What makes a symbiont succeed? The role of host shifts in arthropod symbiont evolution.

About half of all insect and spider species carry specialised symbiotic bacteria that are transmitted from mothers to offspring (“inherited symbionts”) and typically cannot reproduce outside their arthropod hosts. Inherited symbionts may affect their hosts in profound ways: they contribute to nutrition, alter reproductive output, or provide protection from pathogens. Key to the success of inherited symbionts and the reason for their ubiquitous nature is their ability to shift hosts, i.e., establish in novel host species. While we know how novel symbionts may impact arthropods, we have a very limited understanding of symbiont properties important in host shifts: We do not know why some symbionts are better host shifters than others and how the process of establishing in novel hosts impacts symbionts. These questions are fundamental for our appreciation of symbiont ecology and evolution as well as arthropod biology. Further, they are of applied interest for biological control of disease through pathogen blocking symbionts.

We will address these issues by consolidating experimental evolution of highly evolvable Spiroplasma symbionts with genomic surveys of Wolbachia symbionts in natural host populations. Firstly, we will determine symbiont properties important in host shifts. To this end, we will artificially create host shifts in the laboratory, and experimentally evolve Spiroplasma symbionts in novel Drosophila hosts. Key factors in host shifts evolve quickly when novel symbioses are established, and will be characterised using symbiont genome sequencing before and after adaptation to novel hosts. We will independently verify these factors by genomic comparison of very common and very rare Wolbachia strains from bee populations, as representatives of good and poor host shifters, respectively. Secondly, we ask how environmental factors determine a symbiont’s success in hot shifting. Using experimental evolution, we will monitor how well Spiroplasma establishes in novel Drosophila hosts under varying temperatures (which may impact Spiroplasma fitness) and in the presence of parasitoid wasps (against which Spiroplasma confers protection). We will further determine if the presence of pathogens aids in the establishment of novel, potentially pathogen-blocking Wolbachia symbionts in natural bee populations. Thirdly, we will ascertain how adaptation to novel hosts impacts symbiont fitness and host shifting ability. We will experimentally adapt Spiroplasma strains to frequent host shifting or to a single novel host. Fitness of the evolved strains will then be determined in their novel and other hosts to better understand the trade-off between maximising fitness in a single host and retaining the ability to infect many other potential hosts. In sum, the project will lead to a better understanding of the role of symbionts in host shifts, which will ultimately help to explain the extraordinary diversity and abundance of inherited symbionts in arthropods.

This project is funded by DFG's Emmy Noether-Programme (Project number 497854142).