Abstract
Wolbachia pipientis is an intracellular endosymbiont infecting many arthropods and filarial nematodes. Little is known about the short-term evolution of Wolbachia or its interaction with its host. Wolbachia is maternally inherited, resulting in co-inheritance of mitochondrial organelles such as mtDNA. Here I explore the evolution of Wolbachia, and the relationship between Wolbachia and mtDNA, using a large inbred panel of Drosophila simulans. I compare this to the only other large population genomic Wolbachia dataset from D. melanogaster. I find reduced diversity relative to expectation in both Wolbachia and mtDNA, but only mtDNA shows evidence of a recent selective sweep or population bottleneck. I estimate Wolbachia and mtDNA titre in each genotype, and I find considerable variation in both phenotypes, despite low genetic diversity in Wolbachia and mtDNA. A phylogeny of Wolbachia and of mtDNA suggest a recent origin of the infection derived from a single origin. Using Wolbachia and mtDNA titre as a phenotype, I perform the first association analysis using this phenotype with the nuclear genome and find several implicated regions, including one which contains four CAAX-box protein processing genes. CAAX-box protein processing can be an important part of host-pathogen interactions in other systems, suggesting interesting directions for future research.
Highlights
Heritable symbiotic associations such as that between Drosophila and Wolbachia pipientis have widespread impact on host ecology and evolution
It is thought to have been horizontally transmitted to D. simulans from D. ananassae, though the same strain is found in D. suzukii[22]
Wolbachia DNA is frequently inserted into the host genome, though this has not occurred with wRi in D. simulans[21]
Summary
Heritable symbiotic associations such as that between Drosophila and Wolbachia pipientis have widespread impact on host ecology and evolution. Most notably mtDNA will be forced through a bottleneck, lowering the diversity of mtDNA in infected populations[18,23,24] This will cause mtDNA and Wolbachia to be more closely associated than nuclear genes, and this coupling has been demonstrated previously in D. simulans[18,23,25]. D. simulans is known to have three major mitochondrial haplotypes (siI, siII, and siIII) and two subtypes (siIIA and siIIB) that harbor very little variation and that appear to be nonrandomly associated with Wolbachia strains[26,27,28]. Differences in Wolbachia titre when it is transinfected between species suggests a role of host background in controlling copy number, population genomics in D. melanogaster suggest an effect of host background, and there does seem to be host-specific patterns of tissue colonization[52,53,54]. It is possible to select for greater Wolbachia densities, though the heritability of this is unclear[56,57]
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