Cargando…

The complete mitochondrial genomes of Paradiplozoon yarkandense and Paradiplozoon homoion confirm that Diplozoidae evolve at an elevated rate

BACKGROUND: Diplozoidae are monogenean (Monogenea: Polyopisthocotylea) fish parasites characterised by a unique life history: two larvae permanently fuse into an X-shaped “Siamese” organism. Taxonomy and phylogeny of Diplozoidae and Polyopisthocotylea remain unresolved due to the unavailability of m...

Descripción completa

Detalles Bibliográficos
Autores principales: Hao, Cui-Lan, Arken, Kadirden, Kadir, Munira, Zhang, Wen-Run, Rong, Meng-Jie, Wei, Nian-Wen, Liu, Yan-Jun, Yue, Cheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9044634/
https://www.ncbi.nlm.nih.gov/pubmed/35477556
http://dx.doi.org/10.1186/s13071-022-05275-x
_version_ 1784695147494113280
author Hao, Cui-Lan
Arken, Kadirden
Kadir, Munira
Zhang, Wen-Run
Rong, Meng-Jie
Wei, Nian-Wen
Liu, Yan-Jun
Yue, Cheng
author_facet Hao, Cui-Lan
Arken, Kadirden
Kadir, Munira
Zhang, Wen-Run
Rong, Meng-Jie
Wei, Nian-Wen
Liu, Yan-Jun
Yue, Cheng
author_sort Hao, Cui-Lan
collection PubMed
description BACKGROUND: Diplozoidae are monogenean (Monogenea: Polyopisthocotylea) fish parasites characterised by a unique life history: two larvae permanently fuse into an X-shaped “Siamese” organism. Taxonomy and phylogeny of Diplozoidae and Polyopisthocotylea remain unresolved due to the unavailability of molecular markers with sufficiently high resolution. Mitogenomes may be a suitable candidate, but there are currently only 12 available for the Polyopisthocotylea (three for Diplozoidae). The only available study of diplozoid mitogenomes found unique base composition patterns and elevated evolution rates in comparison with other Monogenean mitogenomes. METHODS: To further explore their evolution and generate molecular data for evolutionary studies, we sequenced the complete mitogenomes of two Diplozoidae species, Paradiplozoon homoion and Paradiplozoon yarkandense, and conducted a number of comparative mitogenomic analyses with other polyopisthocotyleans. RESULTS: We found further evidence that mitogenomes of Diplozoidae evolve at a unique, elevated rate, which was reflected in their exceptionally long branches, large sizes, unique base composition, skews, and very low gene sequence similarity levels between the two newly sequenced species. They also exhibited remarkably large overlaps between some genes. Phylogenetic analysis of Polyopisthocotylea resolved all major taxa as monophyletic, and Mazocraeidea was split into two major clades: (Diplozoidae) + (all four remaining families: Diclidophoridae, Chauhaneidae, Mazocraeidae and Microcotylidae). It also provided further confirmation that the genus Paradiplozoon is paraphyletic and requires a taxonomic revision, so the two species may have to be renamed Indodiplozoon homoion and Diplozoon yarkandense comb. nov. CONCLUSIONS: Although our findings indicate that mitogenomes may be a promising tool for resolving the phylogeny of Polyopisthocotylea, elevated evolutionary rates of Diplozoidae may cause phylogenetic artefacts, so future studies should pay caution to this problem. Furthermore, as the reason for their elevated evolution remains unknown, Diplozoidae are a remarkably interesting lineage for other types of evolutionary mitogenomic studies. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05275-x.
format Online
Article
Text
id pubmed-9044634
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-90446342022-04-28 The complete mitochondrial genomes of Paradiplozoon yarkandense and Paradiplozoon homoion confirm that Diplozoidae evolve at an elevated rate Hao, Cui-Lan Arken, Kadirden Kadir, Munira Zhang, Wen-Run Rong, Meng-Jie Wei, Nian-Wen Liu, Yan-Jun Yue, Cheng Parasit Vectors Research BACKGROUND: Diplozoidae are monogenean (Monogenea: Polyopisthocotylea) fish parasites characterised by a unique life history: two larvae permanently fuse into an X-shaped “Siamese” organism. Taxonomy and phylogeny of Diplozoidae and Polyopisthocotylea remain unresolved due to the unavailability of molecular markers with sufficiently high resolution. Mitogenomes may be a suitable candidate, but there are currently only 12 available for the Polyopisthocotylea (three for Diplozoidae). The only available study of diplozoid mitogenomes found unique base composition patterns and elevated evolution rates in comparison with other Monogenean mitogenomes. METHODS: To further explore their evolution and generate molecular data for evolutionary studies, we sequenced the complete mitogenomes of two Diplozoidae species, Paradiplozoon homoion and Paradiplozoon yarkandense, and conducted a number of comparative mitogenomic analyses with other polyopisthocotyleans. RESULTS: We found further evidence that mitogenomes of Diplozoidae evolve at a unique, elevated rate, which was reflected in their exceptionally