Phylomitogenomic Analyses Provided Further Evidence for the Resurrection of the Family Pseudoacanthocephalidae (Acanthocephala: Echinorhynchida)

SIMPLE SUMMARY: Acanthocephalans, commonly known as spiny-headed or thorny-headed worms, are a small group of endoparasites with veterinary, medical and economic importance due to their ability to cause disease in domestic animals, wildlife, and humans. In recent decades, great progress has been made using mitochondrial genome data to clarify the phylogenetic relationships of acanthocephalans. However, the current mitochondrial genome database for acanthocephalans remains very limited. Herein, the characterization of the mitochondrial genome of Pseudoacanthocephalus bufonis (Shipley, 1903), the first representative of the family Pseudoacanthocephalidae, is reported. Phylogenetic analyses using the amino acid sequences of 12 protein-coding genes supported the validity of the family Pseudoacanthocephalidae and suggested a close affinity between Pseudoacanthocephalidae and Cavisomatidae. Our phylogenetic results also showed that the families Polymorphidae and Centrorhynchidae have a closer relationship than Plagiorhynchidae in the Polymorphida. These findings contribute to revealing the patterns of mitogenomic evolution in this group and represent a substantial step towards reconstructing the classification of the phylum Acanthocephala. ABSTRACT: The phylum Acanthocephala is an important monophyletic group of parasites, with adults parasitic in the digestive tracts of all major vertebrate groups. Acanthocephalans are of veterinary, medical, and economic importance due to their ability to cause disease in domestic animals, wildlife, and humans. However, the current genetic data for acanthocephalans are sparse, both in terms of the proportion of taxa surveyed and the number of genes sequenced. Consequently, the basic molecular phylogenetic framework for the phylum is still incomplete. In the present study, we reported the first complete mitochondrial genome from a representative of the family Pseudoacanthocephalidae Petrochenko, 1956. The mitogenome of Pseudoacanthocephalus bufonis (Shipley, 1903) is 14,056 bp in length, contains 36 genes (12 protein-coding genes (PCGs) (lacking atp8), 22 tRNA genes, and 2 rRNA genes (rrnL and rrnS)) and two non-coding regions (NCR1 and NCR2), and displayed the highest GC-skew in the order Echinorhynchida. Phylogenetic results of maximum likelihood (ML) and Bayesian inference (BI) using the amino acid sequences of 12 protein-coding genes in different models provided further evidence for the resurrection of the family Pseudoacanthocephalidae and also supported that the order Echinorhynchida is paraphyletic. A monophyletic clade comprising P. bufonis and Cavisoma magnum suggests a close affinity between Pseudoacanthocephalidae and Cavisomatidae. Our phylogenetic analyses also showed that Polymorphidae has a closer relationship with Centrorhynchidae than Plagiorhynchidae in the monophyletic order Polymorphida.