Behavior Genetics

, Volume 37, Issue 4, pp 585–594

Age-Dependent Stability of Sensorimotor Functions in the Life-Extended Drosophila mutant Methuselah

Original Paper

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.

Keywords

Drosophila Methuselah Lifespan Sensorimotor 

References

  1. Aigaki T, Seong KH, Matsuo T (2002) Longevity determination genes in Drosophila melanogaster. Mech Ageing Dev 123:1531–1541PubMedCrossRefGoogle Scholar
  2. 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 21:389–396CrossRefGoogle Scholar
  3. Autrum H (1958) Electrophysiological analysis of the visual systems in insects. Exp Cell Res 5(Suppl.):426–439Google Scholar
  4. Barja G (2004) Free radicals and aging. Trends Neurosci 27:595–600PubMedCrossRefGoogle Scholar
  5. Bokov A, Chaudhuri A, Richardson A (2004) The role of oxidative damage and stress in aging. Mech Aging Dev 125:811–826PubMedCrossRefGoogle Scholar
  6. Buchner E (1976) Elementary movement detectors in an insect visual system. Biol Cybern 24:85–101CrossRefGoogle Scholar
  7. 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 40:793–800PubMedCrossRefGoogle Scholar
  8. Cook-Wiens E, Grotewiel MS (2002) Dissociation between functional senescence and oxidative stress resistance in Drosophila. Exp Gerontol 37:1345–1355CrossRefGoogle Scholar
  9. Cosens D, Spatz HC (1978) Flicker fusion studies in lamina and receptor region of Drosophila eye. J Insect Physiol 24:587–594CrossRefGoogle Scholar
  10. Curtsinger JW, Fukui HH, Khazaeli AA, Kirscher A, Pletcher SD, Promislow SEL, Tatar M (1995) Genetic variation and aging. Annu Rev Genet 29:553–575PubMedCrossRefGoogle Scholar
  11. 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 6:540–546PubMedCrossRefGoogle Scholar
  12. 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–F29PubMedCrossRefGoogle Scholar
  13. Hadler NM (1964) Genetic influence on phototaxis in Drosophila Melanogaster. Biol Bull 126:264–273CrossRefGoogle Scholar
  14. Harman D (2003) The free radical theory of aging. Antioxid Redox Sognal 5:557–561CrossRefGoogle Scholar
  15. Harman D (1995) Free radical theory of aging: alzheimer’s disease pathogenesis. AGE 18:97–119CrossRefGoogle Scholar
  16. Heisenberg M, Wolf R (1984) Vision in Drosophila. Springer, BerlinGoogle Scholar
  17. Landis GN, Tower J (2005) Superoxide dismutase evolution and life span regulation. Mech Aging Dev 126:365–379PubMedCrossRefGoogle Scholar
  18. Lehmann FO, Dickinson MH (1998) The control of wing kinematics and flight forces in fruit flies (Drosophila spp.). J Exp Biol 201:385–401Google Scholar
  19. Lehmann FO, Dickinson MH (2001) The production of elevated flight force compromises maneuverability in the fruit fly Drosophila melanogaster. J Exp Biol 204:627–635PubMedGoogle Scholar
  20. Lin YJ, Seroude L, Benzer S (1998) Extended life-span and stress resistance in the Drosophila mutant Methuselah. Science 282:943–946PubMedCrossRefGoogle Scholar
  21. Mair W, Goymer P, Pletcher SD, Partridge L (2003) Demography of dietary restriction and death in Drosophila. Science 301:1731–1733PubMedCrossRefGoogle Scholar
  22. 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 100:3369–3373PubMedCrossRefGoogle Scholar
  23. Miller GV, Hansen KN, Stark WS (1981) Phototaxis in Drosophila–R1-6 input and interaction among ocellar and compound eye receptors. J Insect Physiol 27:813–819CrossRefGoogle Scholar
  24. Osiewacz HD (1997) Genetic regulation of aging. J Mol Med 75:715–727PubMedCrossRefGoogle Scholar
  25. 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 138:127–134PubMedCrossRefGoogle Scholar
  26. Rubin GM, Yandell MD, Wortman JR, et al (2000) Comparative genomics of the eukaryotes. Science 287:2204–2215PubMedCrossRefGoogle Scholar
  27. Sherman A, Dickinson MH (2004) Summation of visual and mechanosensory feedback in Drosophila flight control. J Exp Biol 207:133–142PubMedCrossRefGoogle Scholar
  28. 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 36:105–119PubMedCrossRefGoogle Scholar
  29. Tammero LF, Dickinson MH (2002) Collision-avoidance and landing responses are mediated by separate pathways in the fruit fly, Drosophila melanogaster. J Exp Biol 205:2785–2798PubMedGoogle Scholar
  30. 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 292:107–110PubMedCrossRefGoogle Scholar
  31. Van Voorhies WA, Ward S (1999) Genetic and environmental conditions that increase longevity in Caenorhabditis elegans decrease metabolic rate. Proc Natl Acad Sci USA 96:1139–11403CrossRefGoogle Scholar
  32. Vaupel JW, Carey JR, Christensen K (2003) It’s never too late. Science 301:1679PubMedCrossRefGoogle Scholar
  33. Wang HD, Kazemi-Esfarjani P, Benzer S (2004) Multiple-stress analysis for isolation of Drosophila longevity genes. Proc Natl Acad Sci USA 101:12610–12615PubMedCrossRefGoogle Scholar
  34. 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 98:3744–3749PubMedCrossRefGoogle Scholar
  35. 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 127:680–686PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  1. 1.Department of Cognitive SciencesUniversity of CaliforniaIrvineUSA

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