Birds as long-lived animal models for the study of aging
Section snippets
Introduction: why use birds for aging studies?
Useful animal models for the study of aging should ideally meet one or more of three criteria: (1) specificity, the ability to directly address a particular research question or hypothesis; (2) generalizability, the extent to which findings can be applied to a range of animal species; and (3) feasibility, which includes such logistical considerations as costs and husbandry requirements for maintaining a given species or strain once criteria (1) or (2) have been met (Holmes and Austad, 1995a,
Bird are long-lived despite high lifetime energy expenditures
Birds belong to the class Aves, which consists of approximately 9000 species with a wide range of body sizes, life histories and aging patterns (Sibley and Monroe, 1990, Sibley and Monroe, 1993, Gill, 1995, Bennett and Owens, 2002). Most birds live longer (up to three times) than mammals of equivalent body mass. Even small hummingbirds and migratory songbirds often survive over five years in the wild. Some wild seabirds live over 50 years; many captive parrots enjoy life spans in excess of 75
Avian longevity is consistent with evolutionary predictions
Based on the robust positive correlation in warm-blooded vertebrates between body size and longevity, and an equally strong inverse association between life spans and metabolic rates, past zoologists hypothesized that life spans and aging rates in homeotherms were constrained by the ‘rate of living’ (Pearl, 1928, Rose, 1991). This generalization is clearly refuted, however, by the disproportionately long life spans of flying birds and bats (compared with non-flying members of their respective
Birds may have special adaptations for combating free-radical damage and glycosylation
Selection for prolonged somatic maintenance means longer life spans and slower aging. Although the mechanisms whereby organism accomplish this at the metabolic or cellular level are still unclear, there is growing evidence that slow aging is associated with lower production of ROS per molecule of oxygen consumed, or more effective defenses against oxidative damage to biological molecules leading to the accumulated morbidity from pathologies of aging. The diseases associated with senescence are
Most bird species exhibit slow to negligible age-related reproductive declines
The delayed aging typical of birds extends to slow reproductive aging in both sexes (for reviews, see Holmes et al., 2003, Holmes, 2003). Mouse-sized domestic birds like budgerigars and canaries have reproductive life spans up to five times as long as rats and mice (4–5 years, vs. 1 or 2); the 110-g American Kestrel (maximum recorded life span over 10 years) shows little reproductive aging for up to 7 years or so. In captivity under hospitable conditions, birds generally enjoy postreproductive
Caloric restriction improves reproductive performance in poultry
The aging-retarding effects of caloric restriction (CR) are a well-established paradigm in biogerontology (see Barger et al., this volume), and seem to apply to a broad range of animal taxa, including invertebrates as well as vertebrates. Reliable effects of CR typically include extended life span, delayed onset of aging-related diseases, sustained healthy metabolic and endocrine function, and delayed loss of reproductive capacity (for reviews, see Weindruch and Walford, 1988, Finch, 1990,
Avian telomeres are surprisingly long, but not clearly implicated in longevity or slow aging
There has been a great deal of interest recently in a possible relationship between telomere length and maximum life span in vertebrates, including birds, as well as aging-related changes in telomeric DNA sequences in tissues of individual animals. Telomeres, which are conserved nucleotide sequences essential for replication of linear chromosomes, have been shown to shorten with age in somatic cells of humans, and are implicated in cellular senescence in mice (Harley, 1995). Thus far, however,
Birds in the laboratory: likely candidates and special considerations
The best candidate species as avian laboratory models in most cases are small, domesticated birds in several different orders, for which husbandry practices are well established and maintenance costs nearly as economical as for laboratory rodents (for an earlier review of these and other considerations, see Austad, 1997) (Table 4). They include short-lived species, like the Japanese quail (maximum life span 6 years), and several popular pet species, like the budgerigar (a small parrot), and the
Acknowledgements
D. Holmes acknowledges the support of Biomedical Research Infrastructure (BRIN) grant P20RR16454-01 (National Institutes of Health) to the University of Idaho during the preparation of this paper. M.A. Ottinger acknowledges National Science Foundation grant #9817024.
References (89)
- et al.
A decrease in free radical production near critical targets as a cause of maximum longevity in animals
Comp. Biochem. Physiol. Biochem. Mol. Biol.
(1994) - et al.
