Drosophila melanogaster females change mating behaviour and offspring production based on social context

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1737, 2012, Pages 2417-2425

  Billeter, Jean Christophe ^a,b   Jagadeesh, Samyukta ^a   Stepek, Nancy ^a   Azanchi, Reza ^a   Levine, Joel D ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Bruce effect; Drosophila melanogaster; Mate choice; Reproduction; Social behaviour; Sperm competition

Indexed keywords

DROSOPHILA MELANOGASTER; RODENTIA;

ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; COMPARATIVE STUDY; DROSOPHILA MELANOGASTER; FEMALE; GENETIC VARIABILITY; GENETICS; MALE; ODOR; PHYSIOLOGY; REPRODUCTION; REPRODUCTIVE FITNESS; SEXUAL BEHAVIOR; SOCIAL ENVIRONMENT; STATISTICAL MODEL;

ANALYSIS OF VARIANCE; ANIMALS; DROSOPHILA MELANOGASTER; FEMALE; GENETIC FITNESS; GENETIC VARIATION; LINEAR MODELS; MALE; REPRODUCTION; SEXUAL BEHAVIOR, ANIMAL; SMELL; SOCIAL ENVIRONMENT;

EID: 84865193480     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2011.2676     Document Type: Article

References (42)

1. Allee, W. C. 1938 The social life of animals. New York, NY: W.W. Norton and Co.
2. Clutton-Brock, T. 2002 Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296, 69–72. (doi:10.1126/science.296.5565.69)
3. Moore, A., Brodie III, E. & Wolf, J. 1997 Interacting phenotypes and the evolutionary process. I. Direct and indirect genetic effects of social interactions. Evolution 51, 1352–1362.
4. Wolf, J., Brodie III, E., Cheverud, J., Moore, A. & Wade, M. 1998 Evolutionary consequences of indirect genetic effects. Trends Ecol. Evol. 13, 64–69. (doi:10.1016/S0169-5347(97)01233-0)
5. Mcglothlin, J. W., Moore, A. J., Wolf, J. B. & Brodie, III, E. 2010 Interacting phenotypes and the evolutionary process. III. social evolution. Evolution 64, 2558–2574.
6. Formica, V. A., Mcglothlin, J. W., Wood, C. W., Augat, M. E., Butterfield, R. E., Barnard, M. E. & Brodie III, E. D. 2011 Phenotypic assortment mediates the effect of social selection in a wild beetle population. Evolution 65, 2771–2781. (doi:10.1111/j.1558-5646.2011.01340.x)
7. Spieth, H. T. 1974 Courtship behavior in Drosophila. Annu. Rev. Entomol. 19, 385–405. (doi:10.1146/annurev.en.19.010174.002125)
8. Wertheim, B., Allemand, R., Vet, L. & Dicke, M. 2006 Effects of aggregation pheromone on individual behaviour and food web interactions: a field study on Drosophila. Ecol. Entomol. 31, 216–226. (doi:10.1111/j. 1365-2311.2006.00757.x)
9. Sarin, S. & Dukas, R. 2009 Social learning about egg-laying substrates in fruitflies. Proc. R. Soc. B. 276, 4323–4328. (doi:10.1098/rspb.2009.1294)
10. Tinette, S., Zhang, L. & Robichon, A. 2004 Cooperation between Drosophila flies in searching behavior. Genes Brain Behav. 3, 39–50.(doi:10.1046/j.1601-183x.2003.0046.x)
11. Petfield, D., Chenoweth, S. F., Rundle, H. D. & Blows, M. W. 2005 Genetic variance in female condition predicts indirect genetic variance in male sexual display traits. Proc. Natl Acad. Sci. USA. 102, 6045–6050. (doi:10.1073/pnas.0409378102)
12. Hine, E., Chenoweth, S. F. & Blows, M. W. 2004 Multivariate quantitative genetics and the lek paradox: genetic variance in male sexually selected traits of Drosophila serrata under field conditions. Evolution 58, 2754–2762.
13. Saltz, J. B. & Foley, B. R. 2011 Natural genetic variation in social niche construction: social effects of aggression drive disruptive sexual selection in Drosophila melanogaster. Am. Nat. 177, 645–654. (doi:10.1086/659631)
14. Levine, J. D., Funes, P., Dowse, H. B. & Hall, J. C. 2002 Resetting the circadian clock by social experience in Drosophila melanogaster. Science 298, 2010–2012. (doi:10.1126/science.1076008)
15. Krupp, J. J., Kent, C., Billeter, J.-C., Azanchi, R., So, A. K. C., Schonfeld, J. A., Smith, B. P. & Levine, J. D. 2008 Social experience modifies pheromone expression and mating behavior in male Drosophila melanogaster. Curr. Biol. 18, 1373–1383. (doi:10.1016/j.cub.2008.07.089)
16. Kent, C., Azanchi, R., Smith, B., Formosa, A. & Levine, J. D. 2008 Social context influences chemical communication in D. melanogaster males. Curr. Biol. 18, 1384–1389. (doi:10.1016/j.cub.2008.07.088)
17. Arnqvist, G. & Nilsson, T. 2000 The evolution of polyandry: multiple mating and female fitness in insects. Anim. Behav. 60, 145–164. (doi:10.1006/anbe.2000.1446)
