Learning and memory associated with aggression in Drosophila melanogaster - PubMed (original) (raw)

Learning and memory associated with aggression in Drosophila melanogaster

Alexandra Yurkovic et al. Proc Natl Acad Sci U S A. 2006.

Abstract

Male Drosophila melanogaster (Canton-S strain) exhibit aggression in competition for resources, to defend territory, and for access to mates. In the study reported here, we asked: (i) how long flies fight; (ii) whether flies adopt distinct winning and losing strategies as hierarchical relationships are established; (iii) whether flies exhibit experience-dependent changes in fighting strategies in later fights; and (iv) whether flies fight differently in second fights against familiar or unfamiliar opponents. The results showed that flies fought for up to 5 h. As hierarchical relationships were established, behavioral strategies changed: winners progressively lunged more and retreated less, whereas losers progressively lunged less and retreated more. Encounters between flies were frequent during the first 10 min of pairing and then dropped significantly. To ask whether flies remembered previous fights, they were re-paired with familiar or unfamiliar opponents after 30 min of separation. In familiar pairings, there were fewer encounters during the first 10 min of fighting than in unfamiliar pairings, and former losers fought differently against familiar winners than unfamiliar winners. Former losers lost or no decision was reached in all second fights in pairings with familiar or unfamiliar winners or with naive flies. Winner/winner, loser/loser, and naive/naive pairings revealed that losers used low-intensity strategies in later fights and were unlikely to form new hierarchical relationships, compared with winners or socially naive flies. These results strongly support the idea that learning and memory accompany the changes in social status that result from fruit fly fights.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Fig. 1.

Indicators of dominant and subordinate status. (A) Within the first 30 min of interaction, losers spent significantly less time on the food cup surface than winners (two-factor repeated measures ANOVA, mean ± SEM, n = 12 trials). (B) Over the course of successive encounters, winners lunged significantly more than losers (two-factor repeated measures ANOVA, mean ± SEM, n = 30 trials). (C) Losers retreated significantly more than winners (two-factor repeated measures ANOVA, mean ± SEM, n = 30 trials). (∗, P < 0.05; ∗∗, P < 0.01; ∗∗∗, P < 0.001 in post hoc Bonferroni multiple comparison test.) (D) A discriminant function based on approach, lunge, retreat, hold, chase, wing flick, and wing threat in 40 encounters classified 28 of 30 flies (93.33%) the same as the within-fight three-lunge/three-retreat rule. The x axis represents computed values of the discriminant function for individual cases and the y axis represents the number of observations in each bin of discriminant function values for winners (gray bars) and losers (white bars).

Fig. 2.

Fig. 2.

Persistence of dominance relationship and individual recognition. (A) The number of encounters between socially naive opponents drops significantly after the first 10 min from the beginning of the fight (1-factor repeated measures ANOVA, mean ± SEM, n = 43 trials; ∗∗, P < 0.05 in post hoc Dunnett's multiple comparison test). (B) Familiar opponents had significantly fewer encounters in the first 10 min than naive opponents, whereas unfamiliar opponents did not (1-factor ANOVA, mean ± SEM, n = 16, 13, 7 trials; ∗, P < 0.05 in post hoc Bonferroni multiple comparison test). (C) Losers paired with unfamiliar winners lunged more in the first 10 encounters of their second fights than losers paired with familiar losers (Kruskal–Wallis statistic 12.2, Gaussian approximation P < 0.05, Dunn's multiple comparison test fW/L vs. ufW/L P < 0.05). Lunges by losers of naive/naive pairings are included as a control.

Fig. 3.

Fig. 3.

Winner and loser strategies in re-pairings. (A) Naive/naive, winner/winner, and loser/loser pairs had similar numbers of encounters in 60 min (Kruskal–Wallis statistic 2.216, Gaussian approximation P value 0.3301). (B) Loser pairs exhibited significantly fewer lunges than naive pairs (Kruskal–Wallis statistic 8.925, Gaussian approximation P < 0.05, Dunn's multiple comparison test N/N vs. L/L P < 0.05). (C) Loser pairs exhibited significantly fewer retreats than naive pairs (Kruskal–Wallis statistic 7.5, Gaussian approximation P < 0.05, Dunn's multiple comparison test N/N vs. L/L P < 0.05). (D) Fewer loser/loser pairs formed heirarchical relationships than naive/naive and winner/winner pairs (two-sided χ2 = 14.13, df = 2, P < 0.001).

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