Arthropod mtDNA paraphyly: a case study of introgressive origin

Mitochondrial paraphyly between arthropod species is not uncommon and has been speculated to largely be the result of incomplete lineage sorting (ILS) of ancestral variation within the common ancestor of both species, with hybridization playing only a minor role. However, in the absence of comparable nuclear genetic data, the relative roles of ILS and hybridization in explaining mitochondrial DNA (mtDNA) paraphyly remain unclear. Hybridization itself is a multifaceted gateway to mtDNA paraphyly, which may lead to paraphyly across both the nuclear and mitochondrial genomes, or paraphyly that is largely restricted to the mitochondrial genome. These different outcomes will depend upon the frequency of hybridization, its demographic context, and the extent to which mtDNA is subject to direct selection, indirect selection, or neutral processes. Here, we describe extensive mtDNA paraphyly between two species of iron-clad beetle (Zopheridae) and evaluate competing explanations for its origin. We first test between hypotheses of ILS and hybridization, revealing strong nuclear genetic differentiation between species, but with the complete replacement of Tarphius simplex mtDNA through the introgression of at least 5 mtDNA haplotypes from T. canariensis. We then contrast explanations of direct selection, indirect selection, or genetic drift for observed patterns of mtDNA introgression. Our results highlight how introgression can lead to complex patterns of mtDNA paraphyly across arthropod species, while simultaneously revealing the challenges for understanding the selective or neutral drivers that underpin such patterns.