Concerted genome expansion of heritable symbionts in an insect host

Abstract

Maternally transmitted symbionts represent important components of arthropod biology, acting as both beneficial partners and as reproductive parasites. Their strict vertical transmission greatly reduces their effective population size, making selection less efficient and driving a pattern of molecular evolution where genome size reduces. Contrastingly, there are sporadic observations of genome expansion in symbionts from clades where the genome has previously reduced in size. It is currently unclear whether these events are an idiosyncratic consequence of exposure to novel active mobile elements, or are driven by the host context. In this paper, we report the concerted genome expansion of two co-infecting heritable symbionts that supports a host-related driver of expansion. We assembled the genomes of Spiroplasma and Rickettsia bacteria that co-infect the lacewing Mallada desjardinsi. Both symbionts had the largest genome reported to date in their clade, approximately twice the median size for their respective genus. Genome expansion was driven by proliferation of mobile elements in both cases, but the underpinning elements were distinct. The observation that the proximate causes of expansion differed between symbionts led us to reject the hypothesis that concerted expansion was driven by a common mobile element invasion. We hypothesize these processes are driven either by bottleneck events impacting host population size, by the host environment causing stress-induced activation of mobile genetic elements, or by both symbionts having undergone a recent and coincident transition to vertical transmission.