H2O2 production of heart mitochondria and aging rate are slower in canaries and parakeets than in mice: sites of free radical generation and mechanisms involved
Mech. Aging Dev.
(1998) - et al.
Comparative biology of aging in birds: an update
Exp. Gerontol.
(2001) - et al.
Reproductive aging in female birds
Exp. Gerontol.
(2003) - et al.
Normobaric hyperoxic stress in budgerigars: non-enzymic antioxidants
Comp. Biochem. Physiol., Part C
(2001) - et al.
The effects of age at photostimulation and dietary protein intake on reproductive efficiency in three strains of broiler breeders varying in breast yield
Poult. Sci.
(2002) - et al.
Effect of dietary calcium stress on plasma vitamin D3 metabolites in the egg-laying Japanese quail
Poultry Sci.
(1985) - et al.
Comparison of mitochondrial prooxidant generation and antioxidant defenses between rat and pigeon: possible basis of variation in longevity and metabolic potential
Mech. Age. Dev.
(1993) - et al.
Effects of feed restriction during the rearing period and age at photostimulation on the reproductive performance of turkey hens
Poult. Sci.
(1990) - et al.
Neuroendocrine involvement in aging: evidence from studies of reproductive aging and caloric restriction
Neurobiol. Aging
(1995)
Endocrine patterns during aging in the Common Tern (Sterna hirundo)
Gen. Comp. Endocrinol.
Quail and other short-lived birds
Exp. Gerontol.
Low fatty acid unsaturation protects against lipid peroxidation in liver mitochondria from long-lived species: the pigeon and human case
Mech. Age Dev.
A low degree of fatty acid unsaturation leads to lower lipid peroxidation and lipoxidation-derived protein modification in heart mitochondria of the longevous pigeon than in the short-lived rat
Mech. Age. Dev.
The use of feed restriction for improving reproductive traits in male-line large white turkey hens. 1. Growth and carcass characteristics
Poult. Sci.
Ganglion cell and hair cell loss in Coturnix quail associated with aging
Hear Res.
Hair cell regeneration in senescent quail
Hear Res.
TEM analysis of neural terminals on autoradiographically identified regenerated hair cells
Hear Res.
Effects of dietary energy on semen production, fertility, plasma testosterone, and carcass composition of broiler-breeder males in cages
Poult. Sci.
Effects of feeding program and crude protein intake during rearing on fertility of broiler breeder females
Poult. Sci.
The effects of nutrient dilution on the well-being and performance of female broiler breeders
Poult. Sci.
The comparative perspective and choice of animal models in aging research
Aging Clin. Exp. Res.
Birds as models of aging in biomedical research
ILAR J.
Mammalian aging, metabolism, and ecology: evidence from the bats and marsupials
J. Gerontol. Biol. Sci.
Evolutionary approaches to probing aging mechanisms
Mitochondrial free radical production and aging in mammals and birds
Ann. NY Acad. Sci.
Localization at complex I and mechanism of the higher free radical production of brain nonsynaptic mitochondria in the short-lived rat than in the longevous pigeon
J. Bioenerg. Biomembr.
Low mitochondrial free radical production per unit O2 consumption can explain the simultaneous presence of high longevity and high aerobic metabolic rate in birds
Free Rad. Res.
Evolutionary Ecology of Birds. Life Histories, Mating Systems and Extinction
Expression and regulation of Fas antigen and tumor necrosis factor receptor type I in hen granulosa cells
Biol. Reprod.
Mammalian Reproductive Biology
Severe vs. moderate restrictions of feed intake: Effects of body weight, egg production, energetic efficiency and male development of broiler breeders
Proceedings of XVII-World's Poultry Congress
Longevity Records: Life Spans of Mammals, Birds, Amphibians, Reptiles, and Fish
Hypothesis: Glucose as a mediator of aging
J. Am. Geriatr. Soc.
Effects of aging and mate retention on reproductive success of captive female peregrine falcons
Am. Zool.
Organization of telomere sequences in birds: evidence for arrays of extreme length and for in vivo shortening
Cytogenet. Cell Genet.
An approach to free radicals in medicine and biology
Acta Physiol. Scand.
Challenges for brain repair: insights from adult neurogenesis in birds and mammals
Brain Behav. Evol.
Evolution of senescence and specific longevity
Nature
Longevity, Senescence, and the Genome
Basal metabolic rate, thermoregulation and existence energy in birds: world data
Telomeres and aging
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