight, low mortality rates, and longevity in warm-blooded vertebrates. These include comparisons of 1) maximum recorded longevities (MRLs) for birds and mammals of equivalent body mass; 2) MRLs for flying, weakly flying, and non-flying members of each of the two classes; 3) mortality schedules forflyingand non-flying bird and mammal species, and the differential in extinction rates between them; and 4) comparative analyses (both within and between classes) of life history traits in birds and mammals. The comparative approach cannot explain all of the diversity in life span and aging patterns in homeotherms, nor can it be used to make predictions about future evolutionary events. These limitations—and the pos- 309 EVOLUTION OF AVIAN SENESCENCE sibility that common ancestry or evolutionary accident, rather than natural selection, may actually account for some components of the patterns seen—have been discussed thoroughly elsewhere (Harvey and Pagel, 1991; Rose, 1991; Promislow, 1991, 1993; Promislow and Tatar, 1994). Nonetheless, evolutionary aging theory, while it may not account fully for existing patterns, is falsifiable using a comparative approach (see Rose, 1991). More importantly here, the detection of broad taxonomic patterns in aging, including those consistent with antagonistic pleiotropy, are heuristically valuable for identifying useful model organisms for studying proximate, physiological aging processes, either rapid or delayed (Nesse, 1988; Austad, 1993; Holmes and Austad, 1995). Maximum recorded longevities (MRLs) for avian and mammalian fliers and non-fliers MRLs are generally accepted by gerontologists and zoologists as a useful parameter for comparing animal longevities and aging patterns (Comfort, 1979; Finch, 1990; Austad and Fischer, 1991,1992; Rose, 1991; but see Promislow, 1993 for caveats). Ideally, maximum life span serves as an index of the physiological capacity of an organism to resist aging (MRLs, however, reveal nothing about how rates of senescence may vary among species, or how longevities vary among conspecifics). MRLs have been used most often in the analysis of allometric relationships in birds and mammals, particularly relationships between body mass, metabolic rates, and life span (see, for example, Sacher, 1959; Lindstedt and Calder, 1976; Calder, 1984, 1985; Austad and Fischer, 1991). MRLs of wild birds average 1.7 times greater than MRLs of captive mammals, and captive birds on the whole outlive captive mammals by a factor of three (Fig. 1) (Lindstedt and Calder, 1976; Austad and Fischer, 1991; Holmes and Austad, 1995). This difference in life span potential is true despite the fact that birds have metabolic rates and lifetime energy expenditures 2 to 2.5 times those of mammals of similar body size (Welty, 1982; Schmidt-Nielsen, 1990; 1.5 °° °q> o ° o 1.0 CO 0.5 * . " • • . • ' : O Birds • Mammals nn i -3 -2 -1 i < 0 Log Body Mass (kg) FIG. 1. Comparison of regressions of maximum recorded longevity (MRL) on body mass for birds and mammals. For birds, log longevity = 1.23 + 0.19 log mass (adjusted R2 = 0.40; n = 238); for mammals, log longevity = 1.01 + 0.15 log mass (adjusted R2 = 0.40; n = 290). Note that most MRLs available for birds are derived from mark-recapture data on wild populations, and are underestimates of maximum potential life span, while most mammal MRLs come from records of captive longevities. Data sources: Flower, 1931; Anonymous, 1960;Crandall, 1964; Altman and Dittmer, 1972; Altman and Kirmayer, 1976; Haltenorth and Diller, 1977; Clapp et ah, 1982, 1983; Jones, 1982; Welty, 1982; Klimkiewicz et al, 1983; Nowak and Paradiso, 1983; MacDonald, 1985; Fowler, 1986; KJimkiewicz andFutcher, 1987,1989;Perrins, 1990; plus additional primary and secondary literature. Holmes and Austad, 1995). Parenthetically, analysis of the variation in the relationship between body mass and MRL within the class Mammalia has shown that volant mammals, the bats, have life spans averaging three times longer than those of other mammals (Jiirgens and Prothero, 1987; Austad and Fischer, 1991; note that these analyses controlled for body size, but not for phylogeny). This difference is not limited to bat species which undergo torpor. The apparent longevity benefit offlightholds for mammalian gliders, too: of nine glider species from five different orders, all are longer-lived than the average life span predicted for non-volant eutherian mammals of equivalent body size (Austad and Fischer, 1991; Holmes and Austad, 1994). Some parrots (order Psittaciformes), 310 D. J. HOLMES AND S. N. AUSTAD which as a group have the longest absolute avian life spans, have captive life spans recorded reliably at over 90 years (e.g., Ara spp. macaws); this is more than four times the longevity predicted by their body masses. Conversely, the shortest-lived bird for its body mass is the coturnix quail, with an average life span of less than a year in the wild, and a captive MRL of 7 to 8 yr. (Note that this is still a longer life span in captivity than that of a rodent of similar size, or around 90 grams.) Short life span in this bird is coupled with rapid, early reproduction and fast aging (Woodard and Abplanalp, 1971; Ottinger et ai, 1983; Puigcerver et al., 1992). Other species much shorterlived than