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.
Highlights
In animals, mitochondrial DNA is assumed to experience a higher mutation rate than nuclear DNA (Ballard and Whitlock 2004)
Despite the popularity of mitochondrial DNA (mtDNA) as a marker in evolutionary studies, this assumption only relies on a handful of comparisons involving mostly vertebrates species (Brown et al 1979; Miyata et al 1982; Nabholz et al 2009)
We sorted these data sets according to 12 taxonomic groups, each of them represented by a variable number of data sets: Squamata N 1⁄4 20; Teleostei N 1⁄4 20; Insecta N 1⁄4 19; Amphibia N 1⁄4 13; Aves N 1⁄4 11; Mollusca N 1⁄4 10; Mammalia N 1⁄4 8; Arachnida N 1⁄4 8; Crustacea N 1⁄4 6; Testudines N 1⁄4 4; Chondrichthyes N 1⁄4 3; Porifera N 1⁄4 1
Summary
Mitochondrial DNA (mtDNA) is assumed to experience a higher mutation rate than nuclear DNA (nuDNA) (Ballard and Whitlock 2004). Taking a comparative approach, Lynch et al (2006) reported contrasted values for the ratio of mtDNA to nuDNA mutation rate (lmit/lnuc) among animals In this analysis, lmit/lnuc varied from 0.57 and 1.43 in corals and mosquitoes, respectively, to around 18 in crickets and aphids and up to 25 in vertebrates. Havird and Sloan (2016) reported a large range of lmit/lnuc in animals and plants with flies (Diptera) showing a clearly lower lmit/lnuc than mammals. These analyses, were based on a limited number of data sets (less than ten nonvertebrate taxa), so that the extent of the variation in lmit/lnuc and its distribution among taxonomic groups is currently unclear
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