Three new Diplozoidae mitogenomes expose unusual compositional biases within the Monogenea class: implications for phylogenetic studies

Abstract

BackgroundAs the topologies produced by previous molecular and morphological studies were contradictory and unstable (polytomy), evolutionary relationships within the Diplozoidae family and the Monogenea class (controversial relationships among the Discocotylinea, Microcotylinea and Gastrocotylinea suborders) remain unresolved. Complete mitogenomes carry a relatively large amount of information, sufficient to provide a much higher phylogenetic resolution than traditionally used morphological traits and/or single molecular markers. However, their implementation is hampered by the scarcity of available monogenean mitogenomes. Therefore, we sequenced and characterized mitogenomes belonging to three Diplozoidae family species, and conducted comparative genomic and phylogenomic analyses for the entire Monogenea class.ResultsTaxonomic identification was inconclusive, so two of the species were identified merely to the genus level. The complete mitogenomes of Sindiplozoon sp. and Eudiplozoon sp. are 14,334 bp and 15,239 bp in size, respectively. Paradiplozoon opsariichthydis (15,385 bp) is incomplete: an approximately 2000 bp-long gap within a non-coding region could not be sequenced. Each genome contains the standard 36 genes (atp8 is missing). G + T content and the degree of GC- and AT-skews of these three mitogenome (and their individual elements) were higher than in other monogeneans. nad2, atp6 and nad6 were the most variable PCGs, whereas cox1, nad1 and cytb were the most conserved. Mitochondrial phylogenomics analysis, conducted using concatenated amino acid sequences of all PCGs, indicates that evolutionary relationships of the three genera are: (Eudiplozoon, (Paradiplozoon, Sindiplozoon)); and of the three suborders: (Discocotylinea, (Microcotylinea, Gastrocotylinea)). These intergeneric relationships were also supported by the skewness and principal component analyses.ConclusionsOur results show that nad2, atp6 and nad6 (fast-evolving) would be better candidates than cox1 (slow-evolving) for species identification and population genetics studies in Diplozoidae. Nucleotide bias and codon and amino acid usage patterns of the three diplozoid mitogenomes are more similar to cestodes and trematodes than to other monogenean flatworms. This unusual mutational bias was reflected in disproportionately long branches in the phylogram. Our study offsets the scarcity of molecular data for the subclass Polyopisthocotylea to some extent, and might provide important new insights into the evolutionary history of the three genera and three suborders.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1249-3) contains supplementary material, which is available to authorized users.

Molecular phylogenetics and mitogenomics of three avian dicrocoeliids (Digenea: Dicrocoeliidae) and comparison with mammalian dicrocoeliids

“…where anticodon TCT was found for trnS1 and TTT for trnK. This modification of anticodons, supposedly a homoplasy [50], from GCT to TCT (in trnS1) and CTT to TTT (in trnK) was also found in some other flatworms, e.g. Hypoderaeum conoideum (Trematoda: Echinostomatidae) [52] and Khawia sinensis (Cestoda: Caryophyllidea) [53].…”

“…Thus, our analyses showed the comparatively fast mutation rate of atp6, nad5, nad3 and nad2 while cox1, cytb and nad1 are evolving comparatively slowly in the Dicrocoeliidae. Although cox1, cytb, nad1 and two mt [50,54].…”

“…The start codon TTG for the PCGs was observed in the mitogenomes of many other flatworms, for example the nad1, cytb, nad2 and cox1 of Sindiplozoon sp. [50], the nad5 of Fasciola sp. [51] and cytb and nad5 of D. chinensis and D. dendriticum [19].…”

Review on the molecular study of the Diplozoidae: analyses of currently available genetic data, what it tells us, and where to go from here

“…As most of the abovementioned sequence data were for a single species, little can be deduced regarding the barcoding potential of the relative regions. Zhang et al [ 28 ] analysed the mitogenomes of three distinct diplozoids and constructed phylogenies based on all available mitogenomic data for Platyhelminthes, 21 species in total. In contrast to previous studies, diplozoid (Discocotylinea) taxa grouped sister to species of the Chauhaneidae (Gastrocotylinea) and Microcotylidae (Microcotylinea) in all cases, indicating that mitogenomic analyses might provide more insightful results for interrelationships of monogenean suborders [ 28 ].…”

The mitochondrial genomes of Panorpidae: sequence, structure and phylogenetic analysis

“…Although fragment of 648 bp of the gene cox1 is often considered as a universal barcode for species identification in animals [50], it is the least variable gene in Panorpidae and has a relatively lower ratio of Ka/Ks among the PCGs in these 19 mitogenomes. Given the resolution power of cox1 is proved to be sufficiently low, other genes that have fast evolutionary rates and higher ratio of Ka/Ks and are of sufficiently large size should be proposed as potential barcode candidates [39,51,52]. Based on our present study, nad2 and nad6 may be chosen as potential DNA markers for future population genetics and species delimitation studies in Panorpidae.…”