Skip to main content
×
Home

Extensive epistasis for olfactory behaviour, sleep and waking activity in Drosophila melanogaster

  • SHILPA SWARUP (a1) (a2), SUSAN T. HARBISON (a1) (a2), LAUREN E. HAHN (a1), TATIANA V. MOROZOVA (a2) (a3), AKIHIKO YAMAMOTO (a2) (a3), TRUDY F. C. MACKAY (a1) (a2) and ROBERT R. H. ANHOLT (a1) (a2) (a3)...
Summary
Summary

Epistasis is an important feature of the genetic architecture of quantitative traits, but the dynamics of epistatic interactions in natural populations and the relationship between epistasis and pleiotropy remain poorly understood. Here, we studied the effects of epistatic modifiers that segregate in a wild-derived Drosophila melanogaster population on the mutational effects of P-element insertions in Semaphorin-5C (Sema-5c) and Calreticulin (Crc), pleiotropic genes that affect olfactory behaviour and startle behaviour and, in the case of Crc, sleep phenotypes. We introduced Canton-S B (CSB) third chromosomes with or without a P-element insertion at the Crc or Sema-5c locus in multiple wild-derived inbred lines of the Drosophila melanogaster Genetic Reference Panel (DGRP) and assessed the effects of epistasis on the olfactory response to benzaldehyde and, for Crc, also on sleep. In each case, we found substantial epistasis and significant variation in the magnitude of epistasis. The predominant direction of epistatic effects was to suppress the mutant phenotype. These observations support a previous study on startle behaviour using the same D. melanogaster chromosome substitution lines, which concluded that suppressing epistasis may buffer the effects of new mutations. However, epistatic effects are not correlated among the different phenotypes. Thus, suppressing epistasis appears to be a pervasive general feature of natural populations to protect against the effects of new mutations, but different epistatic interactions modulate different phenotypes affected by mutations at the same pleiotropic gene.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Extensive epistasis for olfactory behaviour, sleep and waking activity in Drosophila melanogaster
      Available formats
      ×
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about sending content to Dropbox.

      Extensive epistasis for olfactory behaviour, sleep and waking activity in Drosophila melanogaster
      Available formats
      ×
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about sending content to Google Drive.

