Genomic basis of honest sexual signalling

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Females often show strong sexual preferences to mate with males that exhibit elaborate and exaggerated sexual ornaments. These traits are thought to act as honest signals of male genetic quality, where only high condition males with 'good genes' can afford to invest in elaborate ornaments. However, the genes that give rise to honest sexual signals and enable their evolution are largely unknown. As such, contentious questions central to sexual selection and evolution remain unanswered, such as the role of sexual selection in phenotypic elaboration, molecular evolution and adaptation. Answering these questions is challenging as we require a precise understanding of the genes responsible for honest signals across a range of organisms. However, new technology that deconstructs complex phenotypes to provide single-cell expression data now offers unprecedented potential to probe the genomic basis and evolution of sexual traits, heralding a new era of sexual selection research. The stalk-eyed fly, key to early insights about sexual selection, has several vital characteristics that give the clade exceptional potential to probe the genomics and evolution of honest signalling. Males have highly-exaggerated eye-stalks compared to females. Eye span is an honest indicator of male condition and females prefer to mate with males with longer eye spans. In particular, some stalk-eyed flies harbour a selfish genetic element on the X chromosome that kills Y-bearing sperm. Males from the driver population have lower genetic quality relative to the standard population as half of their sperm are destroyed. Consistent with sexual selection theory, these males exhibit a smaller eye span and are less attractive to females. We will apply state-of-the-art sequencing approaches (scRNA-seq) to this classic model of sexual selection to probe the genomic basis of male genetic quality and honest sexual signalling. Specifically, we will establish how and when spermatogenesis is disrupted in response to the meiotic driver, identify the genes associated with reduced fertility, and test whether these genes are disproportionally located on the sex chromosomes. Our overarching goal is to identify the genomic targets of sexual selection and elucidate the very nature of 'good genes'.