Population Genomics of the Wolbachia Endosymbiont in Drosophila melanogaster

Abstract

Wolbachia are maternally inherited symbiotic bacteria, commonly found in arthropods, which are able to manipulate the reproduction of their host in order to maximise their transmission. The evolutionary history of endosymbionts like Wolbachia can be revealed by integrating information on infection status in natural populations with patterns of sequence variation in Wolbachia and host mitochondrial genomes. Here we use whole-genome resequencing data from 290 lines of Drosophila melanogaster from North America, Europe, and Africa to predict Wolbachia infection status, estimate relative cytoplasmic genome copy number, and reconstruct Wolbachia and mitochondrial genome sequences. Overall, 63% of Drosophila strains were predicted to be infected with Wolbachia by our in silico analysis pipeline, which shows 99% concordance with infection status determined by diagnostic PCR. Complete Wolbachia and mitochondrial genomes show congruent phylogenies, consistent with strict vertical transmission through the maternal cytoplasm and imperfect transmission of Wolbachia. Bayesian phylogenetic analysis reveals that the most recent common ancestor of all Wolbachia and mitochondrial genomes in D. melanogaster dates to around 8,000 years ago. We find evidence for a recent global replacement of ancestral Wolbachia and mtDNA lineages, but our data suggest that the derived wMel lineage arose several thousand years ago, not in the 20th century as previously proposed. Our data also provide evidence that this global replacement event is incomplete and is likely to be one of several similar incomplete replacement events that have occurred since the out-of-Africa migration that allowed D. melanogaster to colonize worldwide habitats. This study provides a complete genomic analysis of the evolutionary mode and temporal dynamics of the D. melanogaster–Wolbachia symbiosis, as well as important resources for further analyses of the impact of Wolbachia on host biology. Host–microbe interactions play important roles in the physiology, development, and ecology of many organisms. Studying how hosts and their microbial symbionts evolve together over time is crucial for understanding the impact that microbes have on host biology. With the advent of high-throughput sequencing technologies, it is now possible to obtain complete genomic information for hosts and their associated microbes. Here we use whole-genome sequences from ∼300 strains of the fruitfly Drosophila melanogaster to reveal the evolutionary history of this model species and its intracellular bacterial symbiont Wolbachia. The major findings of this study are that Wolbachia in D. melanogaster is inherited strictly through the egg with no evidence of horizontal transfer from other species, that the genealogies of Wolbachia and mitochondrial genomes are virtually the same, and that both Wolbachia and mitochondrial genomes show evidence for a recent incomplete global replacement event, which has left remnant lineages in North America, Europe, and Africa. We also use the fact that Wolbachia and mitochondrial genomes have the same genealogy to estimate the rate of molecular evolution for Wolbachia, which allows us to put dates on key events in the history of this important host–microbe model system.