The Evolution of Venom by Co-option of Single-Copy Genes

The classic model for the evolution of novel gene function is through gene duplication followed by evolution of a new function by one of the copies (neofunctionalization) [1, 2]. However, other modes have also been found, such as novel genes arising from non-coding DNA, chimeric fusions, and lateral gene transfers from other organisms [3-7]. Here we use the rapid turnover of venom genes in parasitoid wasps to study how new gene functions evolve. In contrast to the classic gene duplication model, we find that a common mode of acquisition of new venom genes in parasitoid wasps is co-option of single-copy genes from non-venom progenitors. Transcriptome and proteome sequencing reveal that recruitment and loss of venom genes occur primarily by rapid cis-regulatory expression evolution in the venom gland. Loss of venom genes is primarily due to downregulation of expression in the gland rather than gene death through coding sequence degradation. While the majority of venom genes have specialized expression in the venom gland, recent losses of venom function occur primarily among genes that show broader expression in development, suggesting that they can more readily switch functional roles. We propose that co-option of single-copy genes may be a common but relatively understudied mechanism of evolution for new gene functions, particularly under conditions of rapid evolutionary change.