predicted by the average avian MRL-to-body-mass relationship include other weakly flighted galliforms: the wild turkey, for example, has an MRL of 12.5 years—only half the life span predicted by its average body mass. High fecundity in these species is coupled with precociality. MRL analysis provides many examples of bird species for which an apparent positive association between life span and flight proficiency is accompanied by delayed maturity and sustained, slow reproduction as predicted by senescence theory (Holmes and Austad, 1995 and unpublished data). Long-lived pelagic seabirds—despite the fact that there are few long-term demographic studies conducted on them—already have documented MRLs of over 50 years, many with body weights below 10 kg. Albatrosses, fulmars, shearwaters, and other seabirds typically develop slowly, delay reproductive maturity, and lay very small clutches (one egg each at intervals of several years). Some seabirds reproduce for decades with no detectable reproductive decline (Ollasen and punnet, 1988;Ricklefs, 1990). The longestlived birds of all for their body size are hummingbirds, which also reproduce very slowly (note, however, that hummingbirds may exhibit torpor characterized by lowered metabolic rates for significant portions of their life spans). Calder (1990) has reported life spans of over 12 yr. for a 3.5-gram Broadtailed Hummingbird, and 14 yr. for a Planalto Hermit. The latter MRL is almost 2.3 times the predicted life span for a bird of its body weight. Flight proficiency, including such key parameters as wing loading and takeoff time, is a difficult variable to assess, and undoubtedly not the only thing shaping avian life histories and aging rates. It may, however, account for a significant portion of the variability among avian MRLs, particularly if it can be demonstrated to be inversely correlated with mortality rates. More importantly here, species on the extremes of the longevity/flight agility continuum are particularly interesting candidates for gerontological research. Mortality rates of homeotherm fliers vs. non-fliers In a reasonably well-conceived comparative analysis, Pomeroy (1990) showed that average annual adult mortality rates of bats were significantly lower than those of either non-flying mammals or terrestrial birds (but see Promislow, 1991). Mortality rates for penguins were significantly higher than those of other aquatic but flighted birds, and comparable to those of Eurasian land birds. Other bird groups exhibiting lower mortality rates than predicted by body mass in their respective biogeographic regions included the swifts (order Apodiformes), which obviously have remarkable speed and aerial agility. Pomeroy noted also that evolutionary forces other than flight ability undoubtedly impinge on species-specific mortality rates: these include climate, phylogeny, diet, gender, and life history traits other than mortality schedules. Flightless birds occur primarily as part of relict faunas on islands with uncommonly low predator densities. Their extinction rates suggest correspondingly high susceptibility to extrinsic mortality: although they comprise less than one percent of all birds, fully one-third of avian species which have become extinct over the last 400 years have been flightless. The ability to fly may decrease vulnerability to introduced predators, as well as enhancing the ability to exploit new habitats in the event of catastrophic environmental change (Line, 1994; Steadman, 1995). Other factors notwithstanding, comparative analyses of this type, coupled with MRL analysis, generally support the pre- 311 EVOLUTION OF AVIAN SENESCENCE diction that flight influences mortality rates in homeotherms—and that flying and gliding, as well as other adaptations for predator avoidance, may have played a significant role in the evolution of life span variability among vertebrates. We emphasize this possibility not because we see it as an exclusive ultimate explanation for variation in longevities, senescence patterns, and other life history traits seen in nature, but because mortality as a powerful selective force is so often neglected in discussions of avian life history evolution, even though it is a pivotal parameter in senescence and life history theory. By emphasizing the possible influence of flight on the evolution of avian aging patterns, we in no way deny the importance of phylogeny or physiological constraints which undoubtedly (albeit to an unknown degree) contribute to the variation we see (Gaillard etai, 1989; Finch, 1990; Finch et al., 1990; a/., 1994). Do comparative life history analyses for birds support senescence theory? Comparative analyses exploring the relationships among multiple avian life history traits—particularly those among adult mortality rates, fecundity, and life span—have not been conducted as rigorously or extensively as for those of mammals. However, there is clear support for the kind of "slowfast" continuum (Harvey and Zammuto, 1990; Promislow and Harvey, 1991 of life history traits in birds similar to that demonstrated for mammals, and for an inverse relationship between fecundity and longevity (various avian taxa: Western and Ssemakula, 1982; Gaillard et al., 1989; passerines: Montgomerie and Lyon, 1986; gamebirds: Zammuto, 1986). The relationship between mortality rates, fecundity, and life span (either average or maximum) remains to be thoroughly explored for an appropriately large avian database. In some species for which adequate data exist, however, the relationship between changes in mortality and declining fecundity with age is quite striking (e.g., for the Great Tit)(Fig. 2), suggesting good wild bird models for exploring actual genetic and physiological trade-offs between reproduction and longevity. -1 1 1 .5 03 "I E5 # •'"' .3 " • • . . • .1 O - . 