Drosophila female courtship and mating behaviors: sensory signals, genes, neural structures and evolution

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Interest in Drosophila courtship behavior has a long-standing tradition, starting with the works by Sturtevant in 1915, and by Bastock and Manning in the 50s. The neural and genetic base of Drosophila melanogaster courtship behavior has made big strides in recent years, but the studies on males far outnumber those on females. Recent technical developments have made it possible to begin to unravel the biological substrates underlying the complexity of Drosophila female sexual behavior and its decisive effect on mating success. The present review focus more on the female side and summarizes the sensory signals that the male sends, using multiple channels, and which neural circuits and genes are mediating sex-specific behavioral responses.

Section snippets

Introduction: Drosophila female courtship behavior has been poorly studied so far

Sexual selection acting through female choice of the best mate is an extremely important process in shaping the evolution of animal communication [1]. For this reason, female sexual behavior has been extensively investigated in many species, but not in Drosophila melanogaster, one of the best-studied model organisms. In this species, males show very obvious courtship behaviors which are easy to observe and quantify [2] whereas the most conspicuous behaviors shown by females are what appear to

Effect of multiple male sensory signals

There is an obvious sexual dimorphism in D. melanogaster premating behavior, but a detailed description of courtship is necessary to detect the subtle behavioral sequences that are crucial for mating success. Detailed analysis of the dynamic interaction between the two partners has allowed us to determine the nature of the sensory signals involved and to pinpoint the tissues involved in the emission and perception of these signals. Such fine-grained analysis has revealed the existence of

Genes and neural substrate involved

Genes of the sex determination pathway such as transformer (tra), transformer 2 (tra2), fru and doublesex (dsx) play a pivotal role in the realisation of sex-specific behaviors [34]. The sexual identity of sex-specific neurons seems to be specified by the presence/absence of fru and/or dsx [35, 36]. In particular, females expressing the male fru products (FruM) court as though they were males [37] although much less vigorously and in a very simplified manner [38]. Moreover, male-like courtship

Copulatory and postmating behaviors

Copulation posture and duration are also influenced by both sex partners. The male is normally positioned centrally on the back of the female. This posture is altered after the ablation of a single male genital hair, suggesting that this hair contributes to bilateral symmetry in the mating posture [51]. In wild-type strains, copulation duration is normally very stable (≈15 min) but can vary slightly (±2 min) through the influence of female contact pheromones [30] and a previous mating experience

Plasticity and evolutionary aspects

Learning can affect D. melanogaster female mate choice. The female will gain benefits from selecting the best mate, but her reproductive success may decrease if she postpones mating and egg-laying due to excessive choosiness. Immature females (<2 days old) and females in the postmating refractory period, do not accept courtship. When exposed to courting males, such females learn some of males’ traits such as size and mating ability. If a naive female prefers large size males, her preference can

Conclusion and perspectives

In comparison to the wealth of data on male courtship in D. melanogaster, very few reports have dealt with D. melanogaster female behavior during courtship and the best studied female behaviors are related to her reluctance to mate (in both premating and postmating states). Female precopulatory behavior and its interaction with male courtship can be studied by the targeted manipulation of genes and neurons in either sex partner, allowing us to determine the precise relationship between the

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

I warmly thank Daisuke Yamamoto, Takaomi Sakai, Stephen Goodwin and Matthew Cobb for critical reading and suggestions on the manuscript, the CNRS and the Burgundy Regional Council for support and funding.

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