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Behavioural genetics: Sex in fruitflies is
fruitless
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Author: C. P. Kyriacou
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"NEWS & VIEWS NATURE|Vol 436|21 July 2005 334 If decreasing atmospheric CO 2 stabilized the glacial state in the Oligocene, might increasing atmospheric CO 2 from fossil-fuel burning destabilize it in the future? The lesson to be learned here is that we should watch for subtle signs that we are moving from the icehouse world in which Earth has remained for 34 million years into a new, greenhouse world. a73 Lee R. Kump is in the Department of Geosciences, Pennsylvania State University, 535 Deike Building, University Park, Pennsylvania 16802, USA. e-mail: lkump@psu.edu Tra-binding sequences.) Similarly, Tra protein binds to the doublesex (dsx) gene and splices it in male- and female-specific modes (Dsx M and Dsx F , respectively) 8 . The Dsx M and Dsx F tran- scription factors mainly determine sexual morphologies 8 , but the sexual identity of the nervous system is shaped by fru. By forcing males to express the female- specific fruF transcript, Demir and Dickson 1 produced males that showed the characteris- tics of the worst-affected fru mutants. These males were sterile, they barely courted females and they were more interested in courting males, forming courtship chains. By contrast, females jammed into fruM mode mated poorly, produced very few eggs, but ? aston- ishingly ? courted other females (Fig. 2), even to the point of forming chains. And an identity crisis of similar epic proportions was observed in females that were ?masculinized? using a different fru-related genetic trick 3 . Finally, by feminizing specific abdominal glands in males to produce female pheromones, and placing the altered males with fruM females, the sex roles were reversed, so that the females courted the males 1 . In another nifty piece of genetic engineer- ing, both teams 2,3 generated flies in which they could, among other things, mark the parts of the nervous system (just 2%) that show sex- specific expression of Fru. Further genetic manipulations showed that high levels of male?male courtshipresult when the commu- nication between these neurons is shut down, or when fruM expression in these neurons in males is inhibited 2,3 . Both studies found that the central nervous system of males and females looked very similar in terms of sex- specific fru expression, with few differences between the sexes in the numbers, positions or wiring of cells expressing Fru. The fru products were found in almost all sensory organs that have been implicated in courtship 2,3 . Olfactory sensory neurons showed some evidence for sexual dimor- phisms. Those receptors that respond to pheromones project to certain other brain regions that are larger in males than females, reflecting the fact that sex pheromones have a greater functional significance in male Drosophila 2 . By reversibly shutting down the fru-expressing olfactory receptors, both in males and in masculinized females in the mutants can form bizarre courtship chains, where several males, each chasing and court- ing the one in front, generate frenzied revolv- ing circles. The gene mutated in the fruitless flies (termed fru) was molecularly cloned in 1996, and the putative protein that it encodes was identified as a transcription factor 6,7 , a regula- tory molecule that controls gene expression. A large number of different messenger RNAs can be generated from the fru gene, some of which are sex-specific. In particular, an mRNA produced only in males is translated into a protein called Fru M (for male-specific Fruitless) 6,7 . This sex-specific production of the fru mRNAs is determined by the canoni- cal sex-determination system, the most rele- vant component of which is the transformer gene (or tra). Briefly, the encoded Tra protein binds to very short sequences (13 nucleotides) on the immature fru mRNA, to sex-specifically regulate which portions will be ?spliced? into the final transcript 6,7 . (Indeed, Ryner et al. 6 cloned fru by looking for genes that contained BEHAVIOURAL GENETICS Sex in fruitflies is fruitless Charalambos P. Kyriacou The courtship rituals of fruitflies are disrupted by mutations in the fruitless gene. A close look at the gene?s products ? some of which are sex-specific ? hints at the neural basis of the flies? behaviour. Richard Feynman is reported to have said, ?Science is a lot like sex. Sometimes something useful comes of it, but that?s not the reason we?re doing it.? In three