1 • • Fecundity *•••-._ o- - o Mortality . O -.3 _ -O c -.5 Q' o- ^ ~o -.7 o- ^ ^ " °~ / 1 Age (yr) FIG. 2. Comparison of changes in mortality and fecundity rates with age in Great Tits. Mortality data are from over 3,000 banded breeding adults of known age, males and females combined. Fecundity data represent numbers of offspring recruited to the reproductive population by breeding pairs for which ages of both parents are known. Data from McCleery and Perrins, 1988. CURRENT KNOWLEDGE ABOUT AVIAN AGING Avian diseases of aging Despite long-standing belief to the contrary (Nice, 1943; Lack, 1954; Williams, 1992), birds really do age—they just usually do it more slowly than mammals of comparable size. Little research to date has focused on avian aging directly. In captive birds however, including wild species in zoos as well as cage birds and domestic fowl, the pathologies and ensuing mortality from physiological senescence are observed readily and are well documented in the veterinary literature. Avian diseases of aging are generally similar to those seen in mammals, and include atherosclerosis, neoplasms including cancers, senile ocular cataracts, biochemical alterations in collagen and other connective tissues, and reproductive changes, including neoplasms, malignancies, and endocrinological deficiencies (Finch, 1990; Holmes and Austad, 1995). Diabetes has long been recognized by gerontologists as a useful physiological mimic of some aspects of aging, producing very similar types of deterioration; it too is well documented for birds (Altman and Kirmayer, 1976; Lewandowski, 1986), and represents a useful tool for studying the effects of hyperglycemia on 312 D. J. HOLMES AND S. N. AUSTAD "aging-like" disease processes in vertebrates. There is much variation, even among birds with similar life spans and body masses, in the types of age-related disease reported. Arterial lesions, although not systematically or quantitatively surveyed in wild birds, have been reported most frequently in avian carnivores collected in nature (Scheidegger, 1959). A review of pathological lesions recorded in a sizable veterinary clinical database (courtesy of Purdue University School of Veterinary Medicine) revealed an incidence of neoplasms in budgies (weight 30 g; MRL 20 yr.) as much as six times higher than that in canaries (weight 20-25 g; MRL 24 yr.), with even relatively young budgies affected. Domesticated birds—poultry species and pigeons, most notably—have been used successfully to model cardiovascular disease (Mitrukaera/., 1976;Morrisseyetfa/., 1977; Andrews et al., 1979) and reproductive aging. Senescence of the reproductive tract and its hormonal and neurobiological correlates have been studied much more thoroughly than other components of avian aging. Chickens and quail have been employed as the primary avian laboratory models to date (see, for example, Ottinger, 1991; Ottinger era/., 1983, 1995; Bahr and Palmer, 1989; Palmer and Bahr, 1992). Although reproductive declines with age are now also reported for a number of wild birds (for reviews, see Newton, 1989; Saether, 1990; Finch, 1990; vom Saal et al, 1994; Holmes and Austad, 1995; Ottinger et al, 1995), the study of physiological correlates of reproductive senescence in wild bird populations is really in its infancy. The elegant work of Ottinger, Bahr, and others should serve as model approaches for the study of aging and reproduction in a greater diversity of bird species with a fuller range of life spans and life history patterns. Evidence of aging in wild bird populations Evidence of aging in wild mammal and bird populations is necessarily more indirect than that for birds in captivity, and has thus far consisted mostly of actuarial analyses or anecdote. Even longitudinal demo- graphic data obtained using mark-recapture or band return data are, of course, of variable reliability. Actuarial data and analyses, however, continue to improve in quality as well as quantity, and data on long-term reproductive success are becoming available for many species (see, for example, Newton, 1989)(Fig. 2). The old idea that animals die before showing signs of aging in nature (Comfort, 1979; Slobodkin, 1966; Botkin and Miller, 1974; Williams, 1992) has been challenged successfully for mammals (Promislow, 1991; Gaillard et al., 1994), and will probably prove untrue for birds, as well. Fitness declines associated with aging should be manifest in increases in age-specific mortality for birds in stable populations (Botkin and Miller, 1974;Nesse, 1988; Newton, 1989). Many ornithologists have reported increases in adult mortality with age in their study populations (Botkin and Miller, 1974; Loery et al., 1987; Newton, 1989; Aebischer and