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Inbreeding Affects Locomotor Activity in Drosophila melanogaster at Different Ages

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An Erratum to this article was published on 18 October 2014

Abstract

The ability to move is essential for many behavioural traits closely related to fitness. Here we studied the effect of inbreeding on locomotor activity (LA) of Drosophila melanogaster at different ages under both dark and light regimes. We expected to find a decreased LA in inbred lines compared to control lines. We also predicted an increased differentiation between lines due to inbreeding. LA was higher in the dark compared to the light regime for both inbred and outbred control lines. As expected, inbreeding increased phenotypic variance in LA, with some inbred lines showing higher and some lower LA than control lines. Moreover, age per se did not affect LA neither in control nor in inbred lines, while we found a strong line by age interaction between inbred lines. Interestingly, inbreeding changed the daily activity pattern of the flies: these patterns were consistent across all control lines but were lost in some inbred lines. The departure in the daily pattern of LA in inbred lines may contribute to the inbreeding depression observed in inbred natural populations.

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References

  • Allada R (2003) Circadian clocks: a tale of two feedback loops. Cell 112:284–286

    Article  PubMed  Google Scholar 

  • Allada R, Chung BY (2010) Circadian organization of behavior and physiology in Drosophila. Annu Rev Physiol 72:605–624

    Article  PubMed Central  PubMed  Google Scholar 

  • Armbruster P, Reed DH (2005) Inbreeding depression in benign and stressful environments. Heredity 95:235–242

    Article  PubMed  Google Scholar 

  • Auld JR, Relyea RA (2010) Inbreeding depression in adaptive plasticity under predation risk in a freshwater snail. Biol Letters 6:222–224

    Article  Google Scholar 

  • Bahrndorff S, Kjaersgaard A, Pertoldi C, Loeschcke V, Schou TM, Skovgard H, Hald B (2012) The effects of sex-ratio and density on locomotor activity in the house fly. Musca domestica, J Insect Sci 12

    Google Scholar 

  • Bijlsma R, Bundgaard J, Boerema AC (2000) Does inbreeding affect the extinction risk of small populations? predictions from Drosophila. J Evolution Biol 13:502–514

    Article  Google Scholar 

  • Blau J (2003) A new role for an old kinase: CK2 and the circadian clock. Nat Neurosci 6:208–210

    Article  PubMed  Google Scholar 

  • Catterson JH, Knowles-Barley S, James K, Heck MMS, Harmar AJ, Hartley PS (2010) Dietary modulation of Drosophila sleep-wake behaviour. PloS One 5:e12062

  • Charlesworth D, Willis JH (2009) Fundamental concepts in genetics the genetics of inbreeding depression. Nat Rev Genet 10:783–796

    Article  PubMed  Google Scholar 

  • Chen Q, He Y, Yang K (2005) Gene therapy for Parkinson’s disease: progress and challenges. Curr Gene Ther 5:71–80

    Article  PubMed  Google Scholar 

  • Crnokrak P, Roff DA (1999) Inbreeding depression in the wild. Heredity 83:260–270

    Article  PubMed  Google Scholar 

  • Crow JF, Kimura M (1972) An introduction to population genetic theory, 5th edn. Burgess Publishing Company, University of California, Berkeley

    Google Scholar 

  • Dingemanse NJ, Reale D (2005) Natural selection and animal personality. Behaviour 142:1159–1184

    Article  Google Scholar 

  • Douglas B, Maechler M, Bolker B (2013) lme4: Linear mixed-effects models using S4 classes, 2012. R package version 0.999999-0

  • Ewer J, Frisch B, Hamblen-Coyle MJ, Rosbash M, Hall JC (1992) Expression of the period clock gene within different cell types in the brain of Drosophila adults and mosaic analysis of these cells’ influence on circadian behavioral rhythms. J Neurosci 12:3321–3349

    PubMed  Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Prentice Hall, England

    Google Scholar 

  • Fernandez JR, Grant MD, Tulli NM, Karkowski LM, McClearn GE (1999) Differences in locomotor activity across the lifespan of Drosophila melanogaster. Exp Gerontol 34:621–631

    Article  PubMed  Google Scholar 

  • Fox CW, Reed DH (2011) Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 65:246–258

