Large Variation in the Ratio of Mitochondrial to Nuclear Mutation Rate across Animals: Implications for Genetic Diversity and the Use of Mitochondrial DNA as a Molecular Marker

Abstract

It is commonly assumed that mitochondrial DNA (mtDNA) evolves at a faster rate than nuclear DNA (nuDNA) in animals. This has contributed to the popularity of mtDNA as a molecular marker in evolutionary studies. Analyzing 121 multilocus data sets and four phylogenomic data sets encompassing 4,676 species of animals, we demonstrate that the ratio of mitochondrial over nuclear mutation rate is highly variable among animal taxa. In nonvertebrates, such as insects and arachnids, the ratio of mtDNA over nuDNA mutation rate varies between 2 and 6, whereas it is above 20, on average, in vertebrates such as scaled reptiles and birds. Interestingly, this variation is sufficient to explain the previous report of a similar level of mitochondrial polymorphism, on average, between vertebrates and nonvertebrates, which was originally interpreted as reflecting the effect of pervasive positive selection. Our analysis rather indicates that the among-phyla homogeneity in within-species mtDNA diversity is due to a negative correlation between mtDNA per-generation mutation rate and effective population size, irrespective of the action of natural selection. Finally, we explore the variation in the absolute per-year mutation rate of both mtDNA and nuDNA using a reduced data set for which fossil calibration is available, and discuss the potential determinants of mutation rate variation across genomes and taxa. This study has important implications regarding DNA-based identification methods in predicting that mtDNA barcoding should be less reliable in nonvertebrates than in vertebrates.

Leap‐frog dispersal and mitochondrial introgression: Phylogenomics and biogeography of Limnonectes fanged frogs in the Lesser Sundas Archipelago of Wallacea

“…A nuclear DNA mutation rate of 1.42 × 10 −9 substitutions per site per year estimated for the ranoid frog genus Leptopelis (Allio, Donega, Galtier, & Nabholz, ) was used to convert parameter estimates into real world values such as population divergence time in years, effective population size in individuals and population migration rate in individual migrants per generation. All values for Theta and Tau generated by g ‐ phocs are scaled by 10 −4 .…”

Integrating three comprehensive data sets shows that mitochondrial DNA variation is linked to species traits and paleogeographic events in European butterflies

“…Understanding the emergence and maintenance of genetic differentiation exposes fundamental evolutionary processes over a range of spatial and temporal scales. The resolution of such studies has advanced greatly since the onset of DNA sequencing (Allio, Donega, Galtier, & Nabholz, ; Bazin, Glémin, & Galtier, ; Lewontin, ; Nabholz, Mauffrey, Bazin, Galtier, & Glemin, ; Mackintosh et al, ).…”

“…Despite this clear theoretical statement, DNA polymorphism appeared to be weakly correlated to population size and, when correlations have been found, the genetic diversity revealed is orders of magnitude smaller than expected based on differences in population size (Bazin et al, ; Leffler et al, ; Nabholz et al, ; Romiguier et al, ; Mackintosh et al, ). Moreover, the results greatly varied among studies comparing genetic diversity for different taxa as well as when using different genetic markers (such as allozymes, nuclear or mitochondrial markers; Allio et al, ; Bazin et al, ; Fujisawa, Vogler, & Barraclough, ; Leffler et al, ; Nabholz, Glémin, & Galtier, ; Nabholz et al, ; Romiguier et al, ; Mackintosh et al, ).…”

“…First of all, mtDNA has a faster mutation rate compared to nDNA and can show signatures of recent differentiation (e.g., intraspecific) as well as relatively old (Avise, ; Hebert, Cywinska, Ball, & deWaard, ). Secondly, because mtDNA is haploid, maternally inherited and recombination is limited to rare cases of heteroplasmy, its effective population size is four times smaller and coalescence times shorter than in nuclear DNA (Allio et al, ; Nabholz et al, ). mtDNA is involved in respiration processes and has been found to be under strong selection (Galtier, Nabholz, Glémin, & Hurst, ; Nabholz et al, ; Pentinsaari, Salmela, Mutanen, & Roslin, ).…”

Salmo macrostigma(Teleostei, Salmonidae): Nothing more than a brown trout (S. trutta) lineage?

“…Mitochondrial DNA markers are valued for phylogenetic reconstructions using both museum and fresh samples because nucleic acids degrade over time and mitochondrial genomes (mtDNA) are available at much higher copy numbers per cell compared with single‐copy nuclear DNA (Höss, ; Wandeler et al ., ) and because mtDNA has reliable barcoding properties across vertebrates, including fishes (Allio et al ., ). Despite its uniparental inheritance, mtDNA remains an important marker in studies of the S. trutta complex partly because so much data are already available from previous salmonid studies (Bernatchez et al ., ; Crête‐Lafrenière et al ., ; Snoj et al ., ; Sušnik et al ., ; Verspoor et al ., ) and partly because a well‐supported mtDNA‐based hypothesis of phylogenetic relationships is available (Bernatchez, ; Cortey et al ., ; Sanz, ; Snoj et al ., ; Vera et al ., ).…”