Symbiosis between multicellular organisms and microbial symbionts is near universal, and it is now clear that many aspects of organismal biology in health and disease cannot be understood without reference to interactions with microbes. In insects, this includes a diverse range of heritable symbionts, which pass from a female host to her progeny. These symbionts are highly adapted to their host, and encode important properties, such as defence against natural enemies. These properties are used in control of vector borne diseases, such as transmission of the virus causing dengue fever from mosquito to humans.
In contrast to classical adaptive phenotypes, symbiont traits generally arise through a host shift event – the movement of a microbe from into a novel host species. Experimental host shift experiments indicate that there is a compatibility filter: some symbionts in novel host species cause little pathology and transmit vertically efficiently, whereas other do not. Understanding this compatibility filter will clarify the patterns through which host shifts occur in nature, and create a principled basis for manipulation of compatibility, for instance in symbiont-mediated control of vector competence.
The project ‘SYMBCOMPAT’ aimed to identify factors governing host-symbiont compatibility. For inherited bacterial symbionts of arthropods it had been established that in addition to transmission from host mother to offspring, lateral transfers between unrelated individuals (i.e. establishment of novel symbioses) also occur, both in nature and in laboratory settings. It had further been observed that some host-symbiont combinations create a good fit (low cost of symbiont in novel host, high vertical transmission fidelity) while others are not a good fit (high cost of harbouring symbiont and/or low vertical transmission efficiency). However, it had been unclear what mechanisms drive the goodness of fit between host and symbiont.
In this project, we used the natural Drosophila symbiont Spiroplasma to artificially create a novel symbiosis with a bad fit: Spiroplasma was transferred from its natural host Drosophila hydei into Drosophila melanogaster, where it causes pathogenicity, but evolves to become non-pathogenic over ~20 host generations of adaptation to the novel host. Using this experimental setting, the objectives were 1) to identify the cause of the bad fit, i.e. the initial pathogenicity, and 2) identify the genomic changes within Spiroplasma that are associated with evolution of pathogenicity loss, as factors evolving quickly after host shifts were expected to be good candidates for factors important in establishing symbiosis.
The results of this project will impact both upon our understanding of an important natural process and enable better exploitation of symbiont encoded traits in control of vector born disease.
