An explanation for why mitochondrial barcoding fails
DNA barcoding using sequences from mt-encoded proteins or rRNA works very well for bilaterian animals, but it is much less effective in delimiting species boundaries of some other eukaryotic taxa, particularly plants (Chase et al. 2005; Kress et al. 2005) and fungi (Xu 2016) but also Porifera (sponges) and Anthozoa (corals and sea anemones)(Huang et al. 2008). Recombination of mt genomes, which is rare or non-existent in bilaterian animals, slows down or stops selective sweeps because beneficial alleles can be fixed in a mt genotype independent of the frequencies of other genes on the mt chromosome (Charlesworth et al. 1993; Rokas et al. 2003; White et al. 2008). The hypothesis for the evolution of barcode gaps that I outline in this paper, therefore, provides testable hypotheses for why mt DNA barcoding might fail for some taxa. If the efficacy of barcoding is dependent on selective sweeps, which in turn is dependent on lack of recombination of mt genomes, then it follows that taxa with recombination of mt genes will have a poor mt DNA barcode signal. Intriguingly, the mt genomes of Porifera and Anthozoa, for which mt DNA barcoding also works poorly, include introns, have very low mutation rates, and likely engage in recombination (Gissi et al. 2008; Huang et al. 2008; Brockman and McFadden 2012). Recombination of mitochondrial DNA has been documented in some plants and fungi (Barr et al. 2005), but the scope of recombination across these eukaryotic groups remains poorly known. For plants, the extent of recombination and the potential for selection sweeps is likely irrelevant to a failure of an effective mt DNA barcode—the rates of nucleotide substitution in plants (with some exceptions) is far lower than in other eukaryotic taxa, leaving little opportunity for the evolution of species-specific mt genotypes (Cowan et al. 2006). A broad-scale comparison of the efficacy of mt DNA barcoding in relation to rates of recombination and nucleotide substitution of mt DNA could be very illuminating.
Rampant introgression of mt genomes, wherein the mitochondrial genotype of one species replaces the mt genotype of another species with little change to N genotypes, will also erase a barcode signal (Toews and Brelsford 2012; Hill 2019b). Such mt introgression is hypothesized to occur when (1) the fitness gain from a better adapted heterospecific mitochondrion compensate for fitness losses from mitonuclear incompatibilities, (2) escape from mutational erosion and loss of mt function compensate for loss of mitonuclear incompatibilities, or (3) when a maternally transmitted parasite like Wolbachia infects a new host species and, because it is co-transmitted with mitochondria, causes the spread the mt genotype of the original host species in the new host species (Sloan et al. 2017; Hill 2019b). The effects of endosymbionts may be particularly problematic for the persistence of a mt DNA barcode gap because endosymbionts can drag mitochondria across a species boundary and could be an explanation for why phenotypically distinct populations of animals like blowflies (Diptera: Calliphoridae) which have high rates of infection by endosymbionts often share a mitochondrial genotype (Whitworth et al. 2007). Loss of a uniquely coadapted mitonuclear genotype could be viewed as loss of species identity such that a lack of a DNA barcode gap in cases of rampant mt introgression is correctly failing to diagnose a collapsed species (Vonlanthen et al. 2012). Such an argument carries a risk of circularity, but the congruence between mt DNA barcode gaps and both conventional species boundaries (Hebert et al. 2003b; Tavares and Baker 2008) and the transitions in ornamentation used during mate choice for species recognition (Hill 2018) establishes a clear link between transitions in mitochondrial genotype and transitions between populations that taxonomists have recognized as species. The cases of rampant introgression of mt genomes then become rare exceptions that can be explained within the context of the mitonuclear compatibility species concept (Hill 2019b).