The mitochondrial genome sequence of Cyrnea seurati revealed the phylogenetic relationship in Spiruromorpha and its implications for evolution

Abstract

The infraorder Spiruromorpha comprises diverse parasitic nematodes of veterinary and medical importance, many of which utilize arthropods as intermediate hosts/vectors. However, phylogenetic relationships and evolutionary history within this group remain poorly resolved due to limitations of single-gene markers and the scarcity of fossil records. Complete mitochondrial genomes offer robust alternatives for resolving deep evolutionary radiations and understanding adaptive processes relevant to parasite–vector–host interactions. We assembled and characterized the first complete mitochondrial genome of  Cyrnea seurati  (Habronematoidea) from a Eurasian hobby ( Falco subbuteo ) in China. The 13,761 bp circular genome contains 12 protein-coding genes (PCGs), 22 tRNAs, and 2 rRNAs, with gene arrangement conserved within Habronematoidea but featuring unique initiation codons (GTT for nad4 and TTT for  cytb ). Comparative analysis revealed high genetic divergence from other Habronematoidea species (20.5–37.4% in nucleotide sequences), confirming its distinct generic status. Phylogenomic analyses of 54 Spiruromorpha mitogenomes resolved two major clades and widespread paraphyly among superfamilies, with mitochondrial data providing greater resolution than 18S rRNA. Divergence time estimation, calibrated using published fossil records, traced the most recent common ancestor of Spiruromorpha to the Devonian (~ 366.77 Mya), with major radiations coinciding with the Jurassic–Cretaceous transition—a period marked by diversification of insect vectors and vertebrate hosts. Positive selection was detected in nine PCGs, notably in OXPHOS genes ( cox2 ,  cytb ,  nad1 ,  nad6 ), suggesting adaptive evolution to diverse host environments and metabolic demands. Codon usage analysis revealed strong AT-biased preferences and species-specific adaptive patterns linked to host origins. This study provides the first mitogenomic resource for the genus  Cyrnea , significantly advancing the molecular dataset for Spiruromorpha. Our phylogenomic framework resolves long-standing uncertainties in spiruromorph relationships and highlights the potential of mitochondrial markers for tracing parasite–vector coevolutionary dynamics. The detected positive selection signals implicate mitochondrial adaptation in the ecological diversification of these parasites, with implications for understanding nematode parasitism, pathogen control, and the evolutionary interplay between parasites, vectors, and hosts.