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

Abstract

Summary 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 down-regulation 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.

A digestive tract expressing α‐amylase influences the adult lifespan of Pteromalus puparum revealed through RNAi and rescue analyses

“…The gene is highly expressed by its female venom gland. This expression specialization has also been shown in other chalcid venoms, like in Nasonia species . Our results show there is probably evolutionary gene duplication happening between PpAmy2 and PpAmy3 , and PpAmy3 may be recruited from PpAmy2 , the muscle rich one, into P. puparum venom.…”

Evaluating the evolution and function of the dynamic Venom Y protein in ectoparasitoid wasps

“…Within the phylogeny of VenY , both paralogues have relatively short branches that mirror the species tree, which places the base of each gene clade at ~15 Mya (Martinson et al ., ; Fig. ).…”

“…The importance of VenY was first noted after it was identified as the most highly expressed gene in the venom gland of N. vitripennis (Sim and Wheeler, ; Martinson et al ., ). Further searches in the closely related Nasonia giraulti genome revealed a homologue of VenY as well as a paralogue not present in N. vitripennis .…”

“…It is still unknown which venom proteins are affecting specific pathways in the host and how these proteins evolved. Many parasitoid wasp venom proteins have little to no sequence homology to known proteins or are similar to proteins with no functional annotations, therefore providing a challenge to characterize the function of venom proteins (de Graaf et al ., ; Martinson et al ., ). Additionally, these organisms produce a very small volume of total venom, making it challenging to isolate and test individual components of venom for biological effects.…”

“…Nasonia vitripennis produces ~100 venom proteins including ~45% that have no recognizable homology to proteins with annotated functions (Danneels et al ., ; Sim and Wheeler, ; Martinson et al ., ). The most highly expressed gene in the venom gland is an uncharacterized protein named venom protein Y (hereafter VenY) (Sim and Wheeler, ; Martinson et al ., ). In this study, we characterize VenY by reconstructing its evolutionary history, defining its protein sequence and identifying possible functions in the host using RNA interference (RNAi).…”