Coulson, 1990; Calder, 1990; Dann and Cullen, 1990; Finch, 1990; Gustafsson and Part, 1991; Davies, 1992; McDonald et al., unpublished ms.; Wiebe and Martin, unpublished ms.). In a preliminary analysis of 59 avian life tables available from the ornithological literature conforming to specific standards for methodological rigor, 80% showed detectable increases in adult mortality over the life span, and 25% showed a statistically reliable fit to a Gompertz {i.e., linear regression) model for increasing mortality after sexual maturity (Holmes, Austad, and Peppercorn, unpublished data). Additionally, some field ornithologists report obvious signs of gross physical aging in the birds they study (Holmes and Austad, 1995). Comparative demographic data for birds and mammals have already made an enormous contribution to our understanding of the evolution of life span and other life history phenomena. This type of evidence has unavoidable limitations, however, and will always represent circumstantial evidence of the relationship betweenflight,long life span, and slow aging. A particularly important limitation to this approach is that it fails to distinguish between extrinsic causes of death {i.e., those attributable to predation, "acci- EVOLUTION OF AVIAN SENESCENCE dent," or other components of an organism's external environment, including those which hasten aging) and intrinsic mortality factors (i.e., those which are genetically determined and attributable to internal characteristics of the individual itself, including senescent physiological decline) (Medawar, 1952; Edney and Gill, 1968; Promislow, 1991; Abrams, 1993; Gaillard et al., 1994), or to consider complex interactions between them. To evaluate evolutionary hypotheses about senescence in birds and mammals more explicitly—particularly the hypothesis of antagonistic pleiotropy— and to discriminate between extrinsic and intrinsic sources of mortality, we need extensive information on physiological aging processes in diverse representatives of both classes, and particularly in those species representing the full range of flight proficiency, life span, and fecundity. Only in this way can we hope to dissect the relationships among proximate and ultimate mechanisms of aging, and to identify the real sources of mortality and evolutionary basis for life history patterns we see. 313 the generation of highly reactive oxygen radicals during normal metabolic processes (Harman, 1956; Del Maestro, 1980). These free radicals are potentially damaging to a wide range of biological molecules. The importance of radical damage is illustrated by the elaborate cellular defense system evolved to combat its effects, involving scavenging enzymes, antioxidant enzymes, and metal-chelating proteins. If the accumulated damage from oxidative processes is indeed involved in aging processes, birds—with their high metabolic rates and body temperatures—should be especially vulnerable to such damage. Assuming that lifetime energy expenditure per cell is a good rough index of oxidative burden, a 20-g mouse that lives three years experiences about one-twentieth the oxidative burden of a 20-g canary that lives 20 yr. That the long lives of birds have evolved despite this oxidative liability suggests they have mechanisms either to reduce the rate of oxidant production per unit of energy expended, or that they have exquisitely effective antioxidant defenses. Recent work comparing pigeons and rats (with compaGERONTOLOGY FOR ORNITHOLOGISTS: rable body masses and metabolic rates) sugWORKING HYPOTHESES FOR THE gests both reduced oxidant generation and STUDY OF VERTEBRATE AGING more effective defenses on the part of the No single process or mechanism thus far pigeon (Ku and Sohal, 1993; Barja et al, proposed is sufficient to explain all aspects 1994). The study of avian oxidative sysof aging in animals, including humans, and tems, however, has yet to begin in earnest. A second biochemical process hypothefew experimental interventions have been shown to reliably alter the process. Rather sized currently to be important in mediating than being unitary in nature, senescence aging is the Maillard reaction, a complex seems to be characterized by a number of series of nonenzymatic interactions between separate but intricately related physiologi- reducing sugars (such as glucose) and any cal mechanisms (Finch, 1990; Rose, 1991). molecules with free amino groups, includThat diseases of aging are manifold, and ing proteins and nucleic acids (Cerami, 1985; probably influenced by multiple gene loci, Lee and Cerami, 1990; Monnier, 1990; is consistent with evolutionary senescence Monnier et al, 1991). This process protheory (Rose, 1991; etc.), as is the synchro- duces a suite of products collectively referred nous deterioration of diverse and appar- to as "advanced glycation end-products" ently unconnected physiological systems in (AGEs) thought to be involved in molecular cross-linking, and hence the inhibition of aging animals. protein function and the potential for mutagenic alteration of nucleic acids. More Glycation, free-radical damage, and recently, free-radical formation and AGEs synergistic primary aging processes There are several relatively ubiquitous have been suggested to act synergistically biochemical