Wild communities of Morpho butterflies reveal Spiroplasma endosymbiont with inflated genome size and peculiar evolution

AbstractThe evolution of endosymbiont genomes is likely influenced by the ecological interactions with their hosts. Here, we studied the evolution of Spiroplasma genomes, as well as their transmission patterns within and between Morpho butterflies sampled in the wild. Spiroplasma was detected in 4 out of 11 Morpho species studied and displayed a 3 times larger genome size as compared to Spiroplasma genomes 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. Interestingly, these new Spiroplasma genomes also revealed a peculiar evolution of toxin genes in plasmids that may enhance host resistance to parasites. Phylogenetic comparisons with Spiroplasma extracted from other plant and insect host suggest multiple independent colonization of Lepidoptera by Spiroplasma, and probable horizontal exchanges among distantly-related butterfly species occurring in South America. In contrast, resequencing data obtained for multiple populations of the two sister-species M. helenor and M. achilles living in sympatry over the majority of their distribution revealed an opposite prevalence (97% in M. achilles and 3% in M. helenor), suggesting low levels of transmission between these sympatric host- species. Reconciliation analysis of the phylogenetic relationships of mitochondrial genomes within M. achilles and Spiroplasma strains furthermore confirms predominant vertical transfers of the endosymbiont within species. Altogether, our results indicate persistent interactions between Spiroplasma symbiont and some Morpho species, as well as contrasted prevalence among sympatric host-species, consistent with an evolution of ecological interactions between the endosymbiont and its different hosts that may modify their genomic evolution.