Intraspecific mitochondrial gene variation can be as low as that of nuclear rRNA

Abstract

Background: Mitochondrial DNA (mtDNA) has long been used to date historical demographic events. The idea that it is useful for molecular dating rests on the premise that its evolution is neutral. Even though this idea has long been challenged, the evidence against clock-like evolution of mtDNA is often ignored. Here, we present a particularly clear and simple example to illustrate the implications of violations of the assumption of selective neutrality. Methods: DNA sequences were generated for the mtDNA COI gene and the nuclear 28S rRNA of two closely related rocky shore snails, and species-level variation was compared. To our knowledge, this is the first study to use nuclear rRNA at this taxonomic level, presumably because this marker is assumed to evolve so slowly that it is only suitable for phylogenetics. Results: Even though high inter-specific divergence reflected the faster evolutionary rate of COI, intraspecific genetic variation was similar for both markers. As a result, estimates of population expansion times based on mismatch distributions differed between the two markers by millions of years. Conclusions: Assuming that 28S evolves effectively clock-like, these findings can be explained by variation-reducing purifying selection in mtDNA at the species level, and an elevated divergence rate caused by diversifying selection between the two species. Although these two selective forces together make mtDNA suitable as a marker for species identifications by means of DNA barcoding because they create a ‘barcoding gap’, estimates of demographic change based on this marker can be expected to be highly unreliable. Our study contributes to the growing evidence that the utility of mtDNA sequence data beyond DNA barcoding is limited.

phylogatR: Phylogeographic data aggregation and repurposing

“…While single‐locus data has its limitations in making inferences about historical demography (Matumba et al, 2020), DNA barcoding, or the use of other single‐locus DNA markers, has provided tremendous insight into identifying evolutionary significant units and providing information on species in further need of exploration (Bousjein et al, 2021; León‐Tapia, 2021; Nneji et al, 2020; Sholihah et al, 2020; Wang et al, 2020). These data are particularly helpful when aiming to explore broad‐scale patterns such as those on a continental scale (Dincă et al, 2021) or across species (Doorenweerd et al, 2020), especially for a large number of taxonomic groups, as demonstrated here.…”

Coastal dunefields maintain pre‐Holocene genetic structure in a rocky shore red alga

“…Recent research on animals has indicated that mitochondrial DNA can be under strong diversifying selection (Stoeckle and Thaler 2014) and the resulting violation of molecular clock assumptions (Kimura 1983) makes molecular dating problematic (Matumba et al. 2020). Although both markers used in this study are non‐coding, cox2‐3 is linked to protein‐coding genes that are potentially under selection pressure, by virtue of being located on the same genome.…”

Discovery of populations endemic to a marine biogeographical transition zone

“…The data generated here are not considered suitable for inferring what oceanographical conditions existed along the Wild Coast during the time when the regional populations split from their sister taxa. This is because mtDNA is often under strong selection (Meiklejohn, Montooth, & Rand, 2007; Stewart, Freyer, Elson, & Larsson, 2008) and thus violates the assumption of the neutral theory of evolution (Kimura, 1983), which makes its usefulness for molecular dating questionable (Matumba, Oliver, Barker, McQuaid, & Teske, 2020). Our maximum clade credibility tree indicates that the splits may have occurred during the previous interglacial phase (~120,000 years ago) or during the subsequent glacial phase, although potential diversifying selection linked to thermal selection suggests that divergence could have taken place more recently.…”