Ankyrin domain encoding genes resulting from an ancient horizontal transfer are functionally integrated into developmental gene regulatory networks in the wasp Nasonia

Background: How and why regulatory networks incorporate additional components, and how novel genes are maintained and functionally integrated into developmental processes are two important and intertwined questions whose answers have major implications for the evolution of development. We recently described a set of novel genes with robust and unique expression patterns along the dorsal-ventral axis of the embryo of the wasp Nasonia. Given the unique evolutionary history of these genes, and their apparent integration in to the dorsal-ventral (DV) patterning network, they are collectively an excellent model to study the evolution of regulatory networks, and the fates of novel genes. Results: We have found that the novel DV genes are part of a large family of rapidly duplicating and diverging ankyrin domain encoding genes that originated most likely by horizontal transfer from Wolbachia in a common ancestor of the wasp superfamilly Chalcidoidea. We tested the function of those ankyrin encoding genes expressed along the DV axis and found that they participate in early embryonic DV patterning. We also developed a new wasp model system (Melittobia) and found that some functional integration of ankyrin genes have been preserved for over 90 million years, while others are lineage specific. Conclusions: Our results indicate that regulatory networks can incorporate novel genes that then become necessary for stable and repeatable outputs. Even modest role in developmental networks may be enough to allow novel or duplicate genes to be maintained in the genome and become fully integrated network components.