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.

College of Plant Protection Southwest University Chongqing People's Republic of China

Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague Czech Republic

Okinawa Institute of Science and Technology Graduate University Tancha Onna son Okinawa Japan

School of Life and Environmental Sciences University of Sydney Sydney Australia

Zobrazit více v PubMed

Bromham L. 2009. Why do species vary in their rate of molecular evolution? Biol. Lett. 5, 401–404. (10.1098/rsbl.2009.0136) PubMed DOI PMC

Ho SYW, Lo N. 2013. The insect molecular clock. Aust. J. Entomol. 52, 101–105. (10.1111/aen.12018) DOI

Douglas AE. 2010. The symbiotic habit. Princeton, NJ: Princeton University Press.

Martin AP. 1999. Substitution rates of organelle and nuclear genes in sharks: implicating metabolic rate (again). Mol. Biol. Evol. 16, 996–1002. (10.1093/oxfordjournals.molbev.a026189) PubMed DOI

Sheldon FH, Jones CE, McCracken KG. 2000. Relative patterns and rates of evolution in heron nuclear and mitochondrial DNA. Mol. Biol. Evol. 17, 437–450. (10.1093/oxfordjournals.molbev.a026323) PubMed DOI

Lourenço JM, Glémin S, Chiari Y, Galtier N. 2013. The determinants of the molecular substitution process in turtles. J. Evol. Biol. 26, 38–50. (10.1111/jeb.12031) PubMed DOI

Sloan DB, Alverson AJ, Wu M, Palmer JD, Taylor DR. 2012. Recent acceleration of plastid sequence and structural evolution coincides with extreme mitochondrial divergence in the angiosperm genus Silene. Genome Biol. Evol. 4, 294–306. (10.1093/gbe/evs006) PubMed DOI PMC

Smith DR, Lee RW. 2010. Low nucleotide diversity for the expanded organelle and nuclear genomes of Volvox carteri supports the mutational-hazard hypothesis. Mol. Biol. Evol. 27, 2244–2256. (10.1093/molbev/msq110) PubMed DOI

Hua J, Smith DR, Borza T, Lee RW. 2012. Similar relative mutation rates in the three genetic compartments of Mesostigma and Chlamydomonas. Protist 163, 105–115. (10.1016/j.protis.2011.04.003) PubMed DOI

Yan Z, Ye G, Werren JH. 2019. Evolutionary rate correlation between mitochondrial-encoded and mitochondria-associated nuclear-encoded proteins in insects. Mol. Biol. Evol. 36, 1022–1036. (10.1093/molbev/msz036) PubMed DOI

Degnan PH, Lazarus AB, Brock CD, Wernegreen JJ. 2004. Host–symbiont stability and fast evolutionary rates in an ant–bacterium association: cospeciation of Camponotus species and their endosymbionts, Candidatus Blochmannia. Syst. Biol. 53, 95–110. (10.1080/10635150490264842) PubMed DOI

Bourguignon T, et al. . 2018. Transoceanic dispersal and plate tectonics shaped global cockroach distributions: evidence from mitochondrial phylogenomics. Mol. Biol. Evol. 35, 970–983. (10.1093/molbev/msy013) PubMed DOI

Evangelista DA, et al. 2019. An integrative phylogenomic approach illuminates the evolutionary history of cockroaches and termites (Blattodea). Proc. R. Soc. B 286, 20182076 (10.1098/rspb.2018.2076) PubMed DOI PMC

Cornwell PB. 1968. The cockroach. London, UK: Hutchinson.

