Hypotheses of aging in a long-lived vertebrate, Blanding's turtle (Emydoidea blandingii)

Congdon, Justin D.; Nagle, Roy D.; Kinney, Owen M.; Sels, Richard C. van Loben

doi:10.1016/s0531-5565(00)00242-4

Cited by 156 publications

(100 citation statements)

References 18 publications

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“…Our analysis is similar to the former of these approaches, and we indeed document reproductive decline with advancing age, although not in measures traditionally used (such as rates of conception) but rather by calculating egghatching success. Similarly, Congdon et al (24) reported greater embryo mortality attributable to arrested development in eggs produced by the oldest female age class in Blanding's turtles. Other long-lived species tend to exhibit reproductive senescence at rates that are faster than somatic aging and that ends at an earlier age than death, which yields a postreproductive lifespan [primates including humans (16), killer whales (41), but see elephants (42,43)].…”

Section: Discussionmentioning

confidence: 92%

Decades of field data reveal that turtles senesce in the wild

Warner

Miller

Bronikowski

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Lifespan and aging rates vary considerably across taxa; thus, understanding the factors that lead to this variation is a primary goal in biology and has ramifications for understanding constraints and flexibility in human aging. Theory predicts that senescence-declining reproduction and increasing mortality with advancing age-evolves when selection against harmful mutations is weaker at old ages relative to young ages or when selection favors pleiotropic alleles with beneficial effects early in life despite late-life costs. However, in many long-lived ectotherms, selection is expected to remain strong at old ages because reproductive output typically increases with age, which may lead to the evolution of slow or even negligible senescence. We show that, contrary to current thinking, both reproduction and survival decline with adult age in the painted turtle, Chrysemys picta, based on data spanning >20 y from a wild population. Older females, despite relatively high reproductive output, produced eggs with reduced hatching success. Additionally, age-specific mark-recapture analyses revealed increasing mortality with advancing adult age. These findings of reproductive and mortality senescence challenge the contention that chelonians do not age and more generally provide evidence of reduced fitness at old ages in nonmammalian species that exhibit long chronological lifespans.aging | lifespan | painted turtle | reproduction | senescence W hy do some organisms show little to no signs of aging as they get older, whereas others exhibit substantial physiological deterioration and reproductive senescence with advancing age (1, 2)? This question has motivated many studies of aging in the wild, ranging from reviews of demographic aging (3, 4) to compilations of mechanistic studies (e.g., ref. 5 and references therein). Senescence should evolve when selection is weaker on deleterious traits expressed at an old age relative to those expressed at a young age (6). Indeed, mutations with senescent effects can persist because of a tradeoff between beneficial effects early in life and pleiotropic detrimental effects late in life (7,8). Importantly, the persistence of age-specific deleterious mutations will therefore be influenced by levels and sources of extrinsic mortality (e.g., predation, resource scarcity, infectious disease) and the particular ages at which extrinsic sources cause death (9, 10). For example, the onset of physiological or reproductive deterioration is expected to occur relatively early in populations exposed to high levels of extrinsic mortality of adults. Accordingly, such organisms are expected to evolve rapid development/growth, high reproductive effort at young ages, and a shortened lifespan. For species or populations that experience low extrinsic mortality rates, physiological and reproductive function are expected to decline more slowly with advancing age or with a delay in the onset of senescent decline (7). Moreover, such age-specific selection dynamics can result in negligible (11) and even negative ...

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Section: Discussionmentioning

confidence: 92%

Decades of field data reveal that turtles senesce in the wild

Warner

Miller

Bronikowski

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Ectothermic vertebrates have traits that suggest physiological maintenance patterns should deviate from those seen in previously studied endothermic vertebrates. For example, many reptiles are extremely long-lived and have increased reproductive output with age in adult females (as a result of indeterminate growth), suggesting that senescence should be minimal in these taxa and reduced in females compared with males (Patnaik, 1994;Congdon et al, 2003;Madsen et al, 2007;Bronikowski, 2008) (but see Congdon et al, 2001). Senescence in reproductive output appears to be nonexistent in long-lived reptiles (Congdon et al, 2001;Congdon et al, 2003;Sparkman et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