processes now hypothesized by (Kristal and Yu, 1992): that is, glycation gerontologists to be involved in diverse products, in principle, can promote the genaspects of aging. The best known of these is eration of cellular free radicals and simul- 314 D. J. HOLMES AND S. N. AUSTAD taneously inhibit antioxidant defenses. In any case, the rate of AGE formation should be roughly proportional to the concentration of reducing sugars and the heat of the reaction; this presents a special biochemical dilemma for birds. Their exceptional longevity suggests exceptional defenses against glycation-induced damage, as against freeradical damage, but the nature of these adaptations, as well, remains unknown. In sum, it stands to reason that birds— particularly the longest-lived species with the highest metabolic rates—have evolved very effective anti-aging mechanisms. The detailed, comparative study of avian cellular protective mechanisms is likely to yield major insights into basic biochemical aging processes and, quite possibly, into effective mechanisms for slowing or reducing the damage they produce. ORNITHOLOGY MEETS GERONTOLOGY: FUTURE RESEARCH DIRECTIONS This is a watershed time for the comparative biology of aging. Biogerontologists are showing renewed interest in an evolutionary paradigm for understanding senescence, but are often unaware of the diversity of life history patterns seen in animals in nature. Concurrently, there is rapid growth in avian physiological ecology, with a special focus on reproductive endocrinology. Ornithologists are now in a position to make invaluable contributions to the understanding of the ultimate, or evolutionary, as well as proximate, or physiological, mechanisms underlying the variety of life spans and patterns of senescence in animals. We have discussed elsewhere how pet domestic bird species could be adopted as experimental animals for the laboratory study of aging under controlled conditions of altered diet and reproduction (Holmes and Austad, 1995). We need intensified, theoretically integrated study of the physiology of aging in a range of captive birds, including those with long life spans and apparently slow aging, in wild as well as captive representatives, and including species (e.g., zebra finches) in which reproduction can be manipulated and the relationship between hormonal and other reproductive costs and aging explored. We should study the closest wild relatives of domesticated species used most intensively in physiological (and, particularly, endocrinological) research to date—the jungle fowl, for example, as an adjunct to research on domestic chickens—to better understand the effects of domestication and breeding for early, rapid egg production on reproductive aging. Ten questions for avian gerontology Some of the most intriguing, but as yet intractable, questions about senescence, its evolution, physiological mechanisms and manifestations, and the relationship between aging and central questions in behavioral ecology may soon become practical subjects of study. Some of the most obvious of these which could conceivably be addressed using avian models include the following: 1) How do mortality patterns—in captive and wild birds both—reflect the onset of and morbidity associated with measurable physiological senescence? 2) To what extent does variation in fitness attributable to senescence contribute to individual differences in fitness in a given population overall? 3) In practical terms, precisely how can "extrinsic" and "intrinsic" sources of mortality be teased apart using physiological aging measures? 4) Does the physiology of aging differ qualitatively, or merely quantitatively, between short-lived, rapidly aging species (e.g., Coturnix quail) and significantly longer-lived species? 5) Is early fecundity associated, as a rule, with early, rapid physiological aging? 6) Is there clear, physiological evidence for antagonistic pleiotropy in birds —that is, are genes for early reproduction the same as those which cause physiological decline later in life? 7) Is reproductive senescence correlated with overall physiological senescence? 8) If so, does this correlation hold in various avian species, or do some (e.g., long-lived, slowly-aging seabirds) show different relationships between these phenomena? 9) Do individuals with greater lifetime reproductive success age more quickly, or are they more resistant to aging? 10) Are certain social systems (e.g., cooperative parental care systems) or ecological correlates particularly conducive to the evolution of retarded aging? EVOLUTION OF AVIAN SENESCENCE Aging processes in wild bird populations can now be explored cooperatively by physiological gerontologists and field biologists with long-term demographic data. If reliable assays or "biomarkers" of aging can be developed within populations, these might in turn be adapted for quantifying costs of reproduction and other physiological tradeoffs related to the evolution of life history strategies in general, as well as aging in particular. The proceedings of this workshop are evidence that this process is beginning. Others have already argued for this kind of interdisciplinary dialectic (Finch, 1990; Rose, 1991; Austad, 1993). 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