When not to copy: female fruit flies use sophisticated public information to avoid mated males - PubMed
When not to copy: female fruit flies use sophisticated public information to avoid mated males
Adeline Loyau et al. Sci Rep. 2012.
Abstract
Semen limitation (lack of semen to fertilize all of a female's eggs) imposes high fitness costs to female partners. Females should therefore avoid mating with semen-limited males. This can be achieved by using public information extracted from watching individual males' previous copulating activities. This adaptive preference should be flexible given that semen limitation is temporary. We first demonstrate that the number of offspring produced by males Drosophila melanogaster gradually decreases over successive copulations. We then show that females avoid mating with males they just watched copulating and that visual public cues are sufficient to elicit this response. Finally, after males were given the time to replenish their sperm reserves, females did not avoid the males they previously saw copulating anymore. These results suggest that female fruit flies may have evolved sophisticated behavioural processes of resistance to semen-limited males, and demonstrate unsuspected adaptive context-dependent mate choice in an invertebrate.
Figures

Y axis: number of offspring imagos produced by the nth copulation. 24 hours refer to the 5th copulation that occurred 24 hours after the 4th copulations. Number of offspring imagos significantly dropped along the first four copulations (GLM: F1,172 = 44.49; p<0.0001) but returned to the initial level after 24 hours (GLM: F1,90 = 0.43, p = 0.5122). Different letters indicate significant differences (one-tailed post-hoc tests).


Females were allowed to watch male-female social interactions (Mated males copulated, Unmated males courted a female that rejected them, Virgin-control males did not encounter any female), and then were given the choice between the same two males. Observer females with social information preferred mating with the Unmated over the Mated males and the Virgin-control over the Mated males. Female showed no preference between Unmated and Virgin-control males. The horizontal dashed line corresponds to the expected values under random selection of the males.

Females were not allowed to watch male-female social interactions (Mated males copulated, Unmated males courted a female that rejected it, Virgin-control males did not encounter any female), and then were given the choice between the same two males. Observer females without visual social information showed no preference between males. The horizontal dashed line corresponds to the expected values under random selection of the males. Because experiments 1 and 2 were run in parallel, we compared results of experiments 1 and 2 for the same contrast in male type. We found a significant interaction in the case of the contrast between Mated versus Unmated males (GLM; Left panels: Mated/Unmated, male type×with vs. without information: Chi21 = 4.61, p = 0.0318) but not for the other two contrasts in male types (Middle panels: Mated/Virgin-control, male type×with vs. without information: Chi21 = 2.11, p = 0.1460; Right panel: Unmated/Virgin-control, male type×with vs. without information: Chi21 = 0.95, p = 0.3300).

Thus, in the left panel female were given the choice to copulate with one of the two males that they watched during the demonstration phase (this duplicate the situation of Fig. 3 left bars), while in the right panel males had had the same experience during demonstration but were unknown to the observer female. The demonstration phase was the same in both cases: females were allowed to watch Mated males (i.e. that copulated with a virgin female) and Unmated males (i.e. that were rejected by a refractory female) in the two peripheral vials. Females did not prefer the Unmated males over the Mated males when the males were changed while they did so when males were not changed (GLM, male type×treatment: Chi21 = 5.59, p = 0.0181). The horizontal dashed line corresponds to random mate choice.

