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

Schwanz, Lisa E.; Warner, Daniel A.; McGaugh, Suzanne E.; Terlizzi, Roberta Di; Bronikowski, Anne M.

doi:10.1242/jeb.046813

Cited by 47 publications

(41 citation statements)

References 65 publications

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“…Changes in markers of the immune system, broadly consistent with immunosenescence, have also been documented in some studies of wild birds and reptiles (reviewed in Palacios et al, 2011), and in one wild mammal population (Nussey et al, 2012), although it is notable that several studies in birds and reptiles have failed to find patterns consistent with age-related declines in immune function (e.g. Lecomte et al, 2010; Massot et al, 2011; Palacios et al, 2011; Schwanz et al, 2011). …”

Section: Senescence In Wild Animals – An Evidentiary Reviewmentioning

confidence: 85%

Senescence in natural populations of animals: Widespread evidence and its implications for bio-gerontology

Nussey¹,

Froy²,

Lemaître³

et al. 2013

Ageing Research Reviews

596

591

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That senescence is rarely, if ever, observed in natural populations is an oft-quoted fallacy within bio-gerontology. We identify the roots of this fallacy in the otherwise seminal works of Medawar and Comfort, and explain that under antagonistic pleiotropy or disposable soma explanations for the evolution of senescence there is no reason why senescence cannot evolve to be manifest within the life expectancies of wild organisms. The recent emergence of long-term field studies presents irrefutable evidence that senescence is commonly detected in nature. We found such evidence in 175 different animal species from 340 separate studies. Although the bulk of this evidence comes from birds and mammals, we also found evidence for senescence in other vertebrates and insects. We describe how high-quality longitudinal field data allow us to test evolutionary explanations for differences in senescence between the sexes and among traits and individuals. Recent studies indicate that genes, prior environment and investment in growth and reproduction influence aging rates in the wild. We argue that – with the fallacy that wild animals do not senesce finally dead and buried – collaborations between bio-gerontologists and field biologists can begin to test the ecological generality of purportedly ‘public’ mechanisms regulating aging in laboratory models.

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Section: Senescence In Wild Animals – An Evidentiary Reviewmentioning

confidence: 85%

Senescence in natural populations of animals: Widespread evidence and its implications for bio-gerontology

Nussey¹,

Froy²,

Lemaître³

et al. 2013

Ageing Research Reviews

596

591

View full text Add to dashboard Cite

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“…These divergent patterns may be explained by very different rates of extrinsic mortality in turtles (or their ancestors) compared with mammals. Indeed, because of their protective morphology (shell) and lack of senescence in immune function (46), turtles likely experience considerably less late-age mortality attributable to extrinsic factors than do mammals. This comparison between turtles and mammals fits with theoretical expectations for patterns of survival senescence in these taxa, but our results challenge the traditional view that long-lived ectotherms, such as turtles, do not exhibit declining Table 1.…”

Section: Discussionmentioning

confidence: 99%

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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“…We made two modifications to the procedure described by Matson et al [50] based on pilot work to maximize our ability to detect inter-individual variation: 1) we reduced the concentration of the SRBC suspensions in this assay from 1% to 0.5% and 2) the incubation temperature was decreased from 37°C to 26.5°C. This temperature change allowed the assay incubation to more accurately reflect the ambient temperature in which study animals were housed (range 25.0 - 27.2°C), as has been done previously with ectotherms [51] and which is important because incubation temperature plays a significant role in agglutination and lysis [52]. After incubation for 90 min, the plates were tilted for 20 min at 45° to permit visualization of the agglutination response, then digitally scanned at a resolution of 600 dpi.…”

Section: Methodsmentioning

confidence: 99%

The effect of carotenoid supplementation on immune system development in juvenile male veiled chameleons (Chamaeleo calyptratus)

et al. 2014

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IntroductionNutrient availability, assimilation, and allocation can have important and lasting effects on the immune system development of growing animals. Though carotenoid pigments have immunostimulatory properties in many animals, relatively little is known regarding how they influence the immune system during development. Moreover, studies linking carotenoids to health at any life stage have largely been restricted to birds and mammals. We investigated the effects of carotenoid supplementation on multiple aspects of immunity in juvenile veiled chameleons (Chamaeleo calyptratus). We supplemented half of the chameleons with lutein (a xanthophyll carotenoid) for 14 weeks during development and serially measured multiple aspects of immune function, including: agglutination and lysis performance of plasma, wound healing, and plasma nitric oxide concentrations before and after wounding.ResultsThough lutein supplementation effectively elevated circulating carotenoid concentrations throughout the developmental period, we found no evidence that carotenoid repletion enhanced immune function at any point. However, agglutination and lysis scores increased, while baseline nitric oxide levels decreased, as chameleons aged.ConclusionsTaken together, our results indicate that body mass and age, but not carotenoid access, may play an important role in immune performance of growing chameleons. Hence, studying well-understood physiological processes in novel taxa can provide new perspectives on alternative physiological processes and nutrient function.

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

Cited by 47 publications

References 65 publications

Senescence in natural populations of animals: Widespread evidence and its implications for bio-gerontology

Senescence in natural populations of animals: Widespread evidence and its implications for bio-gerontology

Decades of field data reveal that turtles senesce in the wild

The effect of carotenoid supplementation on immune system development in juvenile male veiled chameleons (Chamaeleo calyptratus)

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