果蝇（Drosophila）求偶是所有动物中被研究得最彻底的行为之一，关于该行为的任何新东西都有可能在生物学的其他领域找到相应的东西。一只雄性在遇到一只雌性时，在交配前要在几分钟内完成一系列固定动作。不急于交配可让雌性来测试雄性的身体状况如何。在通过RNA干涉所进行的另一个引人注目的基因剔除应用中，研究人员发现，在大脑中一组约60个神经元中将无效基因（Fruitless gene）的雄性特定产物剔除，会对求偶行为产生特定影响。果蝇花在求偶上的时间大大减少，一些求偶动作被完全省略。缺少关键神经元的果蝇所表现出的简短求偶行为与其他昆虫的正常行为相似，说明物种差别可能反映了很多昆虫物种中一个神经线路中所发生的变化。
Median bundle neurons coordinate behaviours during Drosophila male courtship
Throughout the animal kingdom the innate nature of basic behaviour routines suggests that the underlying neuronal substrates necessary for their execution are genetically determined and developmentally programmed. Complex innate behaviours require proper timing and ordering of individual component behaviours. In Drosophila melanogaster, analyses of combinations of mutations of the fruitless (fru) gene have shown that male-specific isoforms (FruM) of the Fru transcription factor are necessary for proper execution of all steps of the innate courtship ritual. Here, we eliminate FruM expression in one group of about 60 neurons in the Drosophila central nervous system and observe severely contracted courtship behaviour, including rapid courtship initiation, absence of orienting and tapping, and the simultaneous occurrence of wing vibration, licking and attempted copulation. Our results identify a small group of median bundle neurons, that in wild-type Drosophila appropriately trigger the sequential execution of the component behaviours that constitute the Drosophila courtship ritual.
Figure 1 The Drosophila courtship ritual and its regulation by the fru branch of the Drosophila sex-determination hierarchy. a, Visual and olfactory cues used to detect and identify an appropriate female elicit orienting behaviour as the male faces and follows the female at a constant distance3–5. The male then orients to the female's lateral aspect and 'taps' her abdomen, perhaps facilitating the proper recognition of females and progression through the courtship ritual. The male then extends his outer wing and vibrates it to generate a species-specific courtship song, reorients towards the female's posterior, and extends his proboscis to 'lick' her genital region. Following successful licking, the male will then curl his abdomen and attempt copulation. Copulation typically lasts for about 20 min and results in the transfer of sperm and seminal fluids. b, The regulation of male courtship through FruM by the Drosophila sex-determination hierarchy. In males, the lack of Sxl and thus Tra activity leads to the default splicing of fru P1-derived transcripts, yielding FruM.
Figure 2 P52a-GAL4 expression in FruM neurons of the median bundle. P52a-GAL4 directs inhibition of FruM expression by a UAS-fruMIR transgene. a, P52a-GAL4 expression in the Drosophila brain is shown by expression of UAS-driven cytoplasmic -Gal. Arrows indicate cell bodies of median bundle neurons in the suboesophageal ganglion (white), their projections dorsally in the median bundle (red) and their ramification in the dorsal protocerebrum (yellow). b, P52a-GAL4 directs GFPnls (green) expression in FruM-expressing (magenta; overlap in white) suboesophageal ganglion cells. View of the anterior surface. c, P52a-GAL4-directed expression of a UAS-fruMIR transgene successfully inhibits FruM expression in suboesophageal ganglion neurons. Arrows indicate the region of the suboesophageal ganglion where FruM expression is absent (compare with b)
Figure 3 Inhibition of FruM expression in median bundle neurons leads to aberrant courtship behaviour. a, Average courtship latencies for control and P52a-manipulated males in which FruM expression has been reduced using directed expression of a UAS-tra.F (female) or UAS-fruMIR transgene (n = 15 for Canton S, P52a/ + , UAS-fruMIR / + , UAS-GFP and P52a/tra.F, and 20 for P52a/GFP and P52a/fruMIR). P52a-manipulated males show decreases, relative to control males, in courtship latency when presented with virgin females. An asterisk indicates P < 0.01 for values compared with P52a/GFP controls. Error bars indicate s.e.m. values. b, P52a/fruMIR (purple) and control (green) males show no differences in intermediate (top panel, P = 0.79) or long-term (bottom panel, P = 0.65) locomotor activity. c, d, Although sterile, P52a/fruMIR males (d), compared with control P52a/LacZ (c), show no defects in either the innervation of internal genitalia (mAb 22C10 staining, magenta), or the serotonergic differentiation of abdominal ganglion neurons that innervate portions of the internal genitalia (anti-5HT staining, green). ED, ejaculatory duct; SV, seminal vesicle; AC, accessory gland.
Figure 4 A functional schematic of putative median bundle roles during the Drosophila courtship ritual. a, Aberrant courtship behaviour in P52a/fruMIR males. In the absence of FruM-mediated median bundle function, elicitation of rapid-onset courtship by single females (green) or females in the presence of other males (purple, see c) bypasses initial steps (orientation and tapping) and rapidly progresses to attempted copulation. b, In the wild type, proper median bundle function is required for the staging of sequential courtship components and for proper transfer of seminal contents. Tonic inhibitions (red) of later behaviours are dependent upon FruM-expressing median bundle neurons. Disinhibtions of behaviours (green) are elicited in response to specific sensory cues. Recognition of females initiates orienting, tracking and tapping behaviours by means of positively-acting sensory information. Additional cues may relieve the median-bundle-mediated inhibition of rapid courtship initiation and permit progression to tapping. Similar disinhibtion following successful tapping allows wing song and licking, and successful licking disinhibits attempted copulation. Median bundle function is additionally needed for successful insemination (dashed red line). c, In wild-type situations involving multiple males, median bundle neurons function in the inhibition of courtship initiation by a second male when a female is already being courted (dashed purple line).
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