Quaternary climatic changes and biogeographic barriers drove codiversification in the obligate mutualism between Camponotus laevigatus and its endosymbiont Blochmaniella.

Abstract

Codiversification often arises when hosts and their endosymbionts share a linked evolutionary history, exhibit vertical transmission, or share ecological and biogeographic processes. Most studies on the codiversification of carpenter ants (genus Camponotus) have focused on the co-phylogeny of hosts and endosymbionts across multiple species; however, no studies have examined the intraspecific population-level phylogeographic patterns of codiversification within Camponotus. California has been a geographic focus for phylogeographic studies due to its high endemism and complex geographic structure, and Camponotus laevigatus is a carpenter ant primarily found there. Here, we used whole-genome sequencing from C. laevigatus and its endosymbiont, Blochmaniella to investigate phylogeographic patterns of host-endosymbiont codiversification and estimated kinship of ants sampled near one another. We identified three phylogeographic clusters and isolation-by-distance analyses indicated a positive relationship between genetic and geographic distance in C. laevigatus and Blochmaniella. Using estimates of effective migration surfaces, we found that the Central Valley in California acts as a significant barrier to gene flow among populations. Our phylogenetic analyses revealed the congruent phylogenies of C. laevigatus and Blochmaniella, supporting codiversification. We also estimated kinship among individuals from the same and nearby sampling sites; kinship results indicated full-sister relationships among individuals from the same sampling site, except for three pairwise comparisons, and foragers from nearby sampling sites displayed some shared kinship. Lastly, our demographic analysis revealed a Pleistocene divergence, highlighting the role of Quaternary climatic cycles in shaping the population structure of C. laevigatus.