18. Jennions, M. & Petrie, M. 2000 Why do females mate multiply? A review of the genetic benefits. Biol. Rev. 75, 21–64. (doi:10.1017/S0006323199005423)
19. Birkhead, T. R. & Pizzari, T. 2002 Postcopulatory sexual selection. Nat. Rev. Genet. 3, 262–273. (doi:10.1038/nrg774)
20. Clark, A. G., Begun, D. J. & Prout, T. 1999 Female x male interactions in Drosophila sperm competition. Science 283, 217–220. (doi:10.1126/science.283.5399.217)
21. Manier, M. K., Belote, J. M., Berben, K. S., Novikov, D., Stuart, W. T. & Pitnick, S. 2010 Resolving mechanisms of competitive fertilization success in Drosophila melanogaster. Science 328, 354–357. (doi:10.1126/science.1187096)
22. Brown, W. D., Bjork, A., Schneider, K. & Pitnick, S. 2004 No evidence that polyandry benefits females in Drosophila melanogaster. Evolution 58, 1242–1250.
23. Byrne, P. G. & Rice, W. R. 2005 Remating in Drosophila melanogaster: an examination of the trading-up and intrinsic male-quality hypotheses. J. Evol. Biol. 18, 1324–1331. (doi:10.1111/j.1420-9101.2005.00918.x)
24. Morrow, E. H., Stewart, A. D. & Rice, W. R. 2005 Patterns of sperm precedence are not affected by female mating history in Drosophila melanogaster. Evolution 59, 2608–2615.
25. Imhof, M., Harr, B., Brem, G. & Schlötterer, C. 1998 Multiple mating in wild Drosophila melanogaster revisited by microsatellite analysis. Mol. Ecol. 7, 915–917. (doi:10.1046/j.1365-294x.1998.00382.x)
26. Lefevre, G. & Jonsson, U. 1962 sperm transfer, storage, displacement, and utilization in Drosophila melanogaster. Genetics 42, 1719–1736.
27. Ochando, M. D., Reyes, A. & Ayala, F. J. 1996 Multiple paternity in two natural populations (orchard and vineyard) of Drosophila. Proc. Natl Acad. Sci. USA 93 769–773.
28. Kuijper, B. & Morrow, E. 2009 Direct observation of female mating frequency using time-lapse photography. Fly 3, 1–3.(doi:10.4161/fly.3.1.7904)
29. Liu, H. & Kubli, E. 2003 Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 100, 9929–9933. (doi:10.1073/pnas.1631700100)
30. Chapman, T., Bangham, J., Vinti, G., Seifried, B., Lung, O., Wolfner, M. F., Smith, H. K. & Partridge, L. 2003 The sex peptide of Drosophila melanogaster: female postmating responses analyzed by using RNA interference. Proc. Natl Acad. Sci. USA 100, 9923–9928. (doi:10.1073/pnas.1631635100)
31. Yapici, N. Y., Kim, Y. J., Ribeiro, C. & Dickson, B. J. 2007 A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature 451, 33–37. (doi:10.1038/nature06483)
32. Larsson, M. C., Domingos, A. I., Jones, W. D., Chiappe, M. E., Amrein, H. & Vosshall, L. B. 2004 Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43, 703–714. (doi:10. 1016/j.neuron.2004.08.019)
33. Fitzpatrick, M. J., Feder, E., Rowe, L. & Sokolowski, M. B. 2007 Maintaining a behaviour polymorphism by frequency-dependent selection on a single gene. Nature 447, 210–212. (doi:10.1038/nature05764)
34. Bastock, M. 1956A gene mutation which changes a behavior pattern. Evolution 10, 421–439. (doi:10.2307/2407002)
35. Ferveur, J.-F. 2010 Drosophila female courtship and mating behaviors: sensory signals, genes, neural structures and evolution. Curr. Opin. Neurobiol. 20, 1–6. (doi:10.1016/S0959-4388(10)00021-8)
36. Giardina, T. J., Beavis, A., Clark, A. G. & Fiumera, A. C. 2011 Female influence on pre- and post-copulatory sexual selection and its genetic basis in Drosophila melanogaster. Mol. Ecol. 20, 4098–4108. (doi:10.1111/j. 1365-294X.2011.05253.x)
37. Rice, W. R., Stewart, A. D., Morrow, E. H., Linder, J. E., Orteiza, N. & Byrne, P. G. 2006 Assessing sexual conflict in the Drosophila melanogaster laboratory model system. Phil. Trans. R. Soc. B 361, 287–299. (doi:10.1098/rstb. 2005.1787)
38. Snook, R. R. & Hosken, D. J. 2004 Sperm death and dumping in Drosophila. Nature 428, 939–941. (doi:10. 1038/nature02455)
39. Bruce, H. M. & Parrott, D. M. 1960 Role of olfactory sense in pregnancy block by strange males. Science 131, 1526. (doi:10.1126/science.131.3412.1526)
40. Tauber, E., Roe, H., Costa, R., Hennessy, J. M. & Kyria-cou, C. P. 2003 Temporal mating isolation driven by a behavioral gene in Drosophila. Curr. Biol. 13, 140–145. (doi:10.1016/S0960-9822(03)00004-6)
41. Drnevich, J. 2003 Number of mating males and mating interval affect last-male sperm precedence in Tenebrio molitor. Anim. Behav. 66, 349–357. (doi:10.1006/anbe. 2003.2219)
42. Zeh, J. & Zeh, D. 1994 Last-male sperm precedence breaks down when females mate with 3 males. Proc. R. Soc. Lond. B 257, 287–292. (doi:10.1098/rspb. 1994.0127)