Impact of host evolutionary history on endosymbiont genome evolution: a test in Camponotus carpenter ants and their Blochmannia endosymbionts

Mutualism discernibly connects the evolution of two or more interacting taxa. Endosymbioses, especially those that are obligate, are an intimate mutualism that link the evolution of host and endosymbiont. In these instances, we may expect codiversification of hosts and endosymbionts as well as host demography discernibly affecting the course of endosymbiont evolution. While many studies have demonstrated cospeciation of hosts and endosymbionts, detailed investigations of the impact of host demography on endosymbiont molecular evolution are generally lacking. Here, we sequenced complete genomes of carpenter ants (Genus Camponotus) and their Blochmannia endosymbionts to investigate their codiversification and test hypotheses about how host demography impacts molecular evolution in endosymbionts. Using whole genome phylogenomics, we identified strong signatures of codiversification between carpenter ants and their endosymbionts. We found that endosymbiont genes have evolved rapidly, at a pace of ~30x that of their hosts. Using multiple tests for selection in Blochmannia genes, we found signatures of positive selection and shifts in selection strength across the phylogeny. We identified a positive relationship between host demography and shifts toward intensified selection in endosymbiont genes, but no relationship between host demography and shifts toward relaxed selection in endosymbiont genes. About 10% of the Blochmannia genes exhibited variable presence and absence across endosymbiont genomes. Of those, about half exhibited phylogenetic signal, indicating somewhat random patterns of gene loss in endosymbiont genomes. Lastly, we found no relationship between host demography and endosymbiont gene loss.