Eur. J. Entomol. 114: 439-445, 2017 | DOI: 10.14411/eje.2017.056

Gut microbiota influences female choice and fecundity in the nuptial gift-giving species, Drosophila subobscura (Diptera: Drosophilidae)

Benjamin S. WALSH, Chloe HEYS, Zenobia LEWIS*
School of Life Sciences / Institute of Integrative Biology, University of Liverpool, Crown Street, L69 7ZB Liverpool, UK; e-mails: bwalsh@liverpool.ac.uk, bs0u911f@liverpool.ac.uk, z.lewis@liverpool.ac.uk

Recently, there has been rapidly growing interest in the effects of the microbiota on host physiology and behaviour. Due to the nutritional value of bacteria, gut microflora may be particularly important in species that present nuptial gifts during courtship. Here, we explore whether the presence or absence of gut microbiota in males and females of the nuptial gift-giving species Drosophila subobscura (Collin, 1936) alters mating behaviour in terms of female preference, male investment, and female fecundity. We found that females that had been fed antibiotics, compared to females with intact gut bacteria, were more willing to mate with a male that had been fed normally. However female fecundity was higher when both males and females lacked gut bacteria compared to both individuals having a full complement of gut bacteria. This implies that the presence of the microbiota acts to reduce female fecundity in this species, and that male gut bacterial content influences female fecundity. Our results provide further evidence to the growing consensus that the microbiota of an individual may have important effects on both reproductive behaviour and physiology, and suggest that it may also contribute to the nutritional value of the nuptial gift in this system.

Keywords: Diptera, Drosophilidae, Drosophila subobscura, microbiota, gut bacteria, mate preference, reproductive success

Received: August 2, 2017; Accepted: October 9, 2017; Published online: October 23, 2017Show citation

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WALSH, B.S., HEYS, C., & LEWIS, Z. (2017). Gut microbiota influences female choice and fecundity in the nuptial gift-giving species, Drosophila subobscura (Diptera: Drosophilidae). Eur. J. Entomol.114(1), 2017.000. doi: 10.14411/eje.2017.056.
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References