Sacchi L, Corona S, Grigolo A, Laudani U, Selmi MG, Bigliardi E. 1996. The fate of the endocytobionts of Blattella germanica (Blattaria: Blattellidae) and Periplaneta americana (Blattaria: Blattidae) during embryo development. Ital. J. Zool. 63, 1–11. (10.1080/11250009609356100) DOI

López-Sánchez MJ, Neef A, Peretó J, Patiño-Navarrete R, Pignatelli M, Latorre A, Moya A. 2009. Evolutionary convergence and nitrogen metabolism in Blattabacterium strain Bge, primary endosymbiont of the cockroach Blattella germanica. PLoS Genet. 5, e1000721 (10.1371/journal.pgen.1000721) PubMed DOI PMC

Sabree ZL, Huang CY, Arakawa G, Tokuda G, Lo N, Watanabe H, Moran NA. 2012. Genome shrinkage and loss of nutrient-providing potential in the obligate symbiont of the primitive termite Mastotermes darwiniensis. Appl. Environ. Microbiol. 78, 204–210. (10.1128/AEM.06540-11) PubMed DOI PMC

Kinjo Y, et al. . 2018. Parallel and gradual genome erosion in the Blattabacterium endosymbionts of Mastotermes darwiniensis and Cryptocercus wood roaches. Genome Biol. Evol. 10, 1622–1630. (10.1093/gbe/evy110) PubMed DOI PMC

Vicente CSL, Mondal SI, Akter A, Ozawa S, Kikuchi T, Hasegawa K. 2018. Genome analysis of new Blattabacterium spp., obligatory endosymbionts of Periplaneta fuliginosa and P. japonica. PLoS ONE 13, e0200512 (10.1371/journal.pone.0200512) PubMed DOI PMC

Kambhampati S, Alleman A, Park Y. 2013. Complete genome sequence of the endosymbiont Blattabacterium from the cockroach Nauphoeta cinerea (Blattodea: Blaberidae). Genomics 102, 479–483. (10.1016/j.ygeno.2013.09.003) PubMed DOI

Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313. (10.1093/bioinformatics/btu033) PubMed DOI PMC

Legendre P, Desdevises Y, Bazin E. 2002. A statistical test for host–parasite coevolution. Syst. Biol. 51, 217–234. (10.1080/10635150252899734) PubMed DOI

R Development Core Team. 2018. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Moran NA, Bennett GM. 2014. The tiniest tiny genomes. Annu. Rev. Microbiol. 68, 195–215. (10.1146/annurev-micro-091213-112901) PubMed DOI

Mao M, Yang X, Bennett GM. 2018. Evolution of host support for two ancient bacterial symbionts with differentially degraded genomes in a leafhopper host. Proc. Natl Acad. Sci. USA 115, E11691–E11700. (10.1073/pnas.1811932115) PubMed DOI PMC

Wolschin F, Hölldobler B, Gross R, Zientz E. 2004. Replication of the endosymbiotic bacterium Blochmannia floridanus is correlated with the developmental and reproductive stages of its ant host. Appl. Environ. Microbiol. 70, 4096–4102. (10.1128/AEM.70.7.4096-4102.2004) PubMed DOI PMC

Lo N, Bandi C, Watanabe H, Nalepa C, Beninati T. 2003. Evidence for cocladogenesis between diverse dictyopteran lineages and their intracellular endosymbionts. Mol. Biol. Evol. 20, 907–913. (10.1093/molbev/msg097) PubMed DOI

Clark JW, Hossain S, Burnside CA, Kambhampati S. 2001. Coevolution between a cockroach and its bacterial endosymbiont: a biogeographical perspective. Proc. R. Soc. B 268, 393–398. (10.1098/rspb.2000.1390) PubMed DOI PMC

Garrick RC, Sabree ZL, Jahnes BC, Oliver JC. 2017. Strong spatial-genetic congruence between a wood-feeding cockroach and its bacterial endosymbiont, across a topographically complex landscape. J. Biogeogr. 44, 1500–1511. (10.1111/jbi.12992) DOI

Arab DA, Bourguignon T, Wang Z, Ho SYW, Lo N.. 2020. Data from: Evolutionary rates are correlated between cockroach symbiont and mitochondrial genomes Dryad Digital Repository. (10.5061/dryad.v6wwpzgqw) PubMed DOI PMC

Evolutionary rates are correlated between cockroach symbionts and mitochondrial genomes

Zobrazit více v PubMed

Dryad
10.5061/dryad.v6wwpzgqw

figshare
10.6084/m9.figshare.c.4768733