papers, two published in Cell 1,2 , and one in this issue 3 (page 395), science and sex have come together to provide us with something useful ? an extraordinary glimpse into how the male and female nervous systems function to generate sexual behaviour in fruitflies (Drosophila). Unlike many British males on a Friday night, Drosophila males do not simply jump on the first female they see. Courtship behaviour in D. melanogaster is a stereotyped and instinctive sequence of behaviours performed by the male, involving visual, olfactory, gusta- tory, tactile, acoustic and mechanosensory stimuli being exchanged between the sexes (Fig. 1). The female?s role is considerably less dramatic than the male?s: she simply runs away, gives the odd kick, then mates (or not) 4 . Normal mature males seldom court other males, but male fruitless mutants are bisexual, courting not only females but also other males 5 . In exclusive male company, these Figure 1 | The courtship sequence of D. melanogaster males. From left to right, the male orients towards the female, extends a wing and vibrates it, serenading the female with a species-specific love-song. He then licks the female?s genitalia, attempts to copulate, and (maybe) copulates. (Drawings by B. Burnet.) 1. Wise, S. W., Breza, J. R., Harwood, D. M. & Wei, W. in Controversies in Modern Geology (eds Mueller, D., McKenzie, J. & Weissert, H.) 133?177 (Academic, San Diego, 1991). 2. Kennett, J. & Shackleton, N. J. Nature 260, 513?515 (1976). 3. Zachos, J. C., Quinn, T. M. & Salamy, K. A. Paleoceanography 11, 251?266 (1996). 4. Tripati, A., Backman, J., Elderfield, H. & Ferretti, P. Nature 436, 341?346 (2005). 5. Coxall, H. K. et al. Nature 433, 53?57 (2005). 6. Driscoll, N. W. & Haug, G. H. Science 282, 436?438 (1998). 7. Delaney, M. L. & Boyle, E. A. Paleoceanography 3, 137?156 (1988). 8. DeConto, R. M. & Pollard, D. Nature 421, 245?249 (2003). 9. Zachos, J. C. & Kump, L. R. Glob. Planet. Change 47, 51?66 (2005). 10. Kump, L. R., Kasting, J. F. & Crane, R. G. The Earth System 2nd edn (Prentice-Hall, Upper Saddle River, NJ, 2004). 21.7 n&v 333 MH 15/7/05 4:20 PM Page 334 Nature Publishing Group� 2005 � 2005 Nature Publishing Group NATURE|Vol 436|21 July 2005 NEWS & VIEWS 335 sex-reversal paradigm outlined above, court- ship behaviour declined significantly, implying that these receptors are central to sexual inter- actions 2 . However, by decreasing Fru M in males just in these neurons, homosexual courtship increased, so normally these olfactory recep- tors must inhibit male?male interactions 3 . So, a single fru-encoded genetic switch seems to be sufficient to shift the functioning of the nervous system from male to female mode, irrespective of the morphological sex of the animal. The general absence of large-scale sexual dimorphisms in fru-expressing neu- rons implies that it is the molecules regulated by fru that make the difference. Future work will undoubtedly be aimed at finding these molecules, as well as identifying the subset of key neurons that are sufficient to gener- ate male courtship elements. Indeed, Villela et al. 9 have identified neurons downstream of ones expressing fru that are implicated in the control of the male?s courtship song. Finally, an intriguing and mostly forgotten paper was published 30 years ago 10 about ?lesbian? Drosophila females that courted other females ? apparently because of a genetic factor(s) on chromosome 2 (fru is on chromosome 3). Might this long-lost strain have carried a mutation in one of the fru target genes? The work discussed here may well find itself the focus of attention for those interested in the debate (scientific and political) on the genetic versus environmental bases of human sexual- ity. Perhaps we should remind ourselves that normal fly sexual preferences, unlike human sexual behaviour, cannot be modulated to any significant extent by altering experience 11 . a73 Charalambos P. Kyriacou is in the Department of Genetics, University of Leicester, Leicester LE1 7RH, UK. e-mail: cpk@leicester.ac.uk 1. Demir, E. & Dickson, B. J. Cell 125, 785?794 (2005). 2. Stockinger, P., Kvitsiani, D., Rotkopf, S., Tiri�n, L. & Dickson, B. J. Cell 125, 795?807 (2005). 3. Manoli, D. S. et al. Nature 436, 395?400 (2005). 4. Greenspan, R. J. & Ferveur, J. -F. Annu. Rev. Genet. 34, 205?232 (2000). 5. Villela, A. et al. Genetics 147, 1107?1130 (1997). 6. Ryner, L. C. et al. Cell 87, 1079?1089 (1996). 7. Ito, H. et al. Proc. Natl Acad. Sci. USA 93, 9687?9692 (1996). 8. Cline, T. W. & Meyer, B. J. Annu. Rev. Genet. 30, 637?702 (1996). 9. Villela, A., Ferri, S. L., Krystal, J. D. & Hall, J. C. Proc. Natl Acad. Sci. USA (in the press). 