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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.

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Figures

Figure 1
Figure 1. Differences in adult offspring production over 5 successive copulations by males.

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).

Figure 2
Figure 2. Experimental set up.
Figure 3
Figure 3. Drosophila melanogaster female use of social information in mate choice (Experiment 1).

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.

Figure 4
Figure 4. Female mate choice without social information (Experiment 2, run in parallel with Experiment 1).

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).

Figure 5
Figure 5. Female copulation frequency with Mated and Unmated males according to whether males were not changed between the demonstration and test phases (left panel), or were swapped with males of identical copulation histories and phenotypes in another experimental setting (right panel; Experiment 3).

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.

Figure 6
Figure 6. Female mate choice when there was a 24 hours delay between the demonstration and test phases (Experiment 4).

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.

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