      Extensive epistasis for olfactory behaviour, sleep and waking activity in Drosophila melanogaster
      Available formats
      ×
Copyright
The online version of this article is published within an Open Access environment subject to the conditions of the Creative Commons Attribution-NonCommercial-ShareAlike licence . The written permission of Cambridge University Press must be obtained for commercial re-use.
Corresponding author
*Corresponding author: Robert R. H. Anholt, Department of Biology, Box 7617, North Carolina State University, Raleigh, NC 27695-7617, USA. Tel: (919) 515-1173. Fax: (919) 515-1801. E-mail: anholt@ncsu.edu
References
Hide All
Anholt R. R. H. (2010). Making scents of behavioural genetics: lessons from Drosophila. Genetics Research (Cambridge) 92, 349359.
Anholt R. R. H., Lyman R. F. & Mackay T. F. C. (1996). Effects of single P-element insertions on olfactory behavior in Drosophila melanogaster. Genetics 143, 293301.
Anholt R. R. H. & Mackay T. F. C. (2004). Quantitative genetic analyses of complex behaviours in Drosophila. Nature Reviews Genetics 5, 838849.
Bellen H. J., Levis R. W., Liao G., He Y., Carlson J. W., Tsang G., Evans-Holm M., Hiesinger P. R., Schulze K. L., Rubin G. M., Hoskins R. A. & Spradling A. C. (2004). The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 167, 761781.
Brockmann G. A., Kratzsch J., Haley C. S., Renne U., Schwerin M. & Karle S. (2000). Single QTL effects, epistasis, and pleiotropy account for two-thirds of the phenotypic F(2). Variance of growth and obesity in DU6i×DBA/2 mice. Genome Research 10, 19411957.
Carlborg O., Jacobsson L., Ahgren P., Siegel P. & Andersson L. (2006). Epistasis and the release of genetic variation during long-term selection. Nature Genetics 38, 418420.
Cheverud J. M., Vaughn T. T., Pletscher L. S., Peripato A. C., Adams E. S., Erikson C. F. & King-Ellison K. J. (2001). Genetic architecture of adiposity in the cross of LG/J and SM/J inbred mice. Mammalian Genome 12, 3–12.
Clark A. G. & Wang L. (1997). Epistasis in measured genotypes: Drosophila P-element insertions. Genetics 147, 157163.
Dilda C. L. & Mackay T. F. C. (2002). The genetic architecture of Drosophila sensory bristle number. Genetics 162, 16551674.
Edwards A. C. & Mackay T. F. C. (2009). Quantitative trait loci for aggressive behavior in Drosophila melanogaster. Genetics 182, 889897.
Eshed Y. & Zamir D. (1996). Less-than-additive epistatic interactions of quantitative trait loci in tomato. Genetics 143, 18071817.
Falconer D. S. & Mackay T. F. C. (1996). Introduction to Quantitative Genetics, 4/e. Reading, MA: Addison Wesley Longman.
Fedorowicz G. M., Fry J. D., Anholt R. R. H. & Mackay T. F. C. (1998). Epistatic interactions between smell-impaired loci in Drosophila melanogaster. Genetics 148, 18851891.
Flint J. & Mackay T. F. C. (2009). Genetic architecture of quantitative traits in mice, flies, and humans. Genome Research 19, 723733.
Gurganus M. C., Nuzhdin S. V., Leips J. W. & Mackay T. F. C. (1999). High-resolution mapping of quantitative trait loci for sternopleural bristle number in Drosophila melanogaster. Genetics 152, 15851604.
Harbison S. T., Carbone M. A., Ayroles J. A., Stone E. A., Lyman R. F. & Mackay T. F. C. (2009). Co-regulated transcriptional networks contribute to natural genetic variation in Drosophila sleep. Nature Genetics 41, 371375.
Harbison S. T. & Sehgal A. (2008). Quantitative genetic analysis of sleep in Drosophila melanogaster. Genetics 178, 23412360.
Hendricks J. C., Finn S. M., Panckeri K. A., Chavkin J., Williams J. A., Sehgal A. & Pack A. I. (2000). Rest in Drosophila is a sleep-like state. Neuron 25, 129138.
Hill W. G., Goddard M. E. & Visscher P. M. (2008). Data and theory point to mainly additive genetic variance for complex traits. PLoS Genetics 4, e1000008.
Ho K. S. & Sehgal A. (2005). Drosophila melanogaster: an insect model for fundamental studies of sleep. Methods in Enzymology 393, 772793.
