Evolutionary ecology of aging: time to reconcile field and laboratory research
Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
27069592
PubMed Central
PMC4809807
DOI
10.1002/ece3.2093
PII: ECE32093
Knihovny.cz E-zdroje
- Klíčová slova
- Condition‐dependence, evolution of aging, gene‐by‐environment interaction, intrapopulation variability, intraspecific aging rate, mortality, senescence,
- Publikační typ
- časopisecké články MeSH
Aging is an increase in mortality risk with age due to a decline in vital functions. Research on aging has entered an exciting phase. Advances in biogerontology have demonstrated that proximate mechanisms of aging and interventions to modify lifespan are shared among species. In nature, aging patterns have proven more diverse than previously assumed. The paradigm that extrinsic mortality ultimately determines evolution of aging rates has been questioned and there appears to be a mismatch between intra- and inter-specific patterns. The major challenges emerging in evolutionary ecology of aging are a lack of understanding of the complexity in functional senescence under natural conditions and unavailability of estimates of aging rates for matched populations exposed to natural and laboratory conditions. I argue that we need to reconcile laboratory and field-based approaches to better understand (1) how aging rates (baseline mortality and the rate of increase in mortality with age) vary across populations within a species, (2) how genetic and environmental variation interact to modulate individual expression of aging rates, and (3) how much intraspecific variation in lifespan is attributable to an intrinsic (i.e., nonenvironmental) component. I suggest integration of laboratory and field assays using multiple matched populations of the same species, along with measures of functional declines.
Zobrazit více v PubMed
Abrams, P. A. 1993. Does increased mortality favor the evolution of more rapid senescence? Evolution 47:877–887. PubMed
Arendt, J. D. , Reznick D. N., and López‐Sepulcre A.. 2014. Replicated origin of female‐biased adult sex ratio in introduced populations of the Trinidadian guppy (Poecilia reticulata.). Evolution 68:2343–2356. PubMed
Bartáková, V. , Reichard M., Blažek R., Polačik M., and Bryja J.. 2015. Terrestrial fishes: rivers are barriers to gene flow in annual fishes from the African savanna. J. Biogeogr. 42:1832–1844.
Baudisch, A. 2011. The pace and shape of ageing. Methods Ecol. Evol. 2:375–382.
Baumgart, M. , Groth M., Priebe S., Appelt J., Guthke R., Platzer M., et al. 2012. Age‐dependent regulation of tumor‐related microRNAs in the brain of the annual fish Nothobranchius furzeri . Mech. Ageing Dev. 133:226–233. PubMed
Beekman, M. , Blanché H., Perola M., Hervonen A., Bezrukov V., Sikora E., et al. 2013. Genome‐wide linkage analysis for human longevity: genetics of healthy aging study. Aging Cell 12:184–193. PubMed PMC
Berg, E. C. , and Maklakov A. A.. 2012. Sexes suffer from suboptimal lifespan because of genetic conflict in a seed beetle. Proc. Biol. Sci. 279:4296–4302. PubMed PMC
Blagosklonny, M. V. 2008. Aging: ROS or TOR. Cell Cycle 7:3344–3354. PubMed
Blažek, R. , Polačik M., and Reichard M.. 2013. Rapid growth, early maturation and short generation time in African annual fishes. Evodevo 4:1–7. PubMed PMC
Bonduriansky, R. , and Brassil C. E.. 2002. Senescence: rapid and costly ageing in wild male flies. Nature 420:377. PubMed
Bonduriansky, R. , Maklakov A., Zajitschek F., and Brooks R.. 2008. Sexual selection, sexual conflict and the evolution of ageing and life span. Funct. Ecol. 22:443–453.