During the demonstration, females were allowed to watch Mated and Unmated males in the two peripheral vials. Mate choice was assessed either immediately (no delay, which triplicate the situation of Fig. 3 left bars) or 24 hours later (24 hours delay). Females avoided Mated over Unmated males immediately after the demonstration but not after a 24 hours delay when they showed an opposite preference (GLM, male type×treatment: Chi21 = 10.17, p = 0.0014). The horizontal dashed line corresponds to random mate choice.
Similar articles
-
Misra S, Wolfner MF. Misra S, et al. Elife. 2020 Jul 16;9:e58322. doi: 10.7554/eLife.58322. Elife. 2020. PMID: 32672537 Free PMC article.
-
Rezaei A, Krishna MS, Santhosh HT. Rezaei A, et al. Zoolog Sci. 2015 Jan;32(1):16-24. doi: 10.2108/zs140121. Zoolog Sci. 2015. PMID: 25660692
-
Chemical Cues that Guide Female Reproduction in Drosophila melanogaster.
Billeter JC, Wolfner MF. Billeter JC, et al. J Chem Ecol. 2018 Sep;44(9):750-769. doi: 10.1007/s10886-018-0947-z. Epub 2018 Mar 19. J Chem Ecol. 2018. PMID: 29557077 Free PMC article. Review.
-
Light is required for proper female mate choice between winged and wingless males in Drosophila.
Watanabe K, Suzuki Y, Inami S, Ohashi H, Sakai T. Watanabe K, et al. Genes Genet Syst. 2018 Oct 30;93(3):119-123. doi: 10.1266/ggs.18-00004. Epub 2018 Jul 11. Genes Genet Syst. 2018. PMID: 29998908
-
An integrative view of sexual selection in Tribolium flour beetles.
Fedina TY, Lewis SM. Fedina TY, et al. Biol Rev Camb Philos Soc. 2008 May;83(2):151-71. doi: 10.1111/j.1469-185X.2008.00037.x. Biol Rev Camb Philos Soc. 2008. PMID: 18429767 Review.
Cited by
-
Romano D, Benelli G, Stefanini C. Romano D, et al. J R Soc Interface. 2021 Mar;18(176):20210056. doi: 10.1098/rsif.2021.0056. Epub 2021 Mar 17. J R Soc Interface. 2021. PMID: 33726543 Free PMC article.
-
Public information influences sperm transfer to females in sailfin molly males.
Nöbel S, Witte K. Nöbel S, et al. PLoS One. 2013;8(1):e53865. doi: 10.1371/journal.pone.0053865. Epub 2013 Jan 16. PLoS One. 2013. PMID: 23342021 Free PMC article.
-
Incestuous sisters: mate preference for brothers over unrelated males in Drosophila melanogaster.
Loyau A, Cornuau JH, Clobert J, Danchin E. Loyau A, et al. PLoS One. 2012;7(12):e51293. doi: 10.1371/journal.pone.0051293. Epub 2012 Dec 10. PLoS One. 2012. PMID: 23251487 Free PMC article.
-
The importance of life history and population regulation for the evolution of social learning.
Deffner D, McElreath R. Deffner D, et al. Philos Trans R Soc Lond B Biol Sci. 2020 Jul 20;375(1803):20190492. doi: 10.1098/rstb.2019.0492. Epub 2020 Jun 1. Philos Trans R Soc Lond B Biol Sci. 2020. PMID: 32475333 Free PMC article.
-
Social competition stimulates cognitive performance in a sex-specific manner.
Rouse J, McDowall L, Mitchell Z, Duncan EJ, Bretman A. Rouse J, et al. Proc Biol Sci. 2020 Sep 30;287(1935):20201424. doi: 10.1098/rspb.2020.1424. Epub 2020 Sep 16. Proc Biol Sci. 2020. PMID: 32933446 Free PMC article.
References
-
- Chaine A. S. & Lyon B. E. Adaptive plasticity in female mate choice dampens sexual selection on male ornaments in the lark bunting. Science 319, 459–462 (2008). - PubMed
-
- Servedio M. R., Saether S. A. & Saether G.-P. Reinforcement and learning. Evol. Ecol. 23, 109–123 (2009).
-
- Bro-Jørgensen J. Dynamics of multiple signalling systems: animal communication in a world in flux Trends Ecol. Evol. 25(5), 292–300 (2010). - PubMed
-
- Bailey N. W. Mate choice plasticity in the field cricket Telegryllus oceanicus: effects of social experience in multiple modalities. Behav. Ecol. Sociobiol. 65, 2269–2278 (2011).
Publication types
MeSH terms
LinkOut - more resources
Full Text Sources
Molecular Biology Databases