Abstract
Methuselah is a Drosophila mutant with a 35% increased lifespan. We examined the robustness of methuselah’s sensorimotor abilities in tethered flight as a function of age in experiments designed to test visuomotor synchronization and phototaxis in simulated flight. A total of 282 flies from different age groups (4 hours to 70 days) and genotypes (mth and w1118) were individually tethered under an infrared laser-sensor system that digitally recorded wing-beat frequency (WBF). We found that mth has a higher average WBF throughout most of its lifespan compared to parental control flies (w1118) and develops flight ability at a younger age. Its WBF at late life, however, is not significantly different than that of its parental control line. We further found that mth entrains during flight to motion of a visual grating significantly better than its parental line. These findings suggest that the mth gene not only delays chronological aging but enhances sensorimotor abilities critical to survival during early and middle, but not late life.
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References
Aigaki T, Seong KH, Matsuo T (2002) Longevity determination genes in Drosophila melanogaster. Mech Ageing Dev 123:1531–1541
Al-Saffar ZY, Grainger JNR, Aldrich J (1996) Temperature and humidity affecting development, survival and weight loss of the pupal stage of Drosophila melanogaster, and the influence of alternating temperature on the larvae. J Therm Biol 21:389–396
Autrum H (1958) Electrophysiological analysis of the visual systems in insects. Exp Cell Res 5(Suppl.):426–439
Barja G (2004) Free radicals and aging. Trends Neurosci 27:595–600
Bokov A, Chaudhuri A, Richardson A (2004) The role of oxidative damage and stress in aging. Mech Aging Dev 125:811–826
Buchner E (1976) Elementary movement detectors in an insect visual system. Biol Cybern 24:85–101
Carey JR, Liedo P, Müller HG, Wang JL, Senturk D, Harshman L (2005) Biodemography of a long-lived tephritid: reproduction and longevity in a large cohort of female Mexican fruit flies, Anastrepha ludens. Exp Gerontol 40:793–800
Cook-Wiens E, Grotewiel MS (2002) Dissociation between functional senescence and oxidative stress resistance in Drosophila. Exp Gerontol 37:1345–1355
Cosens D, Spatz HC (1978) Flicker fusion studies in lamina and receptor region of Drosophila eye. J Insect Physiol 24:587–594
Curtsinger JW, Fukui HH, Khazaeli AA, Kirscher A, Pletcher SD, Promislow SEL, Tatar M (1995) Genetic variation and aging. Annu Rev Genet 29:553–575
Cvejic S, Zhu Z, Felice SJ, Berman Y, Huang XY (2004) The endogenous ligand stunted of the GPCR Methuselah extends lifespan in Drosophila. Nature Cell Biol 6:540–546
Fortini ME, Skupski MP, Boguski MS, Hariharan IK (2000) A survey of human disease gene counterparts in the Drosophila genome. J Cell Biol 150:F23–F29
Hadler NM (1964) Genetic influence on phototaxis in Drosophila Melanogaster. Biol Bull 126:264–273
Harman D (2003) The free radical theory of aging. Antioxid Redox Sognal 5:557–561
Harman D (1995) Free radical theory of aging: alzheimer’s disease pathogenesis. AGE 18:97–119
Heisenberg M, Wolf R (1984) Vision in Drosophila. Springer, Berlin
Landis GN, Tower J (2005) Superoxide dismutase evolution and life span regulation. Mech Aging Dev 126:365–379
Lehmann FO, Dickinson MH (1998) The control of wing kinematics and flight forces in fruit flies (Drosophila spp.). J Exp Biol 201:385–401
Lehmann FO, Dickinson MH (2001) The production of elevated flight force compromises maneuverability in the fruit fly Drosophila melanogaster. J Exp Biol 204:627–635
Lin YJ, Seroude L, Benzer S (1998) Extended life-span and stress resistance in the Drosophila mutant Methuselah. Science 282:943–946
Mair W, Goymer P, Pletcher SD, Partridge L (2003) Demography of dietary restriction and death in Drosophila. Science 301:1731–1733
Marden JH, Rogina B, Montooth KL, Helfand SL (2003) Conditional Tradeoffs between aging and organismal performance of Indy long-lived mutant flies. Proc Natl Acad Sci USA 100:3369–3373
Miller GV, Hansen KN, Stark WS (1981) Phototaxis in Drosophila–R1-6 input and interaction among ocellar and compound eye receptors. J Insect Physiol 27:813–819
Osiewacz HD (1997) Genetic regulation of aging. J Mol Med 75:715–727
Papadopoulos NT, Katsoyannos BI, Kouloussis NA, Carey JR, Miiller H-G, Zhang Y (2004) High sexual signalling rates of young individuals predict extended life span in male Mediterranean fruit flies. Oecologia 138:127–134
Rubin GM, Yandell MD, Wortman JR, et al (2000) Comparative genomics of the eukaryotes. Science 287:2204–2215
Sherman A, Dickinson MH (2004) Summation of visual and mechanosensory feedback in Drosophila flight control. J Exp Biol 207:133–142
Song W, Ranjan R, Dawson-Scully K, Bronk P, Marin L, Seroude L, Lin YJ, Nie ZP, Atwood HL, Benzer S, Zinsmaier KE (2002) Presynaptic regulation of neurotransmission in Drosophila by the G protein-coupled receptor Methuselah. Neuron 36:105–119
Tammero LF, Dickinson MH (2002) Collision-avoidance and landing responses are mediated by separate pathways in the fruit fly, Drosophila melanogaster. J Exp Biol 205:2785–2798
Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, et al (2001) A mutant Drosophila insulin receptor homolog that extends lifespan and impairs neuroendocrine function. Science 292:107–110
Van Voorhies WA, Ward S (1999) Genetic and environmental conditions that increase longevity in Caenorhabditis elegans decrease metabolic rate. Proc Natl Acad Sci USA 96:1139–11403
Vaupel JW, Carey JR, Christensen K (2003) It’s never too late. Science 301:1679
Wang HD, Kazemi-Esfarjani P, Benzer S (2004) Multiple-stress analysis for isolation of Drosophila longevity genes. Proc Natl Acad Sci USA 101:12610–12615
West AP, Llamas LL, Snow PM, Benzer S, Bjorkman PJ (2001) Crystal structure of the ectodomain of Methuselah, a Drosophila G protein-coupled receptor associated with extended lifespan. Proc Natl Acad Sci USA 98:3744–3749
Zhang Y, Muller HG, Carey JR, Papadopoulos NT (2006) Behavioral trajectories as predictors in event history analysis: male calling behavior forecasts medfly longevity. Mech Ageing Dev 127:680–686
Acknowledgments
We thank Dr. Seymour Benzer who generously provided the mth and parental-line flies, Dr. Michael Dickinson who graciously shared with us his technical expertise, and Dr. Ted Wright for his valuable insights throughout this research. We also thank three anonymous reviewers for their helpful comments. Portions of this work were presented at the 34th national meeting of the Society for Neuroscience, San Diego, CA, USA.
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Petrosyan, A., Hsieh, IH. & Saberi, K. Age-Dependent Stability of Sensorimotor Functions in the Life-Extended Drosophila mutant Methuselah . Behav Genet 37, 585–594 (2007). https://doi.org/10.1007/s10519-007-9159-y
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DOI: https://doi.org/10.1007/s10519-007-9159-y