Wild communities ofMorphobutterflies revealSpiroplasmaendosymbiont with inflated genome size and peculiar evolution

Abstract

AbstractThe evolution of endosymbiont genomes is likely influenced by the ecological interactions with their hosts. Here, we studied the evolution ofSpiroplasmagenomes detected withinMorphobutterflies sampled in the wild.Spiroplasmawas detected in 4 out of the 11Morphospecies studied and displayed a 3 times larger genome size as compared toSpiroplasmagenomes documented in other hosts. This inflation in genome size is caused by massive and recent expansion of various mobile genetic elements and by the acquisition of new genes stemming from prophages. In particular, we documented the peculiar evolution of the toxin genes in plasmids that may enhance host resistance to parasites. Phylogenetic comparisons withSpiroplasmaextracted from other host point at a unique origin ofSpiroplasmainMorpho, and strong divergence fromSpiroplasmafound in other Lepidoptera. Resequencing data obtained for multiple populations of the two sister-speciesM. helenorandM. achillesliving in sympatry over the majority of their distribution revealed a opposite prevalence (97% inM. achillesand 3% inM. helenor), suggesting contrasted ecological interactions with these two host-species. Reconciliation analysis of the phylogenetic relationships ofMorphomitochondrial genomes andSpiroplasmagenomes was then consistent with a predominant vertical transfer of the endosymbiont. Altogether, our results suggest a key role of ecological interactions with the host in the evolution of endosymbiont genomes and point at a putative interaction ofSpiroplasmawith reproductive isolation between sympatric species of butterflies.