Female fruit flies copy the acceptance, but not the rejection, of a mate

Female fruit flies copy the acceptance, but not the rejection, of a mate. Sabine Nöbel, Magdalena Monier, Laura Fargeot, Guillaume Lespagnol, Etienne Danchin, Guillaume Isabel. Behavioral Ecology, arac071, Aug 8 2022, https://doi.org/10.1093/beheco/arac071

Abstract: Acceptance and avoidance can be socially transmitted, especially in the case of mate choice. When a Drosophila melanogaster female observes a conspecific female (called demonstrator female) choosing to mate with one of two males, the former female (called observer female) can memorize and copy the latter female’s choice. Traditionally in mate-copying experiments, demonstrations provide two types of information to observer females, namely, the acceptance (positive) of one male and the rejection of the other male (negative). To disentangle the respective roles of positive and negative information in Drosophila mate copying, we performed experiments in which demonstrations provided only one type of information at a time. We found that positive information alone is sufficient to trigger mate copying. Observer females preferred males of phenotype A after watching a female mating with a male of phenotype A in the absence of any other male. Contrastingly, negative information alone (provided by a demonstrator female actively rejecting a male of phenotype B) did not affect future observer females’ mate choice. These results suggest that the informative part of demonstrations in Drosophila mate-copying experiments lies mainly, if not exclusively, in the positive information provided by the copulation with a given male. We discuss the reasons for such a result and suggest that Drosophila females learn to prefer the successful males, implying that the underlying learning mechanisms may be shared with those of appetitive memory in non-social associative learning.

DISCUSSION

Our goal was to disentangle the role of positive and negative information during the observation of binary mate-choice decisions in D. melanogaster in order to evaluate its ecological relevance. We found that females, that received positive information only or positive and negative information at the same time, learned and copied the choice of the demonstrator females, as in previous studies (Dagaeff et al. 2016; Danchin et al. 2018; Nöbel et al. 2018; Monier et al. 2019). We further found no significant difference in the learning capacities of females of these two treatments. In contrast, females receiving only negative information did not significantly avoid the color they saw being rejected, which differs from a previous study in fish (Witte and Ueding 2003). Thus, positive information appears sufficient to elicit mate copying after one demonstration in fruit flies.

The absence of mate copying in the rejection treatment suggests that one demonstration containing rejection(s) of a male is not sufficient to elicit avoidance behavior in the observer females. This may be because a female can reject a male for reasons that are independent from its quality, like the female being non-receptive (Connolly and Cook 1973; Neckameyer 1998), as this is the case in our study. Alternatively, it may be that observer females were less interested in negative demonstrations as they did not involve copulation, in which case the negative result would simply result from a lack of interest in the demonstrations. Or it could be that the solitary male and the rejected male were evaluated in the same way, and thus, no preference was developed.

A recent study of aversive olfactory memory in Drosophila showed that an initially neutral stimulus can become attractive to fruit flies under some circumstances—the “safety memory” (Jacob and Waddell 2020). Briefly, after a multiple spaced training with sequences of conditioned stimuli (CS) simultaneously with an aversive cue (CS+) followed by another CS without reinforcement (CS−), Jacob and Waddell conclude that the individuals display both a CS + avoidance and an approach movement towards the CS- when later given the choice between the CS + and CS− odors. Thus, in our design, a sequence of several rejections (showing first a male of phenotype A rejected by a female and then a single male of another phenotype B, repeated several times) might elicit aversive learning for phenotype A leading to a choice for the male phenotype B. Interestingly, in the fruit fly larva, appetitive but not aversive olfactory stimuli support associative gustatory learning (Hendel et al. 2005). Opposite to what we observe in fruit fly females, female sailfin mollies (Poecillia latipinna) copy the rejection of a male (Witte and Ueding 2003). However, the setup used in that study was quite different from ours, as the rejection demonstration consisted of a sequence of four 12-min video of four different females escaping from a courting male, so that the rejection cue seemed much stronger than in the present study that only involved a single demonstrator female. Similarly, in humans, women, but not men, decrease their interest for a relationship to a demonstrator after watching a speed-dating video in which the demonstrator and a potential partner showed mutual lack of interest (Place et al. 2010). This can indicate that beyond the effect of the experimental conditions, different species use different social cues for mate copying. However, the motivations to reject a partner are way less studied than for building specific mating preferences.

A last alternative can be that in nature newly emerged females do not see older females choosing between only two males, but rather see females choosing among many males to copulate with one of them. The fact that the former chooses that specific male is informative in itself but the fact that she rejected all other potential male does not reveal much information about all the non-selected males. This purely statistical fact may explain the absence of an effect of seeing only a rejection.

Finally, our results suggest that in the classical Drosophila mate-copying design, the rejected male shown in the demonstration may not constitute the prominent cue triggering learning in the observer female. Moreover, the presentation of a male of the opposite color together with the copulating pair in the classical demonstration might even constitute a distractive stimulus, as indirectly suggested by Germain et al. (2016 experiment 3). In nature, females may observe copulations longer than rejection as copulations likely last for more than 30 min (Markow 2000), while rejections are brief and thus far less prominent (Gromko and Markow 1993). It is thus possible that our result is explained by the fact that D. melanogaster females evolved an ability to gather social information from the most easily detectable and reliable social cues. Alternatively, females might pay attention to rejection events too but might have difficulties in interpreting them or distinguishing them from other neutral information, such as solitary males.

Our finding that the acceptance of a male by the demonstrator female is the most relevant cue to elicit full mate copying by the observer female suggests that it involves networks of appetitive learning neurons and mechanisms rather than the aversive pathway. Several authors suggested that social learning in many contexts can have an associative explanation (e.g., Munger et al. 2010 ; Avarguès-Weber et al. 2015; Heyes and Pearce 2015; Leadbeater and Dawson 2017). For mate copying, this has yet to be proven. At the moment, asocial learning, like olfactory associative direct learning, is way better understood. Here the pairing between a conditioned stimulus (CS; for instance, odor A) and an appetitive US (sucrose) leads flies to prefer odor A over B even in the absence of any reward (Tempel et al. 1983) through the association of odor A to the reward (Schultz et al. 1997). In our social learning paradigm, we can speculate that the relevant cues eliciting learning are the color of the copulating males in association with the successful mating. Hence, the copulating pair would mediate the appetitive US, while male color would constitute the CS (Avarguès-Weber et al. 2015). Under this hypothesis, it would be interesting to study whether mate-copying mechanisms resemble those of visual, appetitive, associative learning, given that its neural bases are now well-understood (Vogt et al. 2014, 2016).

More generally, understanding how social learning works can only help sharpening our view on the evolution of the different types of learning, opening the way to new theories about the evolution of behavior, cognition, and culture in invertebrates.