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Open AccessArticle

Evidence for Adaptive Selection in the Mitogenome of a Mesoparasitic Monogenean Flatworm Enterogyrus malmbergi

by Dong Zhang 1,2,3, Hong Zou 1,2, Shan G. Wu 1,2,3, Ming Li 1,2,3, Ivan Jakovlić 4, Jin Zhang 4, Rong Chen 4, Wen X. Li 1,2,3,* and Gui T. Wang 1,2,3
1
State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China
2
Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China
3
University of Chinese Academy of Sciences, Beijing 100000, China
4
Bio-Transduction Lab, Wuhan 430075, China
*
Author to whom correspondence should be addressed.
Genes 2019, 10(11), 863; https://doi.org/10.3390/genes10110863
Received: 19 September 2019 / Revised: 26 October 2019 / Accepted: 29 October 2019 / Published: 30 October 2019
(This article belongs to the Section Microbial Genetics and Genomics)
Whereas a majority of monogenean flatworms are ectoparasitic, i.e., parasitize on external surfaces (mainly gills) of their fish hosts, Enterogyrus species (subfamily Ancyrocephalinae) are mesoparasitic, i.e., parasitize in the stomach of the host. As there are numerous drastic differences between these two environments (including lower oxygen availability), we hypothesized that this life-history innovation might have produced adaptive pressures on the energy metabolism, which is partially encoded by the mitochondrial genome (OXPHOS). To test this hypothesis, we sequenced mitochondrial genomes of two Ancyrocephalinae species: mesoparasitic E. malmbergi and ectoparasitic Ancyrocephalus mogurndae. The mitogenomic architecture of E. malmbergi is mostly standard for monogeneans, but that of A. mogurndae exhibits some unique features: missing trnL2 gene, very low AT content (60%), a non-canonical start codon of the nad2 gene, and exceptionally long tandem-repeats in the non-coding region (253 bp). Phylogenetic analyses produced paraphyletic Ancyrocephalinae (with embedded Dactylogyrinae), but with low support values. Selective pressure (PAML and HYPHY) and protein structure analyses all found evidence for adaptive evolution in cox2 and cox3 genes of the mesoparasitic E. malmbergi. These findings tentatively support our hypothesis of adaptive evolution driven by life-history innovations in the mitogenome of this species. However, as only one stomach-inhabiting mesoparasitic monogenean was available for this analysis, our findings should be corroborated on a larger number of mesoparasitic monogeneans and by physiological studies. View Full-Text
Keywords: Ancyrocephalus mogurndae; positive selection; Monogenea; Dactylogyridae; flatworms; replication initiation; mtDNA Ancyrocephalus mogurndae; positive selection; Monogenea; Dactylogyridae; flatworms; replication initiation; mtDNA
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Zhang, D.; Zou, H.; Wu, S.G.; Li, M.; Jakovlić, I.; Zhang, J.; Chen, R.; Li, W.X.; Wang, G.T. Evidence for Adaptive Selection in the Mitogenome of a Mesoparasitic Monogenean Flatworm Enterogyrus malmbergi. Genes 2019, 10, 863.

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