Abstract
Drosophila research has identified a new feature of aging that has been called the death spiral. The death spiral is a period prior to death during which there is a decline in life-history characters, such as fecundity, as well as physiological characters. First, we review the data from the Drosophila and medfly literature that suggest the existence of death spirals. Second, we re-analyze five cases with such data from four laboratories using a generalized statistical framework, a re-analysis that strengthens the case for the salience of the death spiral phenomenon. Third, we raise the issue whether death spirals need to be taken into account in the analysis of functional characters over age, in aging research with model species as well as human data.
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References
Beard RE (1959) Note on some mathematical mortality models. In: Wolstenholme GEW, O’Connor M (eds) The lifespan of animals, Ciba Foundation Colloquium on Ageing. Little, Brown, Boston, pp 302–311
Bell G (1984) Evolutionary and nonevolutionary theories of senescence. Am Nat 124:600–603
Belsky DW, Caspic A, Houts R, Cohen HJ, Corcoran DL, Danese A, Harrington H, Israel S, Levine ME, Schaefer JD, Sugden K, Williams B, Yashin AI, Poulton R, Moffitt TE (2015) Quantification of biological aging in young adults. Proc Natl Acad Sci USA 112:E4104–E4110
Carey JR, Liedo P, Orozco D, Vaupel JW (1992) Slowing of mortality rates at older ages in large medfly cohorts. Science 258:457–461
Christensen K, McGue M, Petersen I, Jeune B, Vaupel JW (2008) Exceptional longevity does not result in excessive levels of disability. Proc Natl Acad Sci USA 105:13274–13279
Comfort A (1979) Ageing: the biology of senescence, 3rd edn. Churchill Livingstone, Edinburgh
Crimmins EM (2004) Trends in the health of the elderly. Ann Rev Public Health 25:79–98
Curtsinger JW (2015) The retired fly: detecting life history transition in individual Drosophila melanogaster females. Gerontol A Biol Sci Med Sci 70:1455–1460
Curtsinger JW, Fukui HH, Townsend DR, Vaupel JW (1992) Demography of genotypes: failure of the limited life span paradigm in Drosophila melanogaster. Science 258:461–463
Cutler DM (2001) The reduction in disability among the elderly. Proc Natl Acad Sci USA 98:6546–6547
Fauth EB, Zarit SH, Malmberg B (2008) Mediating relationaships within the disablement process model: a cross-sectional study of the oldest-old. Eur J Aging 5:161–179
Fogel RW, Costa DL (1997) A theory of technophysio evolution, with some implications for forecasting population, health care costs, and pension costs. Demography 34:49–66
Gareth J, Witten D, Hastie T, Tibshirani R (2013) An introduction to statistical learning with applications in R. Spinger, New York
Greenwood M, Irwin JO (1939) Biostatistics of senility. Hum Biol 11:1–23
Grover D, Yang J, Tavare S, Tower J (2008) Simultaneous tracking of fly movement and gene expression using GFP. BMC Biotechnol 8:93
Grover D, Yang J, Ford D, Tavare S, Tower J (2009) Simultaneous tracking of movement and gene expression in multiple Drosophila melanogaster flies using GFP and DsRED fluorescent reporter transgenes. BMC Res Notes 2:58
Hastie T, Tibshirani R, Friedman J (2009) The elements of statistical learning, 2nd edn. Springer, New York
Khazaeli AA, Curtsinger JW (2014) Heterogeneity’s ruses: how hidden variation affects population trajectories of age-dependent fecundity in Drosophila melanogaster. Demogr Res 30:313–332
Klepsatel P, Galikova M, De Maio N, Ricci S, Schlotterer C, Flatt T (2013) Reproductive and post-reproductive life history of wild-caught Drosophila melanogaster under laboratory conditions. J Evol Biol 26:1508–1520
Le Bourg E, Lints FA, Delince J, Lints CV (1988) Reproductive fitness and longevity in Drosophila melanogaster. Exp Gerontol 23:491–500
Luckinbill LS, Clare MJ (1985) Selection for life span in Drosophila melanogaster. Heredity 55:9–18
Manton KG, Gu X (2001) Changes in the prevalence of chronic disability in the United States black and nonblack population above age 65 from 1982 to 1999. Proc Natl Acad Sci USA 98:6354–6359
Manton KG, Gu X, Lamb VL (2006) Change in chronic disability from 1982 to 2004/2005 as measured by long-term changes in function and health in the U.S. elderly population. Proc Natl Acad Sci USA 103:18374–18379
