2-D sex images elicit mate copying in fruit flies.

Although the environment is three-dimensional (3-D), humans are able to extract subtle information from two-dimensional (2-D) images, particularly in the domain of sex. However, whether animals with simpler nervous systems are capable of such information extraction remains to be demonstrated, as this ability would suggest a functional generalisation capacity. Here, we performed mate-copying experiments in Drosophila melanogaster using 2-D artificial stimuli. Mate copying occurs when naïve females observe the mating success of potential mates and use that social information to build their own mating preference. By replacing live demonstrations with (i) photos or (ii) simplified images of copulating pairs, we found that even crudely simplified images of sexual intercourse still elicit mate copying, suggesting that Drosophila is able to extract sex-related information even from a degraded image. This new method constitutes a powerful tool to further investigate mate copying in that species and sexual preferences in general.

Cultural flies: Conformist social learning in fruitflies predicts long-lasting mate-choice traditions.

Despite theoretical justification for the evolution of animal culture, empirical evidence for it beyond mammals and birds remains scant, and we still know little about the process of cultural inheritance. In this study, we propose a mechanism-driven definition of animal culture and test it in the fruitfly. We found that fruitflies have five cognitive capacities that enable them to transmit mating preferences culturally across generations, potentially fostering persistent traditions (the main marker of culture) in mating preference. A transmission chain experiment validates a model of the emergence of local traditions, indicating that such social transmission may lead initially neutral traits to become adaptive, hence strongly selecting for copying and conformity. Although this situation was suggested decades ago, it previously had little empirical support.

Effects of a sex ratio gradient on female mate-copying and choosiness in Drosophila melanogaster.

In many sexually reproducing species, individuals can gather information about potential mates by observing their mating success. This behavioral pattern, that we call mate-copying, was reported in the fruit fly Drosophila melanogaster where females choosing between 2 males of contrasting phenotypes can build a preference for males of the phenotype they previously saw being chosen by a demonstrator female. As sex ratio is known to affect mate choice, our goal was to test whether mate-copying is also affected by encountered sex ratios. Thus, we created a gradient of sex ratio during demonstrations of mate-copying experiments by changing the number of females observing from a central arena 6 simultaneous demonstrations unfolding in 6 peripheral compartments of a hexagonal device. We also tested whether the sex ratio experienced by females during demonstrations affected their choosiness (male courtship duration and double courtship rate) in subsequent mate-choice tests. Experimental male:female sex ratio during demonstrations did not affect mate-copying indices, but positively affected the proportion of both males courting the female during mate-choice tests, as well as male courtship duration, the latter potentially explaining the former relationship. As expected, the sex ratio affected female choosiness positively, and Drosophila females seem to have evolved a mate-copying ability independently of sex ratio, and a capacity to adapt their choosiness to male availability. This suggests that, as in many animal species, individuals, especially females, can adapt their mate choice depending on the current sex ratio.

Dopamine and Serotonin Are Both Required for Mate-Copying in Drosophila melanogaster.

Mate-copying is a form of social learning in which the mate-choice decision of an individual (often a female) is influenced by the mate-choice of conspecifics. Drosophila melanogaster females are known to perform such social learning, and in particular, to mate-copy after a single observation of one conspecific female mating with a male of one phenotype, while the other male phenotype is rejected. Here, we show that this form of social learning is dependent on serotonin and dopamine. Using a pharmacological approach, we reduced dopamine or serotonin synthesis in adult virgin females with 3-iodotyrosine (3-IY) and DL-para-chlorophenylalanine (PCPA), respectively, and then tested their mate-copying performance. We found that, while control females without drug treatment copied the choice of the demonstrator, drug-treated females with reduced dopamine or serotonin chose randomly. To ensure the specificity of the drugs, the direct precursors of the neurotransmitters, either the dopamine precursor L-3,4-dihydroxyphenylalanine (L-DOPA) or the serotonin precursor 5-L-hydroxytryptophan (5-HTP) were given together with the drug, (respectively 3-IY and PCPA) resulting in a full rescue of the mate-copying defects. This indicates that dopamine and serotonin are both required for mate-copying. These results give a first insight into the mechanistic pathway underlying this form of social learning in D. melanogaster.