Sexual behaviour in Drosophila is irreversibly programmed during a critical period

Abstract

Sexual differentiation in Drosophila is controlled by a short cascade of regulatory genes, the expression pattern of which determines all aspects of maleness and femaleness, including complex behaviours displayed by males and females [1-3]. One sex-determining gene is transformer (tra), the activity of which is needed for female development. Flies with a female karyotype (XX) but which are mutant for tra develop and behave as males. In such flies, a female phenotype can be restored by a transgene that carries the female-specific cDNA of tra under the control of a heat-shock promoter. This transgene, called hs[trafem], also transforms XY animals into sterile females [4]. When we raised these XX and XY 'females' at 25 degreesC, however, they displayed vigorous male courtship while at the same time, as a result of their female pheromone pattern, they were attractive to males. Intriguingly, their male courtship behaviour was indiscriminately directed towards both females and males. When we forced expression of tra by heat shock, applied during a limited period around puparium formation, male behaviour was abolished and replaced by female behaviour. We conclude that sexual behaviour is irreversibly programmed during a critical period as a result of the activity or inactivity of a single control gene.

Sex-determining mechanisms in insects

“…The function of P1 promoter is restricted to ~2% of neurons in the CNS, in various regions of the brain and ventral ganglia, from late third instar larva onward (reviewed in Billeter et al, 2002;. To this respect, it is worth mentioning that sexual behaviour of the Drosophila male is irreversibly programmed during a critical period extending from shortly before puparium formation into early metamorphosis (Arthur et al, 1998). Sexual behaviour, however, is not reviewed here.…”

Genetics and genomics of Drosophila mating behavior

“…These include mutations in genes required for normal morphology [white (13,14), yellow (14), and curved (15)], as well as genes involved in learning and memory [Calcium calmodulin kinase II (16), dunce (17,18), rutabaga (19,20), turnip (19,21), and amnesiac (20,22,23)], circadian rhythm [period (18,(24)(25)(26)] and dopamine and serotonin synthesis [Dopa decarboxylase (27), pale (28,29), tan (30,31), and ebony (32)(33)(34)], sex determination [doublesex (35)(36)(37), transformer (38)(39)(40)(41)(42)(43), fruitless (44)(45)(46)(47), and sex lethal (48)], pheromone production [desaturase 2 (49)], and accessory gland-specific peptides (6-8, 50-52). a subset of loci identified by mutational analysis, or will the analysis of natural variants reveal novel loci?…”

Acis-regulatory Sequence Within theyellowLocus ofDrosophila melanogasterRequired for Normal Male Mating Success

“…The fru gene encodes a predicted BTB/POZ family zinc-finger transcription factor, which has been shown to be a member of the D. melanogaster somatic sex determination hierarchy (Ito et al 1996;Ryner et al 1996;Heinrichs et al 1998). The use of an antibody specific to male-limited FRU proteins (FRU M ) (Lee et al 2000;Lee and Hall 2001) has demonstrated that the spatial and temporal distribution of FRU M proteins in the CNS is consistent with the timing of the critical period for programming a male fate (Belote and Baker 1987;Arthur et al 1998) and the regions of the CNS whose maleness is necessary for normal development of male courtship behaviors (Hall 1979;von Schlicher and Hall 1979). Most recently, it has been shown that sex-specific splicing of fru specifies the male courtship behavior fate (Demir and Dickson 2005;Manoli et al 2005;Stockinger et al 2005).…”