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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
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• Mammals
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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
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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). A well-integrated,
synthetic biology of aging—a real "evolutionary gerontology" (sensu Rose, 1991)—
ideally will include collaboration between
field and laboratory zoologists, life history
theorists and biologists, and a more synthetic understanding of the complex interplay among evolutionary and physiological
mechanisms in biology as a whole.
ACKNOWLEDGMENTS
This work was supported by grant AG11534 from the National Institutes of
Health.
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