Exploring population history and gall induction in cynipid gall wasps using genomics and transcriptomics
Cynipid gall wasps have fascinating biology that has piqued the interest of naturalists throughout history. They induce morphologically complex, sometimes spectacular, gall structures on plants in which the larval stages develop. Gall wasps have therefore evolved an intimate association with their hosts - both metabolically, and in terms of their population histories. Gall wasps must both interact physiologically with their hosts to induce galls, and track their host plants through space and time. My thesis centres on two uses of genomic data in understanding the biology of the oak apple gall wasp Biorhiza pallida. I provide a comprehensive investigation into patterns of oak and gall wasp gene expression associated with gall induction, and a population genomic reconstruction of the population history of this species across the Western Palaearctic. While advances in sequencing technology and reduced costs have made these aims possible, analysis of the massive resulting datasets generated creates new challenges. Firstly, in reconstructing the population history of B. pallida, I describe the use of shotgun sequencing and an informatic pipeline to generate alignments of several thousand loci for three B. pallida individuals sampled from putative glacial refugia across the Western Palaearctic in Iberia, the Balkans and Iran. This dataset was analysed using a new maximum likelihood method capable of estimating population splitting and admixture among refugia across very large numbers of loci. The results showed an ancient divide between Iberia and the other two refugia, followed by very recent admixture between easternmost and westernmost regions. This suggests that gall wasps have migrated westwards along the North African coast as well as through mainland Europe. Second, I compare the gene expression profiles of gall wasp and oak tissues sampled from each of three stages of gall development, leading to new insights into potential mechanisms of gall wasp-oak interaction. A highly expressed gall wasp protein was identified that is hypothesised to stimulate somatic embryogenesis-like development of the gall through interaction with oak tissue glycoproteins. Highly expressed oak genes include those coding for nodulin-like proteins similar to those involved in legume nodule formation. Finally, analysis of the gall wasp genome has revealed potential, but as yet unconfirmed, horizontal gene transfer events into gall wasp genomes. Genes discovered in three gall wasp genomes and expressed in three transcriptomes encode plant cell wall degrading enzymes. They are not of hymenopteran origin, and are most homologous to genes of plant pathogenic bacteria. These genes could be involved in several aspects of gall wasp biology, including feeding and developmental manipulation of host plant tissue.