Evolutionary rates are correlated between cockroach symbionts and mitochondrial genomes

Abstract

Bacterial endosymbionts evolve under strong host-driven selection. Factors influencing host evolution might affect symbionts in similar ways, potentially leading to correlations between the molecular evolutionary rates of hosts and symbionts. Although there is evidence of rate correlations between mitochondrial and nuclear genes, similar investigations of hosts and symbionts are lacking. Here, we demonstrate a correlation in molecular rates between the genomes of an endosymbiont (Blattabacterium cuenoti) and the mitochondrial genomes of their hosts (cockroaches). We used partial genome data for multiple strains of B. cuenoti to compare phylogenetic relationships and evolutionary rates for 55 cockroach/symbiont pairs. The phylogenies inferred for B. cuenoti and the mitochondrial genomes of their hosts were largely congruent, as expected from their identical maternal and cytoplasmic mode of inheritance. We found a correlation between evolutionary rates of the two genomes, based on comparisons of root-to-tip distances and on comparisons of the branch lengths of phylogenetically independent species pairs. Our results underscore the profound effects that long-term symbiosis can have on the biology of each symbiotic partner.

Keywords: Blattabacterium cuenoti; cockroach; host–symbiont interaction; molecular evolution; phylogeny; substitution rate.

Figure 1.

Congruence between (a) the phylogenetic tree of host cockroaches inferred using maximum likelihood from whole mitochondrial genomes and (b) the phylogenetic tree of Blattabacterium inferred using maximum likelihood from 104 protein-coding genes (third codon sites excluded from both datasets). Shaded circles at nodes indicate bootstrap values (black = 100%, grey = 85–99%). Nodes without black or grey circles have bootstrap values less than 85%. Red outlines on circles indicate disagreement between the phylogenies. Branches are coloured according to their membership of different cockroach families. (Online version in colour.)

Figure 2.

Comparison of evolutionary rates of Blattabacterium symbionts and their host cockroaches. (a) Correlation of root-to-tip distances in phylogenies of Blattabacterium and cockroaches, inferred using maximum-likelihood analysis of protein-coding genes from each dataset, with third codon sites excluded. (b) Correlation of root-to-tip differences following the removal of five rapidly evolving ectobiid taxa (Amazonina sp., Chorisoserrata sp., Allacta sp., Balta sp. and Euphyllodromia sp.) and two anaplectids. Colours represent data from representatives of different cockroach families, as shown in the colour key. (c) Correlation of log-transformed branch-length differences between phylogenetically independent pairs of host and symbiont taxa, based on protein-coding genes only, and (d) with the addition of rRNAs and tRNAs to the host mitochondrial dataset. (Online version in colour.)