Martinez DE (1998) Mortality patterns suggest lack of senescence in Hydra. Expt Geront 33:217–225
Morley JE (2008) Diabetes and aging: epidemiologic overview. Clin Geriatr Med 24:395–405
Mueller LD, Drapeau MD, Adams CS, Hammerle CW, Doyal KM, Jazayeri AJ, Ly T, Beguwala SA, Mamidi AR, Rose MR (2003) Statistical tests of demographic heterogeneity theories. Exp Gerontol 38:373–386
Mueller LD, Rauser CL, Rose MR (2007) An evolutionary heterogeneity model of late-life fecundity in Drosophilia. Biogerontology 8:147–161
Mueller LD, Shahrestani P, Rauser CL (2009) Predicting death in female Drosophila. Exp Gerontol 44:766–772
Mueller LD, Rauser CL, Rose MR (2011) Does aging stop? Oxford University Press, Oxford
Müller HG, Carey JR, Wu D, Liedo P, Vaupel JW (2001) Reproductive potential predicts longevity of female Mediterranean fruitflies. Proc R Soc Lond Ser B 268:445–450
Papadopoulos NT, Varey JR, Katsoyannos BI, Muller HG, Liu X (2002) Supine behavior predicts time-to-death in male Mediterranean fruit flies. Proc R Soc Lond Ser B 269:1633–1637
Rauser CL, Abdel-Aal Y, Shieh JA, Suen CW, Mueller LD, Rose MR (2005) Lifelong heterogeneity in fecundity is insufficient to explain late-life fecundity plateaus in Drosophila melanogaster. Exp Gerontol 40:660–670
Rauser CL, Mueller LD, Rose MR (2006a) The evolution of late life. Aging Res Rev 5:14–32
Rauser CL, Tierney JJ, Gunion SM, Covarrubias GM, Mueller LD, Rose MR (2006b) Evolution of late-life fecundity in Drosophila melanogaster. J Evol Biol 19:289–301
Rera M, Clark RI, Walker DW (2012) Intestinal barrier dysfunction links metabolic and inflammatory markers of aging to death in Drosophila. Proc Natl Acad Sci USA 109:21528–21533
Rogina B, Wolverton T, Bross TG, Chen K, Muller HG, Carey JR (2007) Distinct biological epochs in the reproductive life of female Drosophila melanogaster. Mech Ageing Dev 128:477–478
Rose MR, Vu LN, Park SU, Graves JL (1992) Selection for stress resistance increases longevity in Drosophila melanogaster. Exp Gerontol 27:241–250
Rose MR, Drapeau MD, Yazdi PG, Shah KH, Moise DB, Thakar RR, Rauser CL, Mueller LD (2002) Evolution of late-life mortality in Drosophila melanogaster. Evolution 56:1982–1991
Rose MR, Rauser CL, Mueller LD (2005) Late life: a new frontier for physiology. Physiol Biochem Zool 78:869–878
Rose MR, Rauser CL, Mueller LD, Benford G (2006) A revolution for aging research. Biogerontology 7:269–277
Schoeni RF, Freedman VA, Martin LG (2008) Why is late-life disability declining? Milbank Q 86:47–89
Shahrestani P, Tran X, Mueller LD (2012a) Patterns of male fitness conform to predictions of evolutionary models of late-life. J Evol Biol 25:1060–1065
Shahrestani P, Tran X, Mueller LD (2012b) Physiological decline prior to death in Drosophila melanogaster. Biogerontology 13:537–545
Vaupel JW, Manton KG, Stallard E (1979) The impact of heterogeneity in individual frailty on the dynamics of mortality. Demography 16:439–454
Vaupel JW, Carey JR, Christensen K, Johnson TE, Yashin AI, Holm NV, Iachine IA, Kannisto V, Khazaeli AA, Liedo P, Longo VD, Zeng Y, Manton KG, Curtsinger JW (1998) Biodemographic trajectories of longevity. Science 280:855–860
Verbrugge LM, Jette AM (1994) The disablement process. Soc Sci Med 38:1–14
Wax TM, Goodrick CL (1978) Nearness to death and wheelrunning behavior in mice. Exp Geront 13:233–236
Yang J, Tower J (2009) Expression of hsp22 and hsp70 transgenes is partially predictive of Drosophila survival under normal and stress conditions. J Gerontol 8:828–838
Zhang WB, Pincus Z (2016) Predicting all-cause mortality from basic physiology in the Framingham heart study. Aging Cell 15:39–48
Acknowledgments
We thank Andrew Noymer for useful suggestions on the manuscript. We thank J. Curtsinger, E. Le Bourg, and T. Flatt for sharing data and answering questions about their research and two anonymous referees for helpful suggestions. This research has been supported by the Ayala School of Biological Sciences, University of California, Irvine.
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Mueller, L.D., Shahrestani, P., Rauser, C.L. et al. The death spiral: predicting death in Drosophila cohorts. Biogerontology 17, 805–816 (2016). https://doi.org/10.1007/s10522-016-9639-7
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DOI: https://doi.org/10.1007/s10522-016-9639-7