    Article  PubMed  Google Scholar 

  • Frankham R (1995) Conservation genetics. Annu Rev Genet 29:305–327

    Article  PubMed  Google Scholar 

  • Fukagawa NK, Bandini LG, Young JB (1990) Effect of age on body-composition and resting metabolic-rate. Am J Physiol 259:E233–E238

    PubMed  Google Scholar 

  • Gui R (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Helfrich-Forster C (2000) Differential control of morning and evening components in the activity rhythm of Drosophila melanogaster sex-specific differences suggest a different quality of activity. J Biol Rhythms 15:135–154

    Article  PubMed  Google Scholar 

  • Hill WG, Mackay TF (2004) D. S. Falconer and Introduction to quantitative genetics. Genetics 167:1529–1536

    PubMed Central  PubMed  Google Scholar 

  • Hirth F, Reichert H (1999) Conserved genetic programs in insect and mammalian brain development. BioEssays 21:677–684

    Article  PubMed  Google Scholar 

  • Jordan KW, Morgan TJ, Mackay TFC (2006) Quantitative trait loci for locomotor behavior in Drosophila melanogaster. Genetics 174:271–284

    Article  PubMed Central  PubMed  Google Scholar 

  • Jordan KW, Carbone MA, Yamamoto A, Morgan TJ, Mackay TF (2007) Quantitative genomics of locomotor behavior in Drosophila melanogaster. Genome Biol 8:R172

    Article  PubMed Central  PubMed  Google Scholar 

  • Kjaersgaard A, Demontis D, Kristensen TN, Le N, Faurby S, Pertoldi C, Sorensen JG, Loeschcke V (2010) Locomotor activity of Drosophila melanogaster in high temperature environments: plastic and evolutionary responses. Clim Res 43:127–134

    Article  Google Scholar 

  • Konopka RJ, Benzer S (1971) Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci USA 68:2112–2116

    Article  PubMed Central  PubMed  Google Scholar 

  • Kristensen TN, Barker JSF, Pedersen KS, Loeschcke V (2008a) Extreme temperatures increase the deleterious consequences of inbreeding under laboratory and semi-natural conditions. P Roy Soc B-Biol Sci 275:2055–2061

    Article  Google Scholar 

  • Kristensen TN, Loeschcke V, Hoffmann AA (2008b) Linking inbreeding effects in captive populations with fitness in the wild: release of replicated Drosophila melanogaster lines under different temperatures. Conserv Biol 22:189–199

    Article  PubMed  Google Scholar 

  • Lebourg E (1987) The rate of living theory. Spontaneous Locomotor-Activity, aging and longevity in Drosophila melanogaster. Exp Gerontol 22:359–369

    Article  Google Scholar 

  • Lebourg E, Lints FA (1984) A songitudinal study of the effects of age on spontaneous locomotor-activity in Drosophila melanogaster. Gerontology 30:79–86

    Article  Google Scholar 

  • Loeschcke V, Hoffmann AA (2007) Consequences of heat hardening on a field fitness component in Drosophila depend on environmental temperature. Am Nat 169:175–183

    Article  PubMed  Google Scholar 

  • Long TAF, Rice WR (2007) Adult locomotory activity mediates intralocus sexual conflict in a laboratory-adapted population of Drosophila melanogaster. P Roy Soc B-Biol Sci 274:3105–3112

    Article  Google Scholar 

  • Lu B, Liu W, Guo F, Guo A (2008) Circadian modulation of light-induced locomotion responses in Drosophila melanogaster. Genes Brain Behav 7:730–739

    Article  PubMed  Google Scholar 

  • Martin JR, Raabe T, Heisenberg M (1999) Central complex substructures are required for the maintenance of locomotor activity in Drosophila melanogaster. J Comp Physiol A 185:277–288

    Article  PubMed  Google Scholar 

  • Nash HA, Scott RL, Lear BC, Allada R (2002) An unusual cation channel mediates photic control of locomotion in Drosophila. Curr Biol 12:2152–2158

    Article  PubMed  Google Scholar 

  • Nicolas G, Sillans D (1989) Immediate and latent effects of carbon-dioxide on insects. Annu Rev Entomol 34:97–116

    Article  Google Scholar 

  • Olanow CW, Tatton WG (1999) Etiology and pathogenesis of Parkinson’s disease. Annu Rev Neurosci 22:123–144