Boonekamp, J. J. , Salomons M., Bouwhuis S., Dijkstra C., and Verhulst S.. 2014. Reproductive effort accelerates actuarial senescence in wild birds: an experimental study. Ecol. Lett. 17:599–605. PubMed
Bronikowski, A. M. , Alberts S. C., Altmann J., Packer C., Carey K. D., and Tatar M.. 2002. The aging baboon: comparative demography in a non‐human primate. Proc. Natl Acad. Sci. USA 99:9591–9595. PubMed PMC
Bronikowski, A. M. , Altmann J., Brockman D. K., Cords M., Fedigan L. M., Pusey A., et al. 2011. Aging in the natural world: comparative data reveal similar mortality patterns across primates. Science 331:1325–1328. PubMed PMC
Bryant, M. J. , and Reznick D.. 2004. Comparative studies of senescence in natural populations of guppies. Am. Nat. 163:55–68. PubMed
Cellerino, A. , Valenzano D. R., and Reichard M.. 2016. From the bush to the bench: the annual Nothobranchius fishes as a new model system in biology. Biol. Rev. doi:10.1111/brv.12183. PubMed DOI
Charmantier, A. , Perrins C., McCleery R. H., and Sheldon B. C.. 2006. Quantitative genetics of age at reproduction in wild swans: support for antagonistic pleiotropy models of senescence. Proc. Natl Acad. Sci. USA 103:6587–6592. PubMed PMC
Chen, H. Y. , and Maklakov A. A.. 2012. Longer life span evolves under high rates of condition‐dependent mortality. Curr. Biol. 22:2140–2143. PubMed
Chen, H. Y. , and Maklakov A. A.. 2014. Condition dependence of male mortality drives the evolution of sex differences in longevity. Curr. Biol. 24:2423–2427. PubMed
Colchero, F. , Jones O. R., and Rebke M.. 2012. BaSTA: an R package for Bayesian estimation of age‐specific survival from incomplete mark–recapture/recovery data with covariates. Methods Ecol. Evol. 3:466–470.
Cornwallis, C. K. , Dean R., and Pizzari T.. 2014. Sex‐specific patterns of aging in sexual ornaments and gametes. Am. Nat. 184:E66–E78. PubMed
Coulson, T. , Benton T. G., Lundberg P., Dall S. R. X., Kendall B. E., and Gaillard J. M.. 2006. Estimating individual contributions to population growth: evolutionary fitness in ecological time. Proc. Biol. Sci. 273:547–555. PubMed PMC
Darwin, C. 1859. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. J. Murray, London. PubMed PMC
Deelen, J. , Beekman M., Uh H. W., Helmer Q., Kuningas M., Christiansen L., et al. 2011. Genome‐wide association study identifies a single major locus contributing to survival into old age; the APOE locus revisited. Aging Cell 10:686–698. PubMed PMC
Di Cicco, E. , Tozzini E. T., Rossi G., and Cellerino A.. 2011. The short‐lived annual fish Nothobranchius furzeri shows a typical teleost aging process reinforced by high incidence of age‐dependent neoplasias. Exp. Gerontol. 46:249–256. PubMed
Dias, B. G. , and Ressler K. J.. 2014. Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat. Neurosci. 17:89–96. PubMed PMC
Evans, J. P. , Pilastro A., and Schlupp I.. 2011. Ecology and evolution of poecilid fishes. Univ. of Chicago Press, Chicago.
Fang, X. , Seim I., Huang Z., Gerashchenko M. V., Xiong Z., Turanov A. A., et al. 2014. Adaptations to a subterranean environment and longevity revealed by the analysis of mole rat genomes. Cell Rep. 8:1354–1364. PubMed PMC
Fontana, L. , Partridge L., and Longo V. D.. 2010. Extending healthy life span – from yeast to humans. Science 328:321–326. PubMed PMC
Fontana, L. , Kennedy B. K., Longo V. D., Seals D., and Melov S.. 2014. Medical research: treat ageing. Nature 511:405–407. PubMed
Gems, D. , and Partridge L.. 2013. Genetics of longevity in model organisms: debates and paradigm shifts. Annu. Rev. Physiol. 75:621–644. PubMed
Hämäläinen, A. , Dammhahn M., Aujard F., Eberle M., Hardy I., Kappeler P. M., et al. 2014. Senescence or selective disappearance? Age trajectories of body mass in wild and captive populations of a small‐bodied primate. Proc. Biol. Sci. 281:20140830. PubMed PMC
Harel, I. , Benayoun B. A., Machado B., Singh P. P., Hu C. K., Pech M. F., et al. 2015. A platform for rapid exploration of aging and diseases in a naturally short‐lived vertebrate. Cell 160:1013–1026. PubMed PMC
Harrison, D. E. , Strong R., Sharp Z. D., Nelson J. F., Astle C. M., Flurkey K., et al. 2009. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460:392–395. PubMed PMC
Hayward, A. D. , Wilson A. J., Pilkington J. G., Pemberton J. M., and Kruuk L. E.. 2009. Ageing in a variable habitat: environmental stress affects senescence in parasite resistance in St Kilda Soay sheep. Proc. Biol. Sci. 276:3477–3485. PubMed PMC
Hayward, A. D. , Wilson A. J., Pilkington J. G., Clutton‐Brock T. H., Pemberton J. M., and Kruuk L. E.. 2011. Natural selection on a measure of parasite resistance varies across ages and environmental conditions in a wild mammal. J. Evol. Biol. 24:1664–1676. PubMed
Hayward, A. D. , Wilson A. J., Pilkington J. G., Clutton‐Brock T. H., Pemberton J. M., and Kruuk L. E.. 2013. Reproductive senescence in female Soay sheep: variation across traits and contributions of individual ageing and selective disappearance. Funct. Ecol. 27:184–195.
