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Arthropod mtDNA paraphyly: a case study of introgressive origin

Noguerales, Víctor1; Emerson, Brent C.1

Published Nov 25, 2024 on Dryad. https://doi.org/10.5061/dryad.866t1g219

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Nov 25, 2024 version files 13.30 MB

Abstract

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 hybridisation playing only a minor role. However, in the absence of 
comparable nuclear genetic data, the relative roles of ILS and hybridisation in explaining 
mitochondrial DNA (mtDNA) paraphyly remain unclear. Hybridisation itself is a multifaceted 
gateway to 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 hybridisation, 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 
hybridisation, revealing strong nuclear genetic differentiation between species, but with the 
complete replacement of Tarphius simplex mtDNA through the introgression of at least five 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.