Huber R., Hill S. L., Holladay C., Biesiadecki M., Tononi G. & Cirelli C. (2004). Sleep homeostasis in Drosophila melanogaster. Sleep 27, 628639.
Jordan K. W., Morgan T. J. & Mackay T. F. C. (2006). Quantitative trait loci for locomotor behavior in Drosophila melanogaster. Genetics 174, 271284.
Khare N., Fascetti N., DaRocha S., Chiquet-Ehrismann R. & Baumgartner S. (2000). Expression patterns of two new members of the Semaphorin family in Drosophila suggest early functions during embryogenesis. Mechanisms of Development 91, 393397.
Klingenberg C. P., Leamy L. J. & Cheverud J. M. (2004). Integration and modularity of quantitative trait locus effects on geometric shape in the mouse mandible. Genetics 166, 19091921.
Kroymann J. & Mitchell-Olds T. (2005). Epistasis and balanced polymorphism influencing complex trait variation. Nature 435, 9598.
Leips J. & Mackay T. F. C. (2000). Quantitative trait loci for life span in Drosophila melanogaster: interactions with genetic background and larval density. Genetics 155, 17731788.
Leips J. & Mackay T. F. C. (2002). The complex genetic architecture of Drosophila life span. Experimental Aging Research 28, 361390.
Long A. D., Mullaney S. L., Reid L. A., Fry J. D., Langley C. H. & Mackay T. F. C. (1995). High resolution mapping of genetic factors affecting abdominal bristle number in Drosophila melanogaster. Genetics 139, 12731291.
Mackay T. F. C., Richards S., Stone E. A., Barbadilla A., Ayroles J. F., Zhu D., Casillas S., Magwire M. M., Cridland J. M., Richardson M. F., Anholt R. R. H., Barrón M., Bess C., Blankenburg K. P., Carbone M. A., Castellano D., Chaboub L., Duncan L., Han Y., Harris Z., Javaid M., Jayaseelan J. C., Jhangiani S. N., Jordan K. W., Lara F., Lawrence F., Lee S. L., Librado P., Linheiro R. S., Lyman R. F., Mackey A. J., Munidasa M., Muzny D. M., Nazareth L., Newsham I., Perales L., Pu L.-L., Qu C., Ràmia M., Reid J. G., Rollmann S. M., Rozas J., Turlapati L., Worley K. C., Wu Y.-Q., Yamamoto A., Zhu Y., Bergman C. M., Thornton K., Mittleman D. & Gibbs R. A. (2012). The Drosophila melanogaster Genetic Reference Panel. Nature 482, 173178.
Mackay T. F. C., Stone E. A. & Ayroles J. F. (2009). The genetics of quantitative traits: challenges and prospects. Nature Reviews Genetics 10, 565577.
Manolio T. A., Collins F. S., Cox N. J., Goldstein D. B., Hindorff L. A., Hunter D. J., McCarthy M. I., Ramos E. M., Cardon L. R., Chakravarti A., Cho J. H., Guttmacher A. E., Kong A., Kruglyak L., Mardis E., Rotimi C. N., Slatkin M., Valle D., Whittemore A. S., Boehnke M., Clark A. G., Eichler E. E., Gibson G., Haines J. L., Mackay T. F. C., McCarroll S. A. & Visscher P. M. (2009). Finding the missing heritability of complex diseases. Nature 461, 747753.
Norga K. K., Gurganus M. C., Dilda C. L., Yamamoto A., Lyman R. F., Patel P. H., Rubin G. M., Hoskins R. A., Mackay T. F. C. & Bellen H. J. (2003). Quantitative analysis of bristle number in Drosophila mutants identifies genes involved in neural development. Current Biology 13, 13881396.
Phillips P. C. (2008). Epistasis – the essential role of gene interactions in the structure and evolution of genetic systems. Nature Reviews Genetics 9, 855867.
Polaczyk P. J., Gasperini R. & Gibson G. (1998). Naturally occurring genetic variation affects Drosophila photoreceptor determination. Development Genes and Evolution 207, 462470.
Prokopenko S. N., He Y., Lu Y. & Bellen H. J. (2000). Mutations affecting the development of the peripheral nervous system in Drosophila: a molecular screen for novel proteins. Genetics 156, 16911715.
Rollmann S. M., Edwards A. C., Yamamoto A., Zwarts L., Callaerts P., Norga K., Mackay T. F. C. & Anholt R. R. H. (2008). Pleiotropic effects of Drosophila neuralized on complex behaviors and brain structure. Genetics 179, 13271336.
