Chemical stimuli induce courtship dominance in Drosophila

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FFA increased. Eye gaze is an important source in reading a person’s desires and intentions. Normally the posterior part of the right superior temporal sulcus (STS) shows heightened activation when we see another person gazing into an unexpected direction. This activation is reduced in ASD and suggests a disconnection between the perceptual processing of gaze and the social interpretation of its meaning. The STS region, which is implicated in the perception of biological motion and the attribution of mental states, has been found to be hypo-functional during resting state in children with ASD and also shows anatomical differences (Figure 3). This region is also involved in the processing of eye gaze. A new target of theories trying to explain social deficits in autism is the ‘mirror neuron system’. This system contains neurons that fire equally when a specific goaldirected action is either performed by the self or observed to be performed by another. Mirror-neurons have been hypothesized to be implicated in the development of imitation, in emotional contagion, in the development of empathic responsiveness and theory of mind. Future outlook The progress that is now possible by combining cognitive theories, functional and structural brain imaging in genetically sensitive designs, should yield some long awaited answers. In particular, it should become clear which features of autism have separate and independent causes, and which arise from one and the same origin in the brain. When the genes for susceptibility to ASD are identified, the diagnosis may be revolutionized. Then cases that are now considered to fall on the same spectrum may be revealed to belong to completely different etiological subgroups, while previously unidentified cases may be identified within genetic pedigrees. Once genes are isolated, then animal models will become truly useful for identifying the neurophysiological

mechanisms and devising means of repairing and preventing neurological abnormalities. All of this progress, however, requires a real understanding of how autism unfolds through development, which are core elements and which merely secondary and avoidable knockon effects. This long-term aim can only be achieved by integrating bottom-up approaches, such as genome-wide screening, and topdown research such as establishing the neural basis of hypothesised cognitive assets and deficits. Further reading Belmonte, M.K., Allen, G., BeckelMitchener, A., Boulanger, L.M., Carper, R.A., and Webb, S.J. (2004). Autism and abnormal development of brain connectivity. J. Neurosci. 20, 9228–9231 Boddaert, N., Chabane, N., Gervais, H., Good, C.D., Bourgeois, M., Plumet, M.H., Barthelemy, C., Mouren, M.C., Artiges, E., Samson, Y., et al. (2004). Superior temporal sulcus anatomical abnormalities in childhood autism: a voxel-based morphometry MRI study. Neuroimage 23, 364–369. Bock, G., and Goode, J. eds. (2003). Autism – neural basis and treatment possibilities. Novartis Found Symp. 251. Chichester: Wiley. Courchesne, E., and Pierce, K. (2005). Brain overgrowth in autism during a critical time in development: implications for frontal pyramidal neuron and interneuron development and connectivity. Int. J. Dev. Neurosci. 23, 153–170. Frith, U., and Hill, eds. (2003). Autism, mind and brain. Oxford: Oxford University Press. Frith, U. (2003). Autism: Explaining the enigma, 2nd edition. Oxford: Blackwell. Happe, F. (1999). Autism: cognitive deficit or cognitive style? Trends Cogn. Sci. 3, 216–222. Klin, A., Jones, W., Schultz, R., Volkmar, F., and Cohen, D. (2002). Quantifying the social phenotype in autism. Am. J. Psychiatry 159, 895–908. Pelphrey, K.A., Morris, J.P., and McCarthy, G. (2005). Neural basis of eye gaze processing deficits in autism. Brain 128, 1038–1048. Sainsbury, C. (2000). Martian in the playground. Bristol: Lucky Duck Publ. 1UCL

Institute of Cognitive Neuroscience, 17 Queen Square, London WC1N 3AR, UK. 2Social, Genetic, and Developmental Psychiatry Centre, Institute of Psychiatry, De Crespigny Park, London SE5 8AF, UK.

Correspondences

Chemical stimuli induce courtship dominance in Drosophila Nicolas Svetec1, Matthew Cobb2 and Jean-François Ferveur1 Courtship dominance in male Drosophila occurs when a male directs high levels of courtship towards another male, who remains passive [1]. We investigated the cues that shape this effect and report here that it is induced by the perception of adult male cuticular hydrocarbons during a critical period. B42 male Drosophila — F1 males from the cross of a B42 female and a wild-type male — carry a single copy of the CheB42 transgene [2] which causes a loss-of-function mutation [3] affecting sex pheromone discrimination [1]. Five-day old B42 males that had been housed with four mature males in their first day of life dominated males that had been housed with four χ2 = 15.34, immature males (χ p < 0.0001; Figure 1), displaying significantly more intense dominance (t76 = 4.69, p < 0.0001). Similar effects were found for males housed with a single mature or immature fly χ2 = 6.26, p < 0.02), indicating (χ that one fly can induce courtship dominance. The strength of courtship dominance declined if social experience occurred at two days χ2 = 5.54, p < 0.025; old (χ dominance intensity: t24 = 1.06, p = n.s.) and disappeared at three χ2 = 0.17, p = n.s.): at days old (χ this age, males that had encountered young or mature flies were equally likely to be dominant. Social experience during the first eight hours of life did not induce courtship dominance: either the critical period occurs outside this time, or a longer duration of social experience is required.