“…For example, many reptiles are extremely long-lived and have increased reproductive output with age in adult females (as a result of indeterminate growth), suggesting that senescence should be minimal in these taxa and reduced in females compared with males (Patnaik, 1994;Congdon et al, 2003;Madsen et al, 2007;Bronikowski, 2008) (but see Congdon et al, 2001). Senescence in reproductive output appears to be nonexistent in long-lived reptiles (Congdon et al, 2001;Congdon et al, 2003;Sparkman et al, 2007). However, age-dependent physiological maintenance in long-lived taxa or in reptiles is largely unknown (Patnaik, 1994;Madsen et al, 2007;Robert et al, 2007;Bronikowski, 2008;Sparkman and Palacios, 2009).…”

Section: Introductionmentioning

confidence: 99%

State-dependent physiological maintenance in a long-lived ectotherm, the painted turtle (Chrysemys picta)

Schwanz

Warner

McGaugh

et al. 2011

Journal of Experimental Biology

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SUMMARYEnergy allocation among somatic maintenance, reproduction and growth varies not only among species, but among individuals according to states such as age, sex and season. Little research has been conducted on the somatic (physiological) maintenance of long-lived organisms, particularly ectotherms such as reptiles. In this study, we examined sex differences and age-and seasonrelated variation in immune function and DNA repair efficiency in a long-lived reptile, the painted turtle (Chrysemys picta). Immune components tended to be depressed during hibernation, in winter, compared with autumn or spring. Increased heterophil count during hibernation provided the only support for winter immunoenhancement. In juvenile and adult turtles, we found little evidence for senescence in physiological maintenance, consistent with predictions for long-lived organisms. Among immune components, swelling in response to phytohemagglutinin (PHA) and control injection increased with age, whereas basophil count decreased with age. Hatchling turtles had reduced basophil counts and natural antibodies, indicative of an immature immune system, but demonstrated higher DNA repair efficiency than older turtles. Reproductively mature turtles had reduced lymphocytes compared with juvenile turtles in the spring, presumably driven by a trade-off between maintenance and reproduction. Sex had little influence on physiological maintenance. These results suggest that components of physiological maintenance are modulated differentially according to individual state and highlight the need for more research on the multiple components of physiological maintenance in animals of variable states. Supplementary material available online at

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“…Indeterminately growing reptiles in general, and snakes in particular, are prime candidates for aging research (e.g., Kardong 1996;Congdon et al 2001Congdon et al , 2003Miller 2001). Snakes are underutilized models for studying the evolution of aging, in spite of the fact that a variety of remarkable characteristics recommend them as vertebrate animal models (Olsson and Shine 1996;Ujvari and Madsen 2006).…”

Section: Introductionmentioning

confidence: 99%

The evolution of aging phenotypes in snakes: a review and synthesis with new data

Bronikowski

2008

AGE

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Reptiles are underutilized vertebrate models in the study of the evolution and persistence of senescence. Their unique physiology, indeterminate growth, and increasing fecundity across the adult female lifespan motivate the study of how physiology at the mechanistic level, life history at the organismal level, and natural selection at the evolutionary timescale define lifespan in this diverse taxonomic group. Reviewed here are, first, comparative results of cellular metabolic studies conducted across a range of colubrid snake species with variable lifespan. New results on the efficiency of DNA repair in these species are synthesized with the cellular studies. Second, detailed studies of the ecology, life history, and cellular physiology are reviewed for one colubrid species with either short or long lifespan (Thamnophis elegans). New results on the rate of telomere shortening with age in this species are synthesized with previous research. The comparative and intraspecific studies both yield results that species with longer lifespans have underlying cellular physiologies support the free-radical/repair mechanistic hypothesis for aging. As well, both underscore the importance of mortality environment for the evolution of aging rate.

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Hypotheses of aging in a long-lived vertebrate, Blanding's turtle (Emydoidea blandingii)

Cited by 156 publications

References 18 publications

Decades of field data reveal that turtles senesce in the wild

Decades of field data reveal that turtles senesce in the wild

State-dependent physiological maintenance in a long-lived ectotherm, the painted turtle (Chrysemys picta)

The evolution of aging phenotypes in snakes: a review and synthesis with new data

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