Behavioral and neurobiological implications of sex-determining factors in Drosophila

The function of the central nervous system as it controls sex-specific behaviors in Drosophila has been studied with renewed intensity, in the context of genetic factors that influence the development of sexually differentiated aspects of this insect. Three categories of genetic variations that cause anomalies in courtship and mating behaviors are discussed: (1) mutants isolated with regard to courtship defects, of which putatively courtship-specific variants such as the fruitless mutant are a subset; (2) general behavioral and neurological variants (including sensory and learning mutants), whose defects include subnormal reproductive performance; and (3) mutations of genes within the sex-determination regulatory hierarchy of Drosophila, the analysis of which has included studies of reproductive behavior. Recent studies of mutations in two of these categories have provided new insights into the control of neuronally based aspects of sex-specific behavior. The doublesex gene, the final factor acting in the sex-determination hierarchy, had been previously thought to regulate all aspects of sexual differentiation. Yet, it has been recently shown that doublesex does not control at least one neuronally-determined feature of sex-specific anatomy—a muscle in the male's abdomen, whose normal development is, however, dependent on the action of fruitless. These considerations prompted us to examine further (and in some cases re-examine) the influences exerted by sex-determination hierarchy genes on behavior. Our results—notably those obtained from assessments of doublesex mutations' effects on general reproductive actions and on a particular component of the courtship sequence (male “singing” behavior)—lead to the suggestion that there is a previously unrecognized branch within the sexdetermination hierarchy, which controls the differentiation of the male- and female- specific phenotypes of Drosophila. This new branch separates from the doublesex-related one immediately before the action of that gene (just after fransformer and transformer-2) and appears to control as least some aspects of neuronally determined sexual differentiation of males. © 1994 Wiley-Liss, Inc.     

Dynamics of mating success in experimental groups ofDrosophila melanogaster (Diptera: Drosophilidae)

Determinants of male courtship success in Drosophila melanogasterwere examined in groups of five males sequentially presented with five individual females. Thirty-three percent of males never mated, while approximately half of the males mated two or three times. Rapid courtship initiation was associated with male success in early matings only. Male size was important for courtship outcome, but the size distributions of mating and nonmating males and their progeny numbers indicate balancing rather than directional selection on size- dependent courtship success.     

Different sexual traits show covariation among genotypes: implications for sexual selection

An unresolved question in sexual selection research is whetherdifferent secondary sexual traits are developmentally independentor instead whether their degree of expression is a manifestationof a general resource pool (i.e., condition) within the organism.If degree of expression of different sexual traits reflectsability to accumulate condition, then covariation should existacross genotypes in the expression of these traits, even ifthey are very different in kind. Here we present evidence forpredicted covariation between morphological (sex comb size)and behavioral (courtship song) sexual traits among geneticlines of Drosophila bipectinata Duda extracted from a naturalpopulation. There is evidence that both these traits in Drosophilaare condition dependent and subject to sexual selection. Wedetected significant body size–independent differencesin comb size among 32 lines. Replicate lines exhibiting relativelyhigh and low values of comb size were then subjected to analysesof courtship song. High sex comb lines exhibited shorter meanburst period and shorter mean burst duration than low sex comblines. These song differences occurred only during the distantpursuit phase of male courtship and existed despite factoringout individual variations in sex comb size, the trait on thebasis of which test lines were originally chosen. The resultsverify the prediction of an association between condition-dependentsecondary sexual traits across genotypes and, therefore, supportthe existence of an overall genetic quality related to conditionacquisition.     

Sexual experience does not compensate for the disruptive effects of zinc sulfate--lesioning of the main olfactory epithelium on sexual behavior in male mice

Recent studies point to an important role for the main olfactory epithelium (MOE) in regulating sexual behavior in male mice. We asked whether sexual experience could compensate for the disruptive effects of lesioning the MOE on sexual behavior in male mice. Male mice, which were either sexually naive or experienced, received an intranasal irrigation of either a zinc sulfate solution to destroy the MOE or saline. Sexual behavior in mating tests with an estrous female was completely abolished in zinc sulfate-treated male mice regardless of whether subjects were sexually experienced or not before the treatment. Furthermore, zinc sulfate treatment clearly disrupted olfactory investigation of both volatile and nonvolatile odors. Destruction of the MOE by zinc sulfate treatment was confirmed by a significant reduction in the expression of Fos protein in the main olfactory bulb following exposure to estrous female urine. By contrast, vomeronasal function did not seem to be affected by zinc sulfate treatment: nasal application of estrous female urine induced similar levels of Fos protein in the mitral and granule cells of the accessory olfactory bulb (AOB) of zinc sulfate- and saline-treated males. Likewise, the expression of soybean agglutinin, which stains the axons of vomeronasal organ neurons projecting to the glomerular layer of the AOB, was similar in zinc sulfate- and saline-treated male mice. These results show that the main olfactory system is essential for the expression of sexual behavior in male mice and that sexual experience does not overcome the disruptive effects of MOE lesioning on this behavior.     

Brief Exposure to Female Odors “Emboldens” Male Mice by Reducing Predator-Induced Behavioral and Hormonal Responses

In rodents, where chemical signals play a particularly important role in determining intersexual interactions, various studies have shown that male behavior and physiology is sensitive to female odor cues. Here we examined the effects of brief (1 min) and more prolonged (60 min) preexposure to the odors of a novel estrous female on the behavioral and hormonal responses of sexually experienced and inexperienced male mice, Mus musculus, to subsequent predator (cat and weasel) odor exposure and potential predator risk. Brief, but not prolonged, preexposure to the odors of an estrous female decreased the aversion and avoidance responses of male mice to cat odor in a Y-maze preference test, with the extent of responses being affected by a males prior sexual experience. Similarly, brief, but not prolonged, preexposure to female odors markedly attenuated the analgesic responses elicited in male mice by weasel odor. Brief exposure to a novel estrous female by itself had no significant immediate effects on either corticosterone or testosterone levels in the males. However, brief, but not prolonged, preexposure to the odors of an estrous female attenuated the marked increase in corticosterone and decrease in testosterone that were induced in males by exposure to weasel odor. The decreases in aversive responses to, and effects of, predator odor exposure that are induced by brief exposure to a novel estrous female may reflect a greater risk taking and boldness in males that could directly facilitate access to an immediately, and possibly transiently, available novel sexually receptive female.     

A sex-specific switch between visual and olfactory inputs underlies adaptive sex differences in behavior

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Contrasting sexual selection on males and females in a role-reversed swarming dance fly, Rhamphomyia longicauda Loew (Diptera: Empididae)

Although there are several hypotheses for sex-specific ornamentation, few studies have measured selection in both sexes. We compare sexual selection in male and female dance flies, Rhamphomyia longicauda (Diptera: Empididae). Swarming females display size-enhancing abdominal sacs, enlarged wings and decorated tibiae, and compete for nuptial gifts provided by males. Males preferentially approach large females, but the nature of selection and whether it is sex-specific are unknown. We found contrasting sexual selection for mating success on structures shared by males and females. In females, long wings and short tibiae were favoured, whereas males with short wings and long tibiae had a mating advantage. There was no assortative mating. Females occupying potentially advantageous swarm positions were large and, in contrast to selection for mating success, tended to have larger tibiae than those of rivals. We discuss our findings in the context of both the mating biology of dance flies, and the evolution of sexual dimorphism in general.