Holzenberger, M. , Dupont J., Ducos B., Leneuve P., Géloën A., Even P. C., et al. 2003. IGF‐1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421:182–187. PubMed
Jones, O. R. , Gaillard J. M., Tuljapurkar S., Alho J. S., Armitage K. B., Becker P. H., et al. 2008. Senescence rates are determined by ranking on the fast–slow life‐history continuum. Ecol. Lett. 11:664–673. PubMed
Jones, O. R. , Scheuerlein A., Salguero‐Gómez R., Camarda C. G., Schaible R., Casper B. B., et al. 2014. Diversity of ageing across the tree of life. Nature 505:169–173. PubMed PMC
Kawasaki, N. , Brassil C. E., Brooks R. C., and Bonduriansky R.. 2008. Environmental effects on the expression of life span and aging: an extreme contrast between wild and captive cohorts of Telostylinus angusticollis (Diptera: Neriidae). Am. Nat. 172:346–357. PubMed
Kawecki, T. J. , Lenski R. E., Ebert D., Hollis B., Olivieri I., and Whitlock M. C.. 2012. Experimental evolution. Trends Ecol. Evol. 27:547–560. PubMed
Kenyon, C. J. 2010. The genetics of ageing. Nature 464:504–512. PubMed
Kimber, C. M. , and Chippindale A. K.. 2013. Mutation, condition, and the maintenance of extended lifespan in Drosophila . Curr. Biol. 23:2283–2287. PubMed
Kirkwood, T. B. L. 1977. Evolution of ageing. Nature 270:301–304. PubMed
Kirkwood, T. B. L. , and Austad S. N.. 2000. Why do we age? Nature 408:233–238. PubMed
Kirkwood, T. B. L. , and Rose M.. 1991. Evolution of senescence: late survival sacrificed for reproduction. Philos. Trans. R Soc. Lond. B Biol. Sci. 332:15–24. PubMed
Kraus, C. , Pavard S., and Promislow D. E.. 2013. The size–life span trade‐off decomposed: why large dogs die young. Am. Nat. 181:492–505. PubMed
Ladiges, W. , Van Remmen H., Strong R., Ikeno Y., Treuting P., Rabinovitch P., et al. 2009. Lifespan extension in genetically modified mice. Aging Cell 8:346–352. PubMed
Lee, W. S. , Monaghan P., and Metcalfe N. B.. 2013. Experimental demonstration of the growth rate–lifespan trade‐off. Proc. Biol. Sci. 280:20122370. PubMed PMC
Lemaître, J. F. , Gallard J. M., Pemberton J. M., Clutton‐Brock T. H., and Nussey D. H.. 2014. Early life expenditure in sexual competition is associated with increased reproductive senescence in male red deer. Proc. Biol. Sci. 281:20140792. PubMed PMC
Liao, C. Y. , Rikke B. A., Johnson T. E., Diaz V., and Nelson J. F.. 2010. Genetic variation in the murine lifespan response to dietary restriction: from life extension to life shortening. Aging Cell 9:92–95. PubMed PMC
Lind, M. I. , Zwoinska M. K., Meurling S., Carlsson H., and Maklakov A. A.. 2016. Sex‐specific trade‐offs with growth and fitness following lifespan extension by rapamycin in an outcrossing nematode, Caenorhabditis remanei . J. Gerontol. A Biol. Sci. Med. Sci. doi: 10.1093/gerona/glv174. PubMed DOI
Lohr, J. N. , David P., and Haag C. R.. 2014. Reduced lifespan and increased ageing driven by genetic drift in small populations. Evolution 68:2494–2508. PubMed
López‐Otín, C. , Blasco M. A., Partridge L., Serrano M., and Kroemer G.. 2013. The hallmarks of aging. Cell 153:1194–1217. PubMed PMC
de Magalhães, J. P. , Wuttke D., Wood S. H., Plank M., and Vora C.. 2012. Genome‐environment interactions that modulate aging: powerful targets for drug discovery. Pharmacol. Rev. 64:88–101. PubMed PMC
Maklakov, A. A. , and Lummaa V.. 2013. Evolution of sex differences in lifespan and aging: causes and constraints. BioEssays 35:717–724. PubMed
Maklakov, A. A. , Fricke C., and Arnqvist G.. 2007. Sexual selection affects lifespan and aging in the seed beetle. Aging Cell 6:739–744. PubMed
Massot, M. , Clobert J., Montes‐Poloni L., Haussy C., Cubo J., and Meylan S.. 2011. An integrative study of ageing in a wild population of common. Funct. Ecol. 25:848–858.