10. Cook, R. Nature 254, 241?242 (1975). 11. Siegel, R. W., Hall, J. C., Gailey, D. A. & Kyriacou, C. P. Behav. Genet. 14, 383?410 (1984). greatest calamity to befall Earth?s biosphere since the Permian era ? an impact 65 million years ago in present-day Mexico that is postu- lated, among other things, to have wiped out the dinosaurs. That got people?s attention. But the geological subtleties of asteroids remained largely unappreciated for a further ten years. This situation began to change with the first detailed ground-based radar observations 3 , and the Galileo mission?s fly-by of the asteroids Ida and Gaspra 4 . Now, a new generation of sci- entists is appreciating asteroids as geological entities 2,5,6 . If Thomas and Robinson?s hypothesis of seismic shaking 1 is correct, then the cratering history of any asteroid is complex. Impacts of small meteoroids make the surface heavily cratered, giving it an ?old? look, whereas impacts of larger meteoroids ? by causing the surface to vibrate ? erase smaller craters, making the asteroid appear ?young?. This aster- oidal Botox calls into question the habit of dating asteroid surfaces through their crater- ing record: although the passage of time is indeed recorded here, so too is internal struc- ture. A young asteroid of the type that resem- bles a rubble pile, for instance, is more capable of damping vibrations, and might retain more craters ? and so appear older ? than an ancient, ?competent? asteroid that has a more monolithic interior and thus transmits seismic energy more effectively. But Thomas and Robinson?s work also opens up a new way of looking at asteroids generally. It shows how we might gauge interior structure from surface observations: craters and other landforms, and their degradation, could be used as proxies for seismic data. The idea of seismic processes resurfacing asteroids is not itself new. The formation of the large crater Stickney on Phobos (Fig. 1, over- leaf), a martian moon about the size of Eros and perhaps a captured asteroid, was mod- elled 7 12 years ago using a computational tool called a hydrocode to simulate the effect of the high-velocity impact. The simulation showed that seismic resurfacing could erase craters smaller than about 100 metres in diameter, and significantly degrade larger craters. The same method was later used to show 8 that the jolting of the asteroid Gaspra by large impacts could lead to the unusual distribution of its crater sizes. In an argument analogous to that used by Thomas and Robinson for Eros, the asteroid Ida was suggested 9 to have a relatively monolithic deep interior, given evidence that stress energy was transmitted from a large impact structure at one end to Figure 2 | Courtship remodelled. A fruM female extends a wing as if ?singing? towards a normal female (reproduced with permission from ref. 1). ASTEROIDS Shaken on impact Erik Asphaug A single recent impact may have modified the craters on the asteroid Eros into the pattern we see today. This finding has implications for how we view the structure of asteroids ? and for addressing any hazards they present. Asteroids seem to get stranger with every pass- ing year. Thomas and Robinson?s finding (page 366 of this issue) 1 ? that impact-induced vibrations of an asteroid may be the dominant mechanism reshaping its surface ? shakes things up still further. In the case of the well- studied asteroid Eros, the authors link this resurfacing mechanism to the recent impact of a meteoroid that left a particularly large crater. They thereby make the first detailed mechan- ical connection between surface observations and an asteroid?s global geology. The authors conclude that Eros, a rocky asteroid 33 by 13 by 13 kilometres in size, has a relatively homo- geneous interior that transmits seismic shocks efficiently and is mantled by a hundred metres or more of regolith. (Regolith is the loose soil- like material familiar from pictures of the sur- face of the Moon.) This might not come as a surprise, given Eros?s appearance 2 , but for the first time, the authors provide convincing evidence that makes this conclusion more than just reasonable conjecture. Thomas and Robinson?s discovery marks another stage in the journey asteroids have taken from insignificance, through notoriety, into the mainstream of scientific interest. The turning point came in the 1980s, when an asteroid was found to be responsible for the 21.7 n&v 333 MH 15/7/05 4:20 PM Page 335 Nature Publishing Group� 2005 � 2005 Nature Publishing Group "
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