<i>Wolbachia</i>Acquisition by<i>Drosophila yakuba</i>-Clade Hosts and Transfer of Incompatibility Loci Between Distantly Related<i>Wolbachia</i>

Abstract

Maternally transmitted <i>Wolbachia</i> infect about half of insect species, yet the predominant mode(s) of <i>Wolbachia</i> acquisition remains uncertain. Species-specific associations could be old, with <i>Wolbachia</i> and hosts codiversifying (<i>i.e.</i>, cladogenic acquisition), or relatively young and acquired by horizontal transfer or introgression. The three <i>Drosophila yakuba</i>-clade hosts [(<i>D. santomea</i>, <i>D. yakuba</i>) <i>D. teissieri</i>] diverged ∼3 MYA and currently hybridize on the West African islands Bioko and São Tomé. Each species is polymorphic for nearly identical <i>Wolbachia</i> that cause weak cytoplasmic incompatibility (CI)-reduced egg hatch when uninfected females mate with infected males. <i>D. yakuba</i>-clade <i>Wolbachia</i> are closely related to <i>w</i>Mel, globally polymorphic in <i>D. melanogaster</i> We use draft <i>Wolbachia</i> and mitochondrial genomes to demonstrate that <i>D. yakuba</i>-clade phylogenies for <i>Wolbachia</i> and mitochondria tend to follow host nuclear phylogenies. However, roughly half of <i>D. santomea</i> individuals, sampled both inside and outside of the São Tomé hybrid zone, have introgressed <i>D. yakuba</i> mitochondria. Both mitochondria and <i>Wolbachia</i> possess far more recent common ancestors than the bulk of the host nuclear genomes, precluding cladogenic <i>Wolbachia</i> acquisition. General concordance of <i>Wolbachia</i> and mitochondrial phylogenies suggests that horizontal transmission is rare, but varying relative rates of molecular divergence complicate chronogram-based statistical tests. Loci that cause CI in <i>w</i>Mel are disrupted in <i>D. yakuba</i>-clade <i>Wolbachia</i>; but a second set of loci predicted to cause CI are located in the same WO prophage region. These alternative CI loci seem to have been acquired horizontally from distantly related <i>Wolbachia</i>, with transfer mediated by flanking <i>Wolbachia</i>-specific ISWpi1 transposons.