<i>Trans</i> regulation of an odorant binding protein by a proto-Y chromosome affects male courtship in house fly.

Abstract

The male-limited inheritance of Y chromosomes favors alleles that increase male fitness, often at the expense of female fitness. Determining the mechanisms underlying these sexually antagonistic effects is challenging because it can require studying Y-linked alleles while they still segregate as polymorphisms. We used a Y chromosome polymorphism in the house fly, <i>Musca domestica</i>, to address this challenge. Two male determining Y chromosomes (Y^M and III^M) segregate as stable polymorphisms in natural populations, and they differentially affect multiple traits, including male courtship performance. We identified differentially expressed genes encoding odorant binding proteins (in the <i>Obp56h</i> family) as candidate agents for the courtship differences. Through network analysis and allele-specific expression measurements, we identified multiple genes on the house fly III^M chromosome that could serve as <i>trans</i> regulators of <i>Obp56h</i> gene expression. One of those genes is homologous to <i>Drosophila melanogaster CG2120</i>, which encodes a transcription factor that binds near <i>Obp56h</i>. Upregulation of <i>CG2120</i> in <i>D. melanogaster</i> nervous tissues reduces copulation latency, consistent with this transcription factor acting as a negative regulator of <i>Obp56h</i> expression. The transcription factor gene, which we name <i>speed date</i>, demonstrates a molecular mechanism by which a Y-linked gene can evolve male-beneficial effects.