DNA Barcoding Will Often Fail to Discover New Animal Species over Broad Parameter Space

Abstract

With increasing force, genetic divergence of mitochondrial DNA (mtDNA) is being argued as the primary tool for discovery of animal species. Two thresholds of single-gene divergence have been proposed: reciprocal monophyly, and 10 times greater genetic divergence between than within species (the "10x rule"). To explore quantitatively the utility of each approach, we couple neutral coalescent theory and the classical Bateson-Dobzhansky-Muller (BDM) model of speciation. The joint stochastic dynamics of these two processes demonstrate that both thresholds fail to "discover" many reproductively isolated lineages under a single incompatibility BDM model, especially when BDM loci have been subject to divergent selection. Only when populations have been isolated for > 4 million generations did these thresholds achieve error rates of < 10% under our model that incorporates variable population sizes. The high error rate evident in simulations is corroborated with six empirical data sets. These properties suggest that single-gene, high-throughput approaches to discovering new animal species will bias large-scale biodiversity surveys, particularly toward missing reproductively isolated lineages that have emerged by divergent selection or other mechanisms that accelerate reproductive isolation. Because single-gene thresholds for species discovery can result in substantial error at recent divergence times, they will misrepresent the correspondence between recently isolated populations and reproductively isolated lineages (= species).

Mitonuclear coevolution as the genesis of speciation and the mitochondrial DNA barcode gap

“…2003; Moritz and Cicero 2004; Hickerson et al. 2006). Within the context of DNA barcodes, there is some discussion that the reason that COX1 is so conserved is that it plays a vital role in cellular respiration and hence is subject to strong stabilizing selection (Stoeckle and Thaler 2014) and that it is coadapted with the nuclear genes with which it interacts (Hebert et al.…”

“…2005; Hickerson et al. 2006). Some of the reservations by taxonomists about the application of DNA barcoding arise from concern that automating taxonomy will remove the need for taxonomists and undercut support and funding for museum scientists (Will et al.…”

Assessing species boundaries and the phylogenetic position of the rare Szechwan ratsnake, Euprepiophis perlaceus (Serpentes: Colubridae), using coalescent-based methods

“…Nevertheless, methods based on criteria such as genetic distance or reciprocal monophyly to identify species boundaries are also subjective (Hey, 2009) and fail to account for incomplete lineage sorting, introgression and gene duplication causing gene-tree incongruence with the species tree. Genetic barcoding may also fail to assign individuals into the corresponding species (Edwards, 2009;Hickerson et al, 2006;O'Meara, 2010).…”

Phylogeny and DNA barcoding of inquiline oak gallwasps (Hymenoptera: Cynipidae) of the Western Palaearctic

“…% sequence divergence) to define taxa, but attempts to identify idependently evolving lineages. Because the topology of an individual gene tree can differ significantly from population and species trees, identification of such lineages is best approached using data for multiple loci (Meyer & Paulay 2005;Hickerson et al 2006;Vogler & Monaghan 2006). A second approach captures the sequence diversity present in a group of 105 samples by identifying molecular operational taxonomic units (or MOTUs; Floyd et al, 2002), defined as a group of sequences differing from one another by a specified maximum number of base pairs (Blaxter 2004).…”

“…Coalescent theory predicts that both intraspecific sequence diversity and the probability of shared barcode sequences among discrete biological species will be 130 sensitive to population demography, particularly species age and past effective population size (Moritz & Cicero 2004;Meyer & Paulay 2005;Hickerson et al 2006;Nielsen & Matz 2006;Knowles & Carstens 2007). Young species with large effective population sizes are predicted not to be monophyletic for their barcode sequence, and where past population sizes vary substantially within a group of taxa, a single threshold divergence is unlikely to separate 135 6 intraspecific variation from varation among species -in other words, there may be no barcoding gap (Funk & Omland 2003;DeSalle et al, 2005;Meyer & Paulay, 2005;Cognato 2006; Vogler & Monaghan, 2006;Rubinoff, 2006).…”