Exploring Evolutionary Relationships within Neodermata Using Putative Orthologous Groups of Proteins, with Emphasis on Peptidases

Abstract

The phylogenetic relationships within Neodermata were examined based on putative orthologous groups of proteins (OGPs) from 11 species of Monogenea, Trematoda, and Cestoda. The dataset included OGPs from BUSCO and OMA. Additionally, peptidases were identified and evaluated as phylogenetic markers. Phylogenies were inferred using the maximum likelihood method. A network analysis and a hierarchical grouping analysis of the principal components (HCPC) of orthologous groups of peptidases were performed. The phylogenetic analyses showed the monopisthocotylean monogeneans as the sister-group of cestodes, and the polyopisthocotylean monogeneans as the sister-group of trematodes. However, the sister-group relationship between Monopisthocotylea and Cestoda was not statistically well supported. The network analysis and HCPC also showed a cluster formed by polyopisthocotyleans and trematodes. The present study supports the non-monophyly of Monogenea. An analysis of mutation rates indicated that secreted peptidases and inhibitors, and those with multiple copies, are under positive selection pressure, which could explain the expansion of some families such as C01, C19, I02, and S01. Whilst not definitive, our study presents another point of view in the discussion of the evolution of Neodermata, and we hope that our data drive further discussion and debate on this intriguing topic.

An insight into the functional genomics and species classification of Eudiplozoon nipponicum (Monogenea, Diplozoidae), a haematophagous parasite of the common carp Cyprinus carpio

“…In line with the latest phylogenetic analysis confirming a closer relationship of the monogenean subclass Polyopisthocotylea to trematodes than to cestodes [ 18 ], we observed that most E. nipponicum proteins are homologues (based on annotation in the UniProt/UniRef100 protein database) to monogenean representative Protopolystoma xenopodis ( n = 2,360), followed by trematodes, such as Paragonimus westermani ( n = 608), Schistosoma japonicum ( n = 462), Echinostoma caproni ( n = 429), and cestode Schistocephalus solidus ( n = 410) (Table 5 ).…”

“…They perform essential functions in a broad range of physiological processes, such as protein metabolism, feeding, anticoagulation, digestion, regulation of development, immune evasion, and reproduction, and they have been intensively studied and repeatedly reviewed [ 74 – 77 ]. Moreover, peptidases can be used to reveal both micro- and macroevolutionary changes during the evolution of parasites [ 18 , 66 ]. Majority of identified individual peptidases ( n = 54) belong to peptidases with serine catalytic type, specifically to the S1 family (chymotrypsin family, PA clan) and S1A subfamily (chymotrypsin A).…”

“…Infestation by monogeneans can cause in the fish hosts serious and often lethal diseases, leading to significant economic losses in commercial fish-breeding stocks, especially those with a high stocking density [ 13 , 14 ]. As demonstrated by a number of studies [ 15 – 18 ], the Monogenea class is, in terms of its molecular, structural, and functional characteristics, probably the most diverse group within the obligate parasitic superclass Neodermata, and a better understanding of monogeneans is key to deciphering the evolution of parasitism in flatworms. Monogeneans tend to be studied in terms of phylogenetics [ 19 , 20 ] and population characteristics [ 21 – 23 ].…”

An inside out journey: biogenesis, ultrastructure and proteomic characterisation of the ectoparasitic flatworm Sparicotyle chrysophrii extracellular vesicles

“…and Schistosoma spp. because of the phylogenetic proximity among Trematoda, Cestoda and Polyopisthocotyla [ 1 , 2 ] and considering their genomic quality based on individual genome assembly statistics. The same steps and criteria as described above were employed to interrogate S. chrysophrii datasets for these neodermate homologues.…”

“…Monogeneans, recently reclassified into two unrelated classes, Monopisthocotyla and Polyopisthocotyla [ 1 , 2 ], are important aquatic, mainly ectoparasitic neodermates whose presence in fish farms pose a significant bottleneck for fish health, welfare, performance and economic revenue due to the artificial environment in which livestock is set [ 3 ].…”