  1. Albo M.J., Bilde T. & Uhl G. 2013: Sperm storage mediated by cryptic female choice for nuptial gifts. - Proc. R. Soc. Lond. (B) 280: 20131735, 6 pp. Go to original source...
  2. Bacigalupe L.D., Crudgington H.S., Hunter F., Moore A.J. & Snook R.R. 2007: Sexual conflict does not drive reproductive isolation in experimental populations of Drosophila pseudoobscura. - J. Evol. Biol. 20: 1763-1771. Go to original source...
  3. Ben-Yosef M., Jurkevitch E. & Yuval B. 2008: Effect of bacteria on nutritional status and reproductive success of the Mediterranean fruit fly Ceratitis capitata. - Physiol. Entomol. 3: 145-154. Go to original source...
  4. Brucker R.M. & Bordenstein S.R. 2013: The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia. - Science 341: 667-669. Go to original source...
  5. Debelle A., Ritchie M.G. & Snook R.R. 2014: Evolution of divergent female mating preference in response to experimental sexual selection. - Evolution 68: 2524-2533. Go to original source...
  6. Drew R.A.I., Courtice A.C. & Teakle D.S. 1983: Bacteria as a natural source of food for adult fruit flies (Diptera: Tephritidae). - Oecologia 60: 279-284. Go to original source...
  7. Everaerts C., Lacaille F. & Ferveur J.F. 2010: Is mate choice in Drosophila males guided by olfactory or gustatory pheromones? - Anim. Behav. 79: 1135-1146. Go to original source...
  8. Haine E.R., Pickup N.J. & Cook J.M. 2005: Horizontal transmission of Wolbachia in a Drosophila community. - Ecol. Entomol. 4: 464-472. Go to original source...
  9. Hamm C.A., Begun D.J., Vo A., Smith C.C.R., Saelao P., Shaver A.O., Jaenike J. & Turelli M. 2014: Wolbachia do not live by reproductive manipulation alone: infection polymorphism in Drosophila suzukii and D. subpulchrella. - Mol. Ecol. 23: 4871-4885. Go to original source...
  10. Harcourt A.H., Harvey P.H., Larson S.G. & Short R.V. 1981: Testis weight, body weight and breeding system in primates. - Nature 293: 55-57. Go to original source...
  11. Hartig F. 2017: DHARMa: Residual Diagnostics for Hierarchical (Multi-Level / Mixed) Regression Models. R Package Version 0.1.5. https://CRAN.R-project.org/package=DHARMa
  12. IBM Corporation 2013: IBM SPSS Statistics for Windows, Version 22.0. IBM Corp., Armonk, NY.
  13. Immonen E., Hoikkala A., Kazem A. & Ritchie M. 2009: When are vomiting males attractive? Sexual selection on condition-dependent nuptial feeding in Drosophila subobscura. - Behav. Ecol. 20: 289-295. Go to original source...
  14. Jennions M.D. & Passmore N.I. 1993: Sperm competition in frogs: testis size and a 'sterile male' experiment on Chiromantis xerampelina (Rhacophoridae). - Biol. J. Linn. Soc. 50: 211-220.
  15. Koukou K., Pavlikaki H., Kilias G., Werren J.H., Bourtzis K. & Alahiotis S.N. 2006: Influence of antibiotic treatment and Wolbachia curing on sexual isolation among Drosophila melanogaster cage populations. - Evolution 60: 87-96. Go to original source...
  16. Krimbas C.B. 1993: Drosophila subobscura: Biology, Genetics and Inversion Polymorphism. Dr Kovac, Hamburg, 395 pp.
  17. Lewis Z. & Lizé A. 2015: Insect behaviour and the microbiome. - Curr. Op. Ins. Sci. 9: 86-90. Go to original source...
  18. Lizé A., McKay R. & Lewis Z. 2014: Kin recognition in Drosophila: the importance of ecology and gut microbiota. - Internat. Soc. Micro. Ecol. J. 8: 469-477.
  19. Mazzetto F., Gonella E. & Alma A. 2015: Wolbachia infection affects female fecundity in Drosophila suzukii. - Bull. Insectol. 68: 153-157.
  20. Pradel E., Zhang Y., Pujol N., Matsuyama T., Bargmann C.I. & Ewbank J.J. 2007: Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans. - Proc. Natn. Acad. Sci. USA 104: 2295-2300. Go to original source...
  21. Price T.A.R., Lizé A., Marcello M. & Bretman A. 2012: Experience of mating rivals causes males to modulate sperm transfer in the fly Drosophila pseudoobscura. - J. Insect Physiol. 58: 1669-1675. Go to original source...
  22. R Core Team 2015: R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
  23. Ridley E.V., Wong A.C., Westmiller S. & Douglas A.E. 2012: Impact of the resident microbiota on the nutritional phenotype of Drosophila melanogaster. - PLoS One 7(5): e36765, 7 pp. Go to original source...
  24. Rosengaus R.B., Zecher C.N., Shultheis K.F., Bruker R.M. & Bordenstein S.R. 2011: Disruption of the termite gut microbiota and its prolonged consequences for fitness. - Appl. Environ. Microbiol. 77: 4303-4312. Go to original source...
  25. Sang J.H. 1956: The quantitative nutritional requirements of Drosophila melanogaster. - J. Exp. Biol. 33: 45-72.
  26. Scott D., Shields A., Straker M., Dalrymple H., Dhillon P.K. & Harbinder S. 2011: Variation in the male pheromones and mating success of wild caught Drosophila melanogaster. - PLoS One 6(8): e23645, 8 pp. Go to original source...
  27. Sharon G., Segal D., Ringo J.M., Hefetz A., Zilver-Rosenberg I. & Rosenberg E. 2010: Commensal bacteria play a role in mating preference of Drosophila melanogaster. - Proc. Natn. Acad. Sci. USA 107: 20051-20056. Go to original source...
  28. Sharon G., Segal D., Zilber-Rosenberg I. & Rosenberg E. 2011: Symbiotic bacteria are responsible for diet-induced mating preference in Drosophila melanogaster, providing support for the hologenome concept of evolution. - Gut Microb. 2: 190-192. Go to original source...
  29. Thornhill R. & Alcock J. 1983: The Evolution of Insect Mating Systems. Harvard University Press, Harvard, 547 pp.
  30. Verspoor R., Cuss M. & Price T.A.R. 2015: Age-based mate choice in the monandrous fruit fly Drosophila subobscura. - Anim. Behav. 102: 199-207. Go to original source...
  31. Wong A.C., Dobson A.J. & Douglas A.E. 2014: Gut microbiota dictates the metabolic response of Drosophila to diet. - J. Exp. Biol. 217: 1894-1901. Go to original source...
  32. Zhang Y., Lu H. & Bargmann C.I. 2005: Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. - Nature 438: 179-184. Go to original source...