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 new function
by one copy (neofunctionalization). 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. 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 venoms 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 of new gene functions, particularly under conditions of rapid
evolutionary change.