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Experience with 4 males 82.1 ± 2.4

% of males dominant

Immature male flies lack the adult unsaturated hydrocarbons 7-tricosene (7-T) and 7-pentacosene (7-P), which modulate adult male–male interactions [4,5]. We tested the effect of housing B42 males between 0–24 hours with mature Desat males, which produce virtually no unsaturated hydrocarbons [6]. These B42 males were dominated by B42 males housed with 7-T rich mature B42 or Dijon wild-type males (Figure 2), suggesting that perception of 7-T, found on the cuticle of most mature males, may induce courtship dominance. To test this hypothesis, B42 males were individually housed at age 0–24 hours with a single mature Desat male that had been ‘perfumed’ with the overall cuticular hydrocarbon profile of Dijon males (*Dijon* — mainly 7-T) or sibling males (*Desat* — no qualitative change in hydrocarbon profile). B42 males housed with *Dijon* males displayed significantly higher levels of courtship dominance than flies housed with *Desat* males χ2 = 7.71, p < 0.01), confirming (χ the role of the principal mature male cuticular hydrocarbon in this phenomenon. However, no significant differences in courtship dominance were observed between males housed with a *Dijon* male and those housed with a *Tai* male (a Desat male perfumed by 7-P rich Tai males), nor between males that had been housed with four headless mature B42 males (HL-B42) or four headless Desat males (HL-Desat) (Figure 2). These experiments show that courtship dominance occurs when the dominant male, but not the subordinate fly, has encountered adult male unsaturated hydrocarbons (7-T and/or 7-P) carried by an active male. This experience-dependent change behaviour lasts at least four days after conditioning but is not permanent: at 10 days old, nine days after social experience and having been held isolated subsequently, there was no significant difference in courtship dominance between males housed with Desat or Dijon males

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Figure 1. Courtship dominance is induced by social experience during a critical period. Pairs of 5-day old male B42 flies (n > 25 in all cases) were observed for 10 minutes in a small cell and the proportion of time each individual spent in behaviour directed to the other fly was noted. Most of this behaviour was courtship, but there was also a low proportion (~5%) of aggressive behaviour. Because of the difficulty of defining these behavioural components, they were pooled in a Behavioural Index (BI), a measure of the intensity of courtship dominance [1]. Males were housed with four other males or one other male. An individual was defined as dominant if BI ≥ 10% of the observation time, while the other male displayed no aggressive or courtship behaviour (BI = 0). Over all conditions courtship dominance was observed in 67–89% of pairs. All pairs where the total BI for both flies <5% were excluded (17% of all pairs); in virtually all these cases both flies had BI = 0. In the remaining pairs, both flies displayed some aggression or courtship, and therefore neither showed courtship dominance as defined above. The figure shows the percentage of dominant males in each condition, and the intensity of the behaviour performed by those males (figures above each bar represent mean BI ± standard error).

χ2 = 0.55, p = n.s.). This suggests (χ that this phenomenon is some kind of non-associative or associative learning. No correlation was observed between courtship dominance and the cuticular hydrocarbons carried by dominant or subordinate males (data not shown); this contrasts with social insects, where cuticular hydrocarbons can communicate dominance [7]. During social experience, immature males are courted by mature males, who produce courtship ‘song’ with their wings. Males housed with *Dijon* males that were intact or had clipped wings displayed the same levels and intensity of courtship dominance, indicating that the social stimuli involved in the effect are not transmitted by the wings. Furthermore, we found no correlation between the behaviour of flies during housing and courtship dominance, nor between courtship dominance and ability to compete for a single

virgin female (see Supplemental Data available with this article online). These data suggest that experience-dependent dominance does not have a direct relation to mating success, in contrast to the situation found in mammals [8] and cockroaches [9], and that this phenomenon is not related to Drosophila courtship conditioning, which results in altered sexual behaviour [10]. One possibility we have yet to investigate is the relation of courtship dominance to territoriality. Experience-induced courtship dominance occurs in male Drosophila following early contact with chemicals carried by adult or immature males. Similar chemical effects can be seen in mice [11], and may be involved in experience-dependent dominance in male golden hamsters [12], suggesting that chemical communication modulates dominance in a range of species.