long branches, large sizes, unique base composition, skews, and very low gene sequence similarity levels between the two newly sequenced species. They also exhibited remarkably large overlaps between some genes. Phylogenetic analysis of Polyopisthocotylea resolved all major taxa as monophyletic, and Mazocraeidea was split into two major clades: (Diplozoidae) + (all four remaining families: Diclidophoridae, Chauhaneidae, Mazocraeidae and Microcotylidae). It also provided further confirmation that the genus Paradiplozoon is paraphyletic and requires a taxonomic revision, so the two species may have to be renamed Indodiplozoon homoion and Diplozoon yarkandense comb. nov. CONCLUSIONS: Although our findings indicate that mitogenomes may be a promising tool for resolving the phylogeny of Polyopisthocotylea, elevated evolutionary rates of Diplozoidae may cause phylogenetic artefacts, so future studies should pay caution to this problem. Furthermore, as the reason for their elevated evolution remains unknown, Diplozoidae are a remarkably interesting lineage for other types of evolutionary mitogenomic studies. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-022-05275-x. BioMed Central 2022-04-27 /pmc/articles/PMC9044634/ /pubmed/35477556 http://dx.doi.org/10.1186/s13071-022-05275-x Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Hao, Cui-Lan
Arken, Kadirden
Kadir, Munira
Zhang, Wen-Run
Rong, Meng-Jie
Wei, Nian-Wen
Liu, Yan-Jun
Yue, Cheng
The complete mitochondrial genomes of Paradiplozoon yarkandense and Paradiplozoon homoion confirm that Diplozoidae evolve at an elevated rate
title The complete mitochondrial genomes of Paradiplozoon yarkandense and Paradiplozoon homoion confirm that Diplozoidae evolve at an elevated rate
title_full The complete mitochondrial genomes of Paradiplozoon yarkandense and Paradiplozoon homoion confirm that Diplozoidae evolve at an elevated rate
title_fullStr The complete mitochondrial genomes of Paradiplozoon yarkandense and Paradiplozoon homoion confirm that Diplozoidae evolve at an elevated rate
title_full_unstemmed The complete mitochondrial genomes of Paradiplozoon yarkandense and Paradiplozoon homoion confirm that Diplozoidae evolve at an elevated rate
title_short The complete mitochondrial genomes of Paradiplozoon yarkandense and Paradiplozoon homoion confirm that Diplozoidae evolve at an elevated rate
title_sort complete mitochondrial genomes of paradiplozoon yarkandense and paradiplozoon homoion confirm that diplozoidae evolve at an elevated rate
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9044634/
https://www.ncbi.nlm.nih.gov/pubmed/35477556
http://dx.doi.org/10.1186/s13071-022-05275-x
work_keys_str_mv AT haocuilan thecompletemitochondrialgenomesofparadiplozoonyarkandenseandparadiplozoonhomoionconfirmthatdiplozoidaeevolveatanelevatedrate
AT arkenkadirden thecompletemitochondrialgenomesofparadiplozoonyarkandenseandparadiplozoonhomoionconfirmthatdiplozoidaeevolveatanelevatedrate
AT kadirmunira thecompletemitochondrialgenomesofparadiplozoonyarkandenseandparadiplozoonhomoionconfirmthatdiplozoidaeevolveatanelevatedrate
AT zhangwenrun thecompletemitochondrialgenomesofparadiplozoonyarkandenseandparadiplozoonhomoionconfirmthatdiplozoidaeevolveatanelevatedrate
AT rongmengjie thecompletemitochondrialgenomesofparadiplozoonyarkandenseandparadiplozoonhomoionconfirmthatdiplozoidaeevolveatanelevatedrate
AT weinianwen thecompletemitochondrialgenomesofparadiplozoonyarkandenseandparadiplozoonhomoionconfirmthatdiplozoidaeevolveatanelevatedrate
AT liuyanjun thecompletemitochondrialgenomesofparadiplozoonyarkandenseandparadiplozoonhomoionconfirmthatdiplozoidaeevolveatanelevatedrate
AT yuecheng thecompletemitochondrialgenomesofparadiplozoonyarkandenseandparadiplozoonhomoionconfirmthatdiplozoidaeevolveatanelevatedrate
AT haocuilan completemitochondrialgenomesofparadiplozoonyarkandenseandparadiplozoonhomoionconfirmthatdiplozoidaeevolveatanelevatedrate
AT arkenkadirden completemitochondrialgenomesofparadiplozoonyarkandenseandparadiplozoonhomoionconfirmthatdiplozoidaeevolveatanelevatedrate
AT kadirmunira completemitochondrialgenomesofparadiplozoonyarkandenseandparadiplozoonhomoionconfirmthatdiplozoidaeevolveatanelevatedrate
AT zhangwenrun completemitochondrialgenomesofparadiplozoonyarkandenseandparadiplozoonhomoionconfirmthatdiplozoidaeevolveatanelevatedrate
AT rongmengjie completemitochondrialgenomesofparadiplozoonyarkandenseandparadiplozoonhomoionconfirmthatdiplozoidaeevolveatanelevatedrate
AT weinianwen completemitochondrialgenomesofparadiplozoonyarkandenseandparadiplozoonhomoionconfirmthatdiplozoidaeevolveatanelevatedrate
AT liuyanjun completemitochondrialgenomesofparadiplozoonyarkandenseandparadiplozoonhomoionconfirmthatdiplozoidaeevolveatanelevatedrate
AT yuecheng completemitochondrialgenomesofparadiplozoonyarkandenseandparadiplozoonhomoionconfirmthatdiplozoidaeevolveatanelevatedrate