Medawar, P. B. 1952. An unsolved problem of biology. H.K. Lewis, London.
Monaghan, P. , Charmantier A., Nussey D. H., and Ricklefs R. E.. 2008. The evolutionary ecology of senescence. Funct. Ecol. 22:371–378.
Morbey, Y. E. , Brassil C. E., and Hendry A. P.. 2005. Rapid senescence in Pacific salmon. Am. Nat. 166:556–568. PubMed
Nussey, D. H. , Kruuk L. E. B., Morris A., and Clutton‐Brock T. H.. 2007. Environmental conditions in early life influence ageing rates in a wild population of red deer. Curr. Biol. 17:R1000–R1001. PubMed
Nussey, D. H. , Wilson A. J., Morris A., Pemberton J., Clutton‐Brock T., and Kruuk L. E. B.. 2008. Testing for genetic trade‐offs between early‐ and late‐life reproduction in a wild red deer population. Proc. Biol. Sci. 275:745–750. PubMed PMC
Nussey, D. H. , Froy H., Lemaitre J.‐F., Gaillard J. M., and Austad S. N.. 2013. Senescence in natural populations of animals: widespread evidence and its implications for bio‐gerontology. Ageing Res. Rev. 12:241–255. PubMed PMC
Nussey, D. H. , Baird D., Barrett E., Boner W., Fairlie J., Gemmell N., et al. 2014. Measuring telomere length and telomere dynamics in evolutionary biology and ecology. Methods Ecol. Evol. 5:299–310. PubMed PMC
Parsons, P. A. 1995. Inherited stress resistance and longevity: a stress theory of ageing. Heredity 75:216–221. PubMed
Partridge, L. , and Gems D.. 2007. Benchmarks for ageing studies. Nature 450:165–167. PubMed
Pianka, E. R. 1970. On r‐and K‐selection. Am. Nat. 104:592–597.
Pincus, Z. , Smith‐Vikos T., and Slack F. J.. 2011. MicroRNA predictors of longevity in Caenorhabditis elegans . PLoS Genet. 7:e1002306. PubMed PMC
Pletcher, S. D. , Khazaeli A. A., and Curtsinger J. W.. 2000. Why do life spans differ? Partitioning mean longevity differences in terms of age‐specific mortality parameters. J. Gerontol. A Biol. Sci. Med. Sci. 55:B381–B389. PubMed
Polačik, M. , Donner M. T., and Reichard M.. 2011. Age structure of annual Nothobranchius fishes in Mozambique: is there a hatching synchrony? J. Fish Biol. 78:796–809. PubMed
Polačik, M. , Blažek R., and Reichard M.. 2016. Laboratory breeding of the short‐lived annual killifish Nothobranchius furzeri . Nat. Protoc. doi: 10.1038/nprot.2016.080. in press. PubMed DOI
Reichard, M. , Polačik M., Blažek R., and Vrtílek M.. 2014. Female bias in the adult sex ratio of African annual fishes: interspecific differences, seasonal trends and environmental predictors. Evol. Ecol. 28:1105–1120.
Reznick, D. N. , Bryant M. J., Roff D., Ghalambor C. K., and Ghalambor D. E.. 2004. Effect of extrinsic mortality on the evolution of senescence in guppies. Nature 431:1095–1099. PubMed
Ricklefs, R. E. 2008. The evolution of senescence from a comparative perspective. Funct. Ecol. 22:379–392.
Ricklefs, R. E. 2010a. Life‐history connections to rates of aging in terrestrial vertebrates. Proc. Natl Acad. Sci. USA 107:10314–10319. PubMed PMC
Ricklefs, R. E. 2010b. Insights from comparative analyses of aging in birds and mammals. Aging Cell 9:273–284. PubMed PMC
Ricklefs, R. E. , and Cadena C. D.. 2007. Lifespan is unrelated to investment in reproduction in populations of mammals and birds in captivity. Ecol. Lett. 10:867–872. PubMed
Roach, D. A. , and Carey J. R.. 2014. Population biology of aging. Annu. Rev. Ecol. Syst. 45:421–443.
