Identification of centres for sex-specific behaviour in the fly brain

KEVIN M.C. O'DELL (p) §, XIN AN #, KIM KAISER #, J. STEVEN DE BELLE %,

# Division of Molecular Genetics, Glasgow University, Glasgow G11 5JS, Scotland, % Max-Planck-Institut für Biologische Kybernetik, D-72076 Tübingen,

Drosophila males and females show distinct, sex-specific courtship behaviour that is clearly innate, but quite how this is mediated by the brain is unclear. Here we address the question of whether gender is built into the brain as a whole or if sexuality is conferred by multiple sex-specific foci. If such foci exist, we could further ask whether gender-specific foci coincide anatomically.

Mushroom bodies (MBs) are important for olfactory learning in flies1. Mosaic analysis also implicates the MBs as a focus for sex-specific behaviour in courtship2. We have previously reported the use of the P[GAL4] enhancer-trap system to express the female-specific transformer (tra) transcript for “feminising” specific sub-domains within the male brain3. Coupled with the work of Ferveur et al.4, we have shown that feminisation of specific sub-domains in either the antennal lobe or MBs leads to males exhibiting non-discriminatory courtship.

Non-discriminatory courtship by partially feminised males implies the existence of gender-specific mate discrimination centres in the brain5. tra-induced bisexual behaviour could be a consequence of feminisation, or simply due to the loss of “maleness”. If we suppose a MB focus for male detection of male “anti-aphrodisiac” pheromonal cues, feminisation would lead to a loss of function. On the other hand, if MBs are a focus for female detection of male “aphrodisiac” pheromonal cues, feminisation would lead to a gain (or change) of function.

We have looked at whether MBs are required for apparently normal courtship in wild-type Canton-S and mushroom body miniature (mbm) mutants combined with MB ablation [using hydroxyurea (HU)1]. To confirm previous findings of a MB sub-domain-focus for bisexual courtship by partially MB-feminized males, we compared MB-specific- and explicitly non-MB-specific P[GAL4]-mediated tra-expressing lines in combination with HU ablation. Several outcomes are possible. If MBs are a “female courtship focus” only, we might expect MB ablation to have no effect on male courtship, whereas, MB-less females should be unreceptive to male courters. Ablation should also revert the sexual preferences of partially feminised bisexual males toward females. If ablation has no effect in the latter case, this would indicate that other non-MB tissues are the “female courtship focus” and have been feminized. On the other hand, if MBs are a “male courtship focus” only, ablation should reduce male courtship directed toward females but have no effect on female receptivity to males.

Finally, other groups have reported a male-male courtship effect of heat-shock mini-white contructs6 (which we use to elicit ectopic tra expression5). However, this does not explain our observations (see abstract by An et al.).

  1. de Belle and Heisenberg, 1994, Science 263, 692.
  2. Siegal and Hall, 1979, PNAS 76, 3430.
  3. O’Dell et al., 1995, Neuron 15, 55.
  4. Ferveur et al., 1995, Science 267, 902.
  5. de Belle, 1995, Neuron 15, 245.
  6. Zhang and Odenwald, 1995, PNAS 92, 5525.