Rollmann S. M., Magwire M. M., Morgan T. J., Özsoy E. D., Yamamoto A., Mackay T. F. C. & Anholt R. R. H. (2006). Pleiotropic fitness effects of the Tre1/Gr5a region in Drosophila. Nature Genetics 38, 824829.
Rollmann S. M., Yamamoto A., Goossens T., Zwarts L., Callaerts-Vegh Z., Callaerts P., Norga K., Mackay T. F. C. & Anholt R. R. H. (2007). The early developmental gene Semaphorin 5c contributes to olfactory behavior in adult Drosophila. Genetics 176, 947956.
Sambandan D., Yamamoto A., Fanara J. J., Mackay T. F. C. & Anholt R. R. H. (2006). Dynamic genetic interactions determine odor-guided behavior in Drosophila melanogaster. Genetics 174, 13491363.
Shaw P. J., Cirelli C., Greenspan R. J., & Tononi G. (2000). Correlates of sleep and waking in Drosophila melanogaster. Science 287, 18341837.
Sinha H., David L., Pascon R. C., Clauder-Munster S., Krishnakumar S., Nguyen M., Shi G., Dean J., Davis R. W., Oefner P. J., McCusker J. H. & Steinmetz L. M. (2008). Sequential elimination of major-effect contributors identifies additional quantitative trait loci conditioning high-temperature growth in yeast. Genetics 180, 16611670.
Spradling A. C., Bellen H. J. & Hoskins R. A. (2011). Drosophila P elements preferentially transpose to replication origins. Proceedings of the Natural Academy of Sciences USA 108, 1594815953.
Steinmetz L. M., Sinha H., Richards D. R., Spiegelman J. I., Oefner P. J., McCusker J. H. & Davis R. W. (2002). Dissecting the architecture of a quantitative trait locus in yeast. Nature 416, 326330.
Stoltzfus J. R., Horton W. J. & Grotewiel M. S. (2003). Odor-guided behavior in Drosophila requires calreticulin. Journal of Comparative Physiology A. Neuroethology Sensory, Neural and Behavioral Physiology 189, 471483.
Swarup S., Williams T. I. & Anholt R. R. H. (2011). Functional dissection of Odorant binding protein genes in Drosophila melanogaster. Genes Brain and Behavior 10, 648657.
van Swinderen B. & Greenspan R. J. (2005). Flexibility in a gene network affecting a simple behavior in Drosophila melanogaster. Genetics 169, 21512163.
Weber K., Eisman R., Morey L., Patty A., Sparks J., Tausek M. & Zeng Z. B. (1999). An analysis of polygenes affecting wing shape on chromosome 3 in Drosophila melanogaster. Genetics 153, 773786.
Workman M. S., Leamy L. J., Routman E. J. & Cheverud J. M. (2002). Analysis of quantitative trait locus effects on the size and shape of mandibular molars in mice. Genetics 160, 15731586.
Yamamoto A., Anholt R. R. H. & Mackay T. F. C. (2009). Epistatic interactions attenuate mutations affecting startle behaviour in Drosophila melanogaster. Genetics Research (Cambridge) 91, 373382.
Yamamoto A., Zwarts L., Callaerts P., Norga K., Mackay T. F. C. & Anholt R. R. H. (2008). Neurogenetic networks for startle-induced locomotion in Drosophila melanogaster. Proceedings of the Natural Academy of Sciences USA 105, 1239312398.
Yi N., Zinniel D. K., Kim K., Eisen E. J., Bartolucci A., Allison D. B. & Pomp D. (2006). Bayesian analyses of multiple epistatic QTL models for body weight and body composition in mice. Genetical Research 87, 4560.
Zwarts L., Magwire M. M., Carbone M. A., Versteven M., Herteleer L., Anholt R. R. H., Callaerts P. & Mackay T. F. C. (2011). Complex genetics architecture of Drosophila aggressive behavior. Proceedings of the Natural Academy of Sciences USA 108, 1707017075.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Genetics Research
  • ISSN: 0016-6723
  • EISSN: 1469-5073
  • URL: /core/journals/genetics-research
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×
Type Description Title
UNKNOWN
Supplementary Materials

Swarup supplementary material
Swarup supplementary material

 Unknown (1.7 MB)
1.7 MB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 13
Total number of PDF views: 132 *
Loading metrics...

Abstract views

Total abstract views: 194 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 22nd November 2017. This data will be updated every 24 hours.