Robinson, M. R. , Mar K. U., and Lummaa V.. 2012. Senescence and age‐specific trade‐offs between reproduction and survival in female Asian elephants. Ecol. Lett. 15:260–266. PubMed
Rose, M. R. , Vu L. N., Park S. U., and Graves J. L.. 1992. Selection on stress resistance increases longevity in Drosophila melanogaster . Exp. Gerontol. 27:241–250. PubMed
Santos, E. , and Nakagawa S.. 2012. The costs of parental care: a meta‐analysis of the trade‐off between parental effort and survival in birds. J. Evol. Biol. 25:1911–1917. PubMed
Schneeberger, K. , Courtiol A., Czirják G. Á., and Voigt C. C.. 2014. Immune profile predicts survival and reflects senescence in a small, long‐lived mammal, the greater sac‐winged bat (Saccopteryx bilineata). PLoS One 9:e108268. PubMed PMC
Selman, C. , Blount J. D., Nussey D. H., and Speakman J. R.. 2012. Oxidative damage, ageing, and life‐history evolution: where now? Trends Ecol. Evol. 27:570–577. PubMed
Sharp, S. P. , and Clutton‐Brock T. H.. 2011. Competition, breeding success and ageing rates in female meerkats. J. Evol. Biol. 24:1756–1762. PubMed
Shokhirev, M. N. , and Johnson A. A.. 2014. Effects of extrinsic mortality on the evolution of aging: a stochastic modeling approach. PLoS One 9:e86602. PubMed PMC
Sol, D. 2008. Artificial selection, naturalization, and fitness: Darwin's pigeons revisited. Biol. J. Linn. Soc. Lond. 93:657–665.
Speakman, J. R. , Blount J. D., Bronikowski A. M., Buffenstein R., Isaksson C., Kirkwood T. B., et al. 2015. Oxidative stress and life histories: unresolved issues and current needs. Ecol. Evol. 5:5745–5757. PubMed PMC
Stearns, S. C. 1992. The evolution of life histories. Oxford Univ. Press, Oxford.
Stearns, S. C. , Ackermann M., Doebeli M., and Kaiser M.. 2000. Experimental evolution of aging, growth, and reproduction in fruitflies. Proc. Natl Acad. Sci. USA 97:3309–3313. PubMed PMC
Stroustrup, N. , Anthony W. E., Nash Z. M., Gowda V., Gomez A., López‐Moyado I. F., et al. 2016. The temporal scaling of Caenorhabditis elegans ageing. Nature 530:103–107. PubMed PMC
Terzibasi Tozzini, E. , Dorn A., Ng'oma E., Polačik M., Blažek R., Reichwald K., et al. 2013. Parallel evolution of senescence in annual fishes in response to extrinsic mortality. BMC Evol. Biol. 13:77. PubMed PMC
Terzibasi, E. , Valenzano D. R., Benedetti M., Roncaglia P., Cattaneo A., Domenici L., et al. 2008. Large differences in aging phenotype between strains of the short‐lived annual fish Nothobranchius furzeri . PLoS One 3:e3866. PubMed PMC
Valenzano, D. R. , Terzibasi E., Genade T., Cattaneo A., Domenici L., and Cellerino A.. 2006. Resveratrol prolongs lifespan and retards the onset of age‐related markers in a short‐lived vertebrate. Curr. Biol. 16:296–300. PubMed
Wilkening, J. L. , Ray C., and Varner J.. 2016. When can we measure stress noninvasively? Postdeposition effects on a fecal stress metric confound a multiregional assessment Ecol. Evol. 6:502–513. PubMed PMC
Williams, G. C. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:398–411.
Williams, P. D. , and Day T.. 2003. Antagonistic pleiotropy, mo rtality source interactions, and the evolutionary theory of senescence. Evolution 57:1478–1488. PubMed
Williams, P. D. , Day T., Fletcher Q., and Rowe L.. 2006. The shaping of senescence in the wild. Trends Ecol. Evol. 21:458–463. PubMed
Wilson, A. J. , Nussey D. H., Pemberton J. M., Pilkington J. G., Morris A., Pelletier F., et al. 2007. Evidence for a genetic basis of aging in two wild vertebrate populations. Curr. Biol. 17:2136–2142. PubMed
Wilson, A. J. , Charmantier A., and Hadfield J. D.. 2008. Evolutionary genetics of ageing in the wild: empirical patterns and future perspectives. Funct. Ecol. 22:431–442.
Winemiller, K. O. , and Rose K. A.. 1992. Patterns of life‐history diversification in North American fishes: implications for population regulation. Can. J. Fish Aquat. Sci. 49:2196–2218.