Abstract
BackgroundRecent mitochondrial phylogenomics studies have reported a sister-group relationship of the orders Capsalidea and Dactylogyridea, which is inconsistent with previous morphology- and molecular-based phylogenies. As Dactylogyridea mitochondrial genomes (mitogenomes) are currently represented by only one family, to improve the phylogenetic resolution, we sequenced and characterized two dactylogyridean parasites, Lamellodiscus spari and Lepidotrema longipenis, belonging to a non-represented family Diplectanidae.ResultsThe L. longipenis mitogenome (15,433 bp) contains the standard 36 flatworm mitochondrial genes (atp8 is absent), whereas we failed to detect trnS1, trnC and trnG in L. spari (14,614 bp). Both mitogenomes exhibit unique gene orders (among the Monogenea), with a number of tRNA rearrangements. Both long non-coding regions contain a number of different (partially overlapping) repeat sequences. Intriguingly, these include putative tRNA pseudogenes in a tandem array (17 trnV pseudogenes in L. longipenis, 13 trnY pseudogenes in L. spari). Combined nucleotide diversity, non-synonymous/synonymous substitutions ratio and average sequence identity analyses consistently showed that nad2, nad5 and nad4 were the most variable PCGs, whereas cox1, cox2 and cytb were the most conserved. Phylogenomic analysis showed that the newly sequenced species of the family Diplectanidae formed a sister-group with the Dactylogyridae + Capsalidae clade. Thus Dactylogyridea (represented by the Diplectanidae and Dactylogyridae) was rendered paraphyletic (with high statistical support) by the nested Capsalidea (represented by the Capsalidae) clade.ConclusionsOur results show that nad2, nad5 and nad4 (fast-evolving) would be better candidates than cox1 (slow-evolving) for species identification and population genetics studies in the Diplectanidae. The unique gene order pattern further suggests discontinuous evolution of mitogenomic gene order arrangement in the Class Monogenea. This first report of paraphyly of the Dactylogyridea highlights the need to generate more molecular data for monogenean parasites, in order to be able to clarify their relationships using large datasets, as single-gene markers appear to provide a phylogenetic resolution which is too low for the task.
Highlights
Recent mitochondrial phylogenomics studies have reported a sister-group relationship of the orders Capsalidea and Dactylogyridea, which is inconsistent with previous morphology- and molecular-based phylogenies
The L. longipenis mitogenome contains the standard [49] 36 flatworm mitochondrial genes, including 12 protein-encoding genes (PCGs; atp8 is absent), 22 tRNA genes, and two rRNA genes, whereas trnS1, trnC and trnG genes are missing in L. spari (Table 1 and Fig. 1)
We carefully checked all intergenic sequences. As these missing tRNA genes are located between nad5 and long non-coding regions (LNCR) in L. longipenis (Table 1, Fig. 2), and as trnC is located between two rRNA genes in many other monogeneans (Fig. 2), we focused on these two fragments
Summary
Recent mitochondrial phylogenomics studies have reported a sister-group relationship of the orders Capsalidea and Dactylogyridea, which is inconsistent with previous morphology- and molecular-based phylogenies. Used phylogenetic markers, morphology and single-genes, are often not suitable for resolving evolutionary history with high confidence; morphological traits can be homoplastic, which often causes taxonomic and phylogenetic artifacts [4,5,6] and, due to the small amount of information (phylogenetic signal) they carry, single-gene molecular markers may have limited resolving power [7]. This is reflected in the unresolved phylogeny of Monogenean parasites [8,9,10,11]. Recent researches [4, 19, 20] relying on the mitochondrial (mt) phylogenomics approach consistently resolved the Dactylogyridea and Capsalidea as sister-groups, thereby further complicating phylogenetic hypotheses for the three aforementioned orders
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