Exploring the determinants of polydnavirus chromosomal integration across host-parasitoid wasp systems

Polydnaviruses (PDV) are domesticated viruses integrated into the genome of parasitoid wasps. During oviposition, female wasps inject into their host both eggs and PDV particles containing wasp DNA circles. Circle-borne genes are expressed in the host and suppress its immune response, ensuring successful development of the wasp larvae. Several dozen distinct circles have been distinguished on the basis of their sequence and location within the wasp genome. Interestingly, these circles display very different propensities to integrate into the caterpillar genome but the factors influencing this variation remain poorly understood. Here, we experimentally quantified and modelled both the number of PDV integrations and the abundance of injected PDV circles in 8 distinct wasp-host systems. Integrations into the host genomes were observed at rates ranging across wasp species from 0.28 to 14.5 integrations per host haploid genome. Our analyses reveal that integration efficiency varies among circles. We particularly highlight a specific circle, referred to as circle 1, which we find to be both the most abundantly injected and the most efficiently integrated, even after controlling for the direct effects of the quantity injected on the total number of integrations. This pattern is compatible with the view that both the quantity and integration efficiency of injected circles may constitute key components of parasitism success. Finally, our analyses indicate that integration efficiency is reduced in non-suitable hosts, suggesting a possible contribution of host factors to the regulation of PDV circle integration.