Misexpression of the white (w) gene triggers male-male courtship in Drosophila.

Abstract

We report here that the general ectopic expression of a tryptophan/guanine transmembrane transporter gene, white (w), induces male-male courtship in Drosophila. Activation of a hsp-70/miniwhite (mini-w) transgene in mature males results in a marked change in their sexual behavior such that they begin to vigorously court other mature males. In transformant populations containing equal numbers of both sexes, most males participate, thus forming male-male courtship chains, circles, and lariats. Mutations that ablate the w transgene function also abolish this inducible behavior. Female sexual behavior does not appear to be altered by ectopic w expression. By contrast, when exposed to an active homosexual courtship environment, nontransformant males alter their behavior and actively participate in the male-male chaining. These findings demonstrate that, in Drosophila, both genetic and environmental factors play a role in male sexual behavior.First reported in 1910 by Morgan, the white (w) gene has, over the decades, served as a prototype for numerous studies concerning gene regulation, insertional mutagenesis, and the behavioral analysis of mutants (1-7). Located at the distal end of the X chromosome (8), its 2.6-kb major transcript (9-11) is predicted to encode a 687-amino acid member of the ATPbinding, transmembrane, transporter superfamily (12, 13), which functions in the passage of the ommochrome and drosopterin pigment precursors, tryptophan and guanine (respectively) across membranes (14, 15). w has been conserved during metazoan evolution as evident from the human and Drosophila cognate proteins sharing 34% identity and 58% similarity (J. Croop, personal communication). In Drosophila, w is required for pigment production in the light-screening cells of the compound eye, ocelli pigment cells, sheath cells of the testes, and the larval Malpighian tubules. Communication between courting Drosophila involves an elaborate repertoire of gender-specific action patterns that transmit either acceptance or repelling signals (2, 16). Use of these signaling routines in a particular order and frequency is dependent upon dynamic feedback, with each partner modifying its behavior in response to signals received (17,18). In Drosophila melanogaster, courtship .between mature males is suppressed by their antiaphrodisiac pheromones and experience-dependent courtship modification (learned from the courting of immature males) as well as through the rejection signals males elicit in response to sexual advances (17,(19)(20)(21). Behavioral analysis of Drosophila mutants has revealed that genetic lesions that knock out single genes frequently have pleiotropic effects that impinge upon normal courtship behavior (reviewed in ref. 22). While the loss of white function does not alter the sexual preference of homozygous viable w-flies, absence of the light-screening pigments in its compound eyes impairs the male's ability to visually track a potential mate, thus reducing his "lights on" mating success when compared toThe publicatio...

Interaction Between Eye Pigment Genes and Tau-Induced Neurodegeneration inDrosophila melanogaster

“…Mutations in ABCG1 are associated with mood and panic disorders (Nakamura et al 1999), and mutations in white and brown have a range of neurobehavioral effects in flies, including reduced sensitivity to anesthesia, learning defects, and abnormal courtship behavior (Zhang and Odenwald 1995;Campbell and Nash 2001;Diegelmann et al 2006). Our data fit a model in which an enzymatic product of XDH is transported by White and Brown into granules and in which interaction of this product with tau is detrimental to the cell.…”

Genetic dissociation of acquisition and memory strength in the heat-box spatial learning paradigm in Drosophila

“…Finding that the scarlet mutation limits memory levels with 4 and 20 min of training restricts the candidates for this signal and centers on serotonin. A similar function for white has been suggested in overexpression and anesthesia studies (Zhang and Odenwald 1995;Hing and Carlson 1996;Nilsson et al 2000;Campbell and Nash 2001). A better understanding of the neural structures in which these genes function will prove useful in determining the processes in which white and scarlet function in memory formation.…”

Phototactic personality in fruit flies and its suppression by serotonin and white

“…4F). Indeed, white mutants have diminished concentrations of the neurotransmitters serotonin, dopamine, and histamine (13,14) and concomitant behavioral phenotypes affecting courtship (15), spatial learning (16), and olfactory learning (17). To further investigate the role of white, we assayed the mutants brown, scarlet, and cinnabar (which encodes an enzyme in the xanthommatin synthesis pathway downstream of Scarlet but not in the serotonin synthesis pathway).…”