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Gr39a, a Highly Diversified Gustatory Receptor in Drosophila, has a Role in Sexual Behavior

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Abstract

Sexual recognition among individuals is crucial for the reproduction of animals. In Drosophila, like in many other animals, pheromones are suggested to play an important role in conveying information about an individual, such as sex, maturity and mating status. Sex-specific cuticular hydrocarbon components are thought to be major sex pheromones in Drosophila, and are postulated to act through the gustatory system, since they are mostly non-volatile chemicals. However, very little is known about the molecular and neural bases of gustatory pheromone reception. So far, a few putative gustatory receptors, including Gr32a and Gr68a, have been implicated in courtship behavior. Here, we examine another putative gustatory receptor, Gr39a, which shares a cluster with both Gr32a and Gr68a in a molecular phylogeny of the gustatory receptor family, for its potential role in courtship behavior. The Gr39a gene produces four isoforms through alternative splicing of different 5′-most exons. A quantitative real-time PCR analysis showed that the expression levels of all four splice variants of Gr39a were reduced in a fly line in which a P element was inserted into the Gr39a locus. Homozygous and hemizygous males for the P-element insertion, as well as males in which Gr39a was knocked down by RNAi, all showed reduced courtship levels toward females. The courtship levels returned to normal when the P element was excised out. A close analysis of courtship behavior of the mutant males revealed that the average duration of a continuous courtship bout was significantly shorter in the mutants than in the wild type. The results suggest that Gr39a has a role in sustaining courtship behavior in males, possibly through the reception of a stimulating arrestant pheromone.

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Acknowledgments

We thank Kazuko Sawaguchi for her secretarial assistance, and the Bloomington Drosophila Stock Center and Vienna Drosophila RNAi Center for the provision of fly strains. This work was supported by a Specially Promoted Research grant (1802012) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) to D.Y. and M.K., a KAKENHI grant (21770074) to M.K., funds from the Tohoku University Neuroscience Global Center of Excellence Program from MEXT to D.Y., and a grant from the Japan Sciences and Technology Agency (JST) in conjunction with the Strategic Japanese-French Cooperative Program to D.Y.

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Authors and Affiliations

  1. Division of Neurogenetics, Graduate School of Life Sciences, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai, 980-8577, Japan

    Kanako Watanabe, Gakuta Toba, Masayuki Koganezawa & Daisuke Yamamoto

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  1. Kanako Watanabe
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  2. Gakuta Toba
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  3. Masayuki Koganezawa
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  4. Daisuke Yamamoto
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Correspondence to Daisuke Yamamoto.

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Edited by Yong-Kyu Kim.

K. Watanabe and G. Toba contributed equally to this work.

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Fig. S1. Locomotor activity, and its relationship to courtship activity

. (A) The locomotor activity of Gr39ak05106 mutant males was significantly lower than that of Canton-S males. Here, locomotor activity was defined as the number of times the fly crossed a reference line in the middle of an assay chamber in a 1-min observation period. Values are shown as the means ± SEM. Student’s t-test was used to evaluate the statistical significance of difference (***, P < 0.001). (B) Correlations between locomotor and courtship activities were examined for Canton-S wild-type and Gr39ak05106 mutant males. The locomotor activity of each individual was plotted against the CI of the same individual. No correlation was detected between the locomotor and courtship activities in both genotypes. Pearson’s correlation coefficients were as follows: Canton-S (r = -0.094), Gr39ak05106 (r = -0.218). The same data set of locomotor activities was used for both (A) and (B). In both (A) and (B), the numbers of males examined were as follows: Canton-S (n = 17), Gr39ak05106 (n = 27). (EPS 437 kb)

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Watanabe, K., Toba, G., Koganezawa, M. et al. Gr39a, a Highly Diversified Gustatory Receptor in Drosophila, has a Role in Sexual Behavior. Behav Genet 41, 746–753 (2011). https://doi.org/10.1007/s10519-011-9461-6

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