Gender trading in a hermaphrodite 60

Nils Anthes, Annika Putz and Nico K. Michiels

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Figure 2. Exposure to adult cuticular hydrocarbons induces courtship dominance in B42 flies. The figure shows the percentage of B42 males displaying courtship dominance following social interactions with a range of male types (n > 25 in all cases). B42 males were housed at age 0–24 hours with adult males of varying genotypes and conditions. Data for dominance intensity (BIs) are not presented; there were no significant differences between dominant and non-dominant males for this measure. B42 and Dijon, males that predominantly produce 7-tricosene; Tai, males that predominantly produce 7-pentacosene; Desat, males that produce no unsaturated cuticular hydrocarbons. Flies marked ** were Desat flies carrying the cuticular profile typical of the strain marked between the asterisks, following hydrocarbon transfer between live flies. Hydrocarbon transfer took place for 24 hours at three days old (at this age, differential dominance can not be induced). HL, headless. Bars are coded according to the hydrocarbon profile of the conditioner males: black, B42; white, Desat; dark grey, Dijon; light grey, Tai. Supplemental data Supplemental data including mating kinetics and details of behaviour are available at http://www.currentbiology.com/cgi/content/full/15/19/ R790/DC1/ References 1. Svetec, N., and Ferveur, J.-F. (2005). Social experience and pheromonal perception can change male-male interactions in Drosophila melanogaster. J. Exp. Biol. 208, 891–898. 2. Xu, A., Park, S.K., D’Mello, S., Kim, E., Wang, Q. and Pikielny, C.W. (2002). Novel genes expressed in subsets of chemosensory sensilla on the front legs of male Drosophila melanogaster. Cell Tiss. Res. 307, 381-392. 3. Svetec, N., Houot, B. and Ferveur, J-F. (2005). Effect of genes, social experience and their interaction on the courtship behaviour of transgenic Drosophila males. Genet. Res. Camb. 85, 1-11. 4. Pechine, J-M., Antony, C. and Jallon, J-M. (1988). Precise characterization of cuticular compounds in young Drosophila by mass-spectrometry. J. Chem. Ecol 14, 1071-1085. 5. Cobb, M., and Jallon, J.-M. (1990). Pheromones, mate recognition and courtship stimulation in the Drosophila melanogaster species sub-group. Anim. Behav. 39, 1058–1067. 6. Marcillac, F., Grosjean, Y., and Ferveur, J-F. (2005). A single mutation alters production and

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discrimination of Drosophila sex pheromones. Proc. Roy. Soc. Lond. B 272, 303-309. Monnin, T. and Peeters, C. (1999) Dominance hierarchy and reproductive conflicts among subordinates in a monogynous queenless ant. Behav. Ecol. 10, 323-332. Creel, S.F. (2005). Dominance, aggression and glucocorticoid levels in social carnivores. J. Mammal. 86, 255-264. Moore, A.J. and Moore, P.J. (1999). Balancing sexual selection through opposing mate choice and male competition. Proc. Roy Soc. Lond. B 266, 711-716. Siegel, R.W., and Hall, J.C. (1979). Conditioned responses in the courtship behavior of normal and mutant Drosophila. Proc. Natl. Acad. Sci. USA 76, 565–578. Ely, D.L. and Henry, J.P. (1978). Neuroendocrine response patterns in dominant and subordinate mice. Horm. Behav. 10, 156-169. Ferris, C.F., Messenger, T. and Sullivan, R. (2005). Behavioral and neuroendocrine consequences of social subjugation across adolescence and adulthood. Front. Zool. 2, 7. doi:10.1186/1742-99942-7

1UMR-CNRS

5548, Université de Bourgogne, 6 bd Gabriel, Dijon 21000, France. 2Faculty of Life Sciences, The University of Manchester, Manchester M13 9PT, UK. E-mail: : [email protected]

Although males and females may face severe sexual conflicts [1], the decision over who donates and who receives sperm is fixed. This is not necessarily the case in simultaneous hermaphrodites, where each mate may insist on copulating as ‘male,’ ‘female’ or both. The resulting conflicts over gender provide an opportunity to study conflict-solving strategies. By directly manipulating mating interests in the sea slug Chelidonura hirundinina, we present the first unequivocal evidence for ‘sperm trading’ [2], a mating strategy where sperm donation is conditional on sperm receipt. Trading enforces reciprocity, offering a simple solution for the gender conflict. Following its original description in 1984 [2], sperm trading has been suggested to be widespread as many hermaphrodites inseminate reciprocally. But recent studies have shown that reciprocity alone does not prove sperm trading [3,4]. Showing that bidirectional sperm exchange is indeed conditional requires experimental manipulation of sex roles, which is impractical in most species studied thus far [5–7]. Hermaphroditic sea slugs of the Order Cephalaspidea are exceptional in this context: they have an open, external skin fold through which semen flows from the genital aperture to the penis (Figure 1). By interrupting this sperm groove, insemination can be prevented without affecting copulatory behaviour [3]. Such ‘experimental cheaters’ provide a unique tool to test whether nonreciprocating mates are deserted, which is the key prediction in proving sperm trading [3]. In C. hirundinina, a single mating sequence involves up to 10 sequential penis intromissions and inseminations per partner (Figure 1A). Pairs usually start with simultaneous sperm donation, followed by alternating unilateral