Evolutionary Rates are Correlated Between Buchnera Endosymbionts and the Mitochondrial Genomes of Their Aphid Hosts.

The evolution of bacterial endosymbiont genomes is strongly influenced by host-driven selection. Factors affecting host genome evolution will potentially affect endosymbiont genomes in similar ways. One potential outcome is correlations in molecular rates between the genomes of the symbiotic partners. Recently, we presented the first evidence of such correlations between the mitochondrial genomes of cockroaches and the genomes of their endosymbiont (Blattabacterium cuenoti). Here we investigate whether similar patterns are found in additional host-symbiont partners. We use partial genome data from multiple strains of the bacterial endosymbionts Buchnera aphidicola and Sulcia muelleri, and the mitochondrial genomes of their sap-feeding insect hosts. Both endosymbionts show phylogenetic congruence with the mitochondria of their hosts, a result that is expected due to their identical mode of inheritance. We compared root-to-tip distances and branch lengths of phylogenetically independent species pairs. Both analyses showed a highly significant correlation of molecular rates between the genomes of Buchnera and the mitochondrial genomes of their hosts. A similar correlation was detected between Sulcia and their hosts, but was not statistically significant. Our results indicate that evolutionary rate correlations between hosts and long-term symbionts may be a widespread phenomenon.

Evolutionary rates are correlated between cockroach symbionts and mitochondrial genomes.

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.

Transoceanic Dispersal and Plate Tectonics Shaped Global Cockroach Distributions: Evidence from Mitochondrial Phylogenomics.

Following the acceptance of plate tectonics theory in the latter half of the 20th century, vicariance became the dominant explanation for the distributions of many plant and animal groups. In recent years, however, molecular-clock analyses have challenged a number of well-accepted hypotheses of vicariance. As a widespread group of insects with a fossil record dating back 300 My, cockroaches provide an ideal model for testing hypotheses of vicariance through plate tectonics versus transoceanic dispersal. However, their evolutionary history remains poorly understood, in part due to unresolved relationships among the nine recognized families. Here, we present a phylogenetic estimate of all extant cockroach families, as well as a timescale for their evolution, based on the complete mitochondrial genomes of 119 cockroach species. Divergence dating analyses indicated that the last common ancestor of all extant cockroaches appeared ∼235 Ma, ∼95 My prior to the appearance of fossils that can be assigned to extant families, and before the breakup of Pangaea began. We reconstructed the geographic ranges of ancestral cockroaches and found tentative support for vicariance through plate tectonics within and between several major lineages. We also found evidence of transoceanic dispersal in lineages found across the Australian, Indo-Malayan, African, and Madagascan regions. Our analyses provide evidence that both vicariance and dispersal have played important roles in shaping the distribution and diversity of these insects.

Parallel evolution of mound-building and grass-feeding in Australian nasute termites.

Termite mounds built by representatives of the family Termitidae are among the most spectacular constructions in the animal kingdom, reaching 6-8 m in height and housing millions of individuals. Although functional aspects of these structures are well studied, their evolutionary origins remain poorly understood. Australian representatives of the termitid subfamily Nasutitermitinae display a wide variety of nesting habits, making them an ideal group for investigating the evolution of mound building. Because they feed on a variety of substrates, they also provide an opportunity to illuminate the evolution of termite diets. Here, we investigate the evolution of termitid mound building and diet, through a comprehensive molecular phylogenetic analysis of Australian Nasutitermitinae. Molecular dating analysis indicates that the subfamily has colonized Australia on three occasions over the past approximately 20 Myr. Ancestral-state reconstruction showed that mound building arose on multiple occasions and from diverse ancestral nesting habits, including arboreal and wood or soil nesting. Grass feeding appears to have evolved from wood feeding via ancestors that fed on both wood and leaf litter. Our results underscore the adaptability of termites to ancient environmental change, and provide novel examples of parallel evolution of extended phenotypes.

Increased Mutation Rate Is Linked to Genome Reduction in Prokaryotes.

The evolutionary processes that drive variation in genome size across the tree of life remain unresolved. Effective population size (Ne) is thought to play an important role in shaping genome size [1-3]-a key example being the reduced genomes of insect endosymbionts, which undergo population bottlenecks during transmission [4]. However, the existence of reduced genomes in marine and terrestrial prokaryote species with large Ne indicate that genome reduction is influenced by multiple processes [3]. One candidate process is enhanced mutation rate, which can increase adaptive capacity but can also promote gene loss. To investigate evolutionary forces associated with prokaryotic genome reduction, we performed molecular evolutionary and phylogenomic analyses of nine lineages from five bacterial and archaeal phyla. We found that gene-loss rate strongly correlated with synonymous substitution rate (a proxy for mutation rate) in seven of the nine lineages. However, gene-loss rate showed weak or no correlation with the ratio of nonsynonymous/synonymous substitution rate (dN/dS). These results indicate that genome reduction is largely associated with increased mutation rate, while the association between gene loss and changes in Ne is less well defined. Lineages with relatively high dS and dN, as well as smaller genomes, lacked multiple DNA repair genes, providing a proximate cause for increased mutation rates. Our findings suggest that similar mechanisms drive genome reduction in both intracellular and free-living prokaryotes, with implications for developing a comprehensive theory of prokaryote genome size evolution.

EasyCodeML: A visual tool for analysis of selection using CodeML.

The genomic signatures of positive selection and evolutionary constraints can be detected by analyses of nucleotide sequences. One of the most widely used programs for this purpose is CodeML, part of the PAML package. Although a number of bioinformatics tools have been developed to facilitate the use of CodeML, these have various limitations. Here, we present a wrapper tool named EasyCodeML that provides a user-friendly graphical interface for using CodeML. EasyCodeML has a custom running mode in which parameters can be adjusted to meet different requirements. It also offers a preset running mode in which an evolutionary analysis pipeline and publication-quality tables can be exported by a single click. EasyCodeML allows visualized, interactive tree labelling, which greatly simplifies the use of the branch, branch-site, and clade models of selection. The program allows comparison of major codon-based models for analyses of selection. EasyCodeML is a stand-alone package that is supported in Windows, Mac, and Linux operating systems, and is freely available at https://github.com/BioEasy/EasyCodeML.