    Article  PubMed  Google Scholar 

  • Overgaard J, Sørensen JG, Jensen LT, Loeschcke V, Kristensen TN (2010) Field tests reveal genetic variation for performance at low temperatures in Drosophila melanogaster. Funct Ecol 24:186–195

    Article  Google Scholar 

  • Panda S, Hogenesch JB, Kay SA (2002) Circadian rhythms from flies to human. Nature 417:329–335

    Article  PubMed  Google Scholar 

  • Partridge L, Ewing A, Chandler A (1987) Male size and mating success in Drosophila melanogaster - the roles of male and female behavior. Anim Behav 35:555–562

    Article  Google Scholar 

  • Pittendrigh CS (1954) On temperature independence in the clock system controlling emergence time in Drosophila. Proc Natl Acad Sci USA 40:1018–1029

    Article  PubMed Central  PubMed  Google Scholar 

  • Reed DH, Fox CW, Enders LS, Kristensen TN (2012) Inbreeding-stress interactions: evolutionary and conservation consequences. Ann Ny Acad Sci 1256:33–48

    Article  PubMed  Google Scholar 

  • Roff DA (1998) Effects of inbreeding on morphological and life history traits of the sand cricket, Gryllus firmus. Heredity 81:28–37

    Article  Google Scholar 

  • Schou MF, Kristensen TN, Kellermann V, Schlötterer C, Loeschcke V (2014) A Drosophila laboratory evolution experiment points to low evolutionary potential under increased temperatures likely to be experienced in the future. J Evol Biol 27(9):1859–1868

    Article  PubMed  Google Scholar 

  • Sharp PM (1984) The effect of inbreeding on competitive male-mating ability in Drosophila melanogaster. Genetics 106:601–612

    PubMed Central  PubMed  Google Scholar 

  • Stoleru D, Peng Y, Agosto J, Rosbash M (2004) Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431:862–868

    Article  PubMed  Google Scholar 

  • Suh J, Jackson FR (2007) Drosophila Ebony activity is required in glia for the circadian regulation of locomotor activity. Neuron 55:435–447

    Article  PubMed Central  PubMed  Google Scholar 

  • Tunnicliff G, Rick JT, Connolly K (1969) Locomotor Activity in Drosophila.V. A comparative biochemical study of selectively bred populations. Comp Biochem Physiol 29:1239–1248

    Article  PubMed  Google Scholar 

  • Wheeler DA, Hamblen-Coyle MJ, Dushay MS, Hall JC (1993) Behavior in light-dark cycles of Drosophila mutants that are arrhythmic, blind, or both. J Biol Rhythms 8:67–94

    Article  PubMed  Google Scholar 

  • Whitlock MC, Fowler K (1999) The changes in genetic and environmental variance with inbreeding in Drosophila melanogaster. Genetics 152:345–353

    PubMed Central  PubMed  Google Scholar 

  • Wisco JJ, Matles H, Berrigan D (1997) Is the scaling of locomotor performance with body size constant? Ecol Entomol 22:483–486

    Article  Google Scholar 

  • Young MW, Kay SA (2001) Time zones: a comparative genetics of circadian clocks. Nat Rev Genet 2:702–715

    Article  PubMed  Google Scholar 

  • Zerr DM, Hall JC, Rosbash M, Siwicki KK (1990) Circadian fluctuations of period protein immunoreactivity in the CNS and the visual system of Drosophila. J Neurosci 10:2749–2762

    PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank Doth Andersen for technical assistance. We also would like to thank Janneke Wit for helpful comments on the manuscript. The Faculty of Science and Technology, Aarhus University supported the PhD project of TM and we wish to thank the Danish Natural Science Research Council for financial support to VL and CP (Grant Numbers: #21-01-0526, #21-03-0125 and 95095995) and AK (Grant Number: #0602-01916B).

Conflict of Interest

Tommaso Manenti, Cino Pertoldi, Neda Nasiri, Mads Fristrup Schou, Anders Kjærsgaard, Sandro Cavicchi, and Volker Loeschcke declare that they have no conflict of interest.

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Correspondence to Tommaso Manenti.

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Manenti, T., Pertoldi, C., Nasiri, N. et al. Inbreeding Affects Locomotor Activity in Drosophila melanogaster at Different Ages. Behav Genet 45, 127–134 (2015). https://doi.org/10.1007/s10519-014-9683-5

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