Introduction
Bilaterian animals carry mitochondrial (mt) genotypes that typically show little variation among individuals within a species but with substantial variation between species (Dasmahapatra and Mallet 2006; Lane 2009b; Bucklin et al. 2011; Zahiri et al. 2014). There is some debate regarding how reliably mt DNA genotype diagnoses species, particularly closely related species (Dupuis et al. 2012; Ratnasingham and Hebert 2013), but for birds (Tavares and Baker 2008), mammals (Clare et al. 2007), turtles (Naro‐Maciel et al. 2010), boney fish (Ward and Holmes 2007), amphibians (Vences et al. 2005), spiders (Coddington et al. 2016), butterflies (Janzen et al. 2009), ants (Smith et al. 2005), parasitoid wasps (Smith et al. 2008), mayflies, stoneflies, and caddisflies (Morinière et al. 2017), among other bilaterian taxa, mt genotypes change abruptly at the great majority of species boundaries. This pattern of differentiation in mt genes among species has led to the use of mt nucleotide sequences as a diagnostic tool in species identification, the so called “DNA barcode”(Hebert et al. 2003a). The substantial divergence in mt DNA sequence observed between most sister pairs of animal taxa is termed the “barcode gap” (Hebert et al. 2003a).
Three mechanisms have been proposed to explain this pattern of diversity of mt genotypes: (1) variations in mt DNA nucleotide sequences are neutral and are fixed via drift in isolated populations (Moritz et al. 1987; Hickerson et al. 2006; Lynch et al. 2006; Zink and Barrowclough 2008; Smith 2016), (2) there have been repeated episodes of extreme population bottlenecks involving the majority of bilaterian taxa (Stoeckle and Thaler 2014) or (3) directional selection on mitochondrial genotypes leads to rapid divergence when gene flow between populations is disrupted (Gershoni et al. 2009; Chou and Leu 2010; Hill 2016; James et al. 2016). In this essay, I focus on the necessity of coadaptation with the nuclear (N) genome throughout the evolution of the mt genome as a foundation for explaining the population structure of mt genomes. I propose that, far from being an unexpected or inexplicable pattern, the tight congruence between mt genotype and species boundaries may be an inevitable consequence of the need for mt and N gene products to cofunction to enable aerobic respiration, especially when the mt chromosome does not engage in recombination. In reviewing previous efforts to explain DNA barcode gaps, I consider the nearly exclusive focus on amino acid substitutions and the protein-coding genes of the mt genome as potential targets of selection, which has discounted the potential key role played by selection on genes coding for tRNA and rRNA as well as selection on origin of replication regions of mt DNA (Ruiz‐Pesini and Wallace 2006; Ellison and Burton 2008a; Barreto and Burton 2013; Adrion et al. 2016; Barreto et al. 2018). I also consider a potential pivotal role played by recombination of mitochondrial chromosomes in the generation of mt DNA barcode gaps. I propose that a better understanding of the evolutionary mechanism that generates the genetic structure of mt DNA across eukaryotes is critical not only with regards to assessing the value of DNA barcodes as a tool in taxonomy (Rubinoff et al. 2006; Baker et al. 2009) but also for a better understanding of the process of speciation (Hill 2016; Sunnucks et al. 2017; Tobler et al. 2019).