Molecular phylogeny of the Cyathocotylidae (Digenea, Diplostomoidea) necessitates systematic changes and reveals a history of host and environment switches

Abstract

The Cyathocotylidae is a globally distributed family of digeneans parasitic as adults in fish, reptiles, birds and mammals in both freshwater and marine environments. Molecular phylogenetic analysis of interrelationships among cyathocotylids is lacking with only a few species included in previous studies. We used sequences of the nuclear 28S rRNA gene to examine phylogenetic affinities of 11 newly sequenced taxa of cyathocotylids and the closely related family Brauninidae collected from fish, reptiles, birds and dolphins from Australia, Southeast Asia, Europe, North America and South America. This is the first study to provide sequence data from adult cyathocotylids parasitic in fish and reptiles. Our analyses demonstrated that the members of the genus Braunina (family Brauninidae) belong to the Cyathocotylidae, placing the Brauninidae into synonymy with the Cyathocotylidae. In addition, our DNA sequences supported the presence of a second species in the currently monotypic Braunina. Our phylogeny revealed that Cyathocotyle spp. from crocodilians belong to a separate genus (Suchocyathocotyle, previously proposed as a subgenus) and subfamily (Suchocyathocotylinae subfam. n.). Morphological study of Gogatea serpentum indicum supported its elevation to species as Gogatea mehri. The phylogeny did not support Holostephanoides within the subfamily Cyathocotylinae; instead, Holostephanoides formed a strongly supported clade with members of the subfamily Szidatiinae (Gogatea and Neogogatea). Therefore, we transfer Holostephanoides into the Szidatiinae. DNA sequence data revealed the potential presence of cryptic species reported under the name Mesostephanus microbursa. Our phylogeny indicated at least two major host switching events in the evolutionary history of the subfamily Szidatiinae which likely resulted in the transition of these parasites from birds to fish and snakes. Likewise, the transition to dolphins by Braunina represents another major host switching event among the Cyathocotylidae. In addition, our phylogeny revealed more than a single transition between freshwater and marine environments demonstrated in our dataset by Braunina and some Mesostephanus.

Phylogeny and systematics of the Proterodiplostomidae Dubois, 1936 (Digenea: Diplostomoidea) reflect the complex evolutionary history of the ancient digenean group

“…Similar to other recent molecular phylogenies of the Diplostomoidea, the currently accepted Diplostomidae and Strigeidae were non-monophyletic. This was demonstrated and discussed in several recent studies (e. g. Blasco-Costa & Locke, 2017 ; Hernández-Mena et al, 2017 ; Locke et al, 2018 ; Achatz et al, 2019b , c , d , 2020 ; Queiroz et al, 2019); therefore, we do not describe details here.

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“…PCR primers along with the 28S internal forward primer DPL600F (5′-CGG AGT GGT CAC CAC GAC CG-3′) and reverse primer DPL700R (5′-CAG CTG ATT ACA CCC AAA G-3′) and cox 1 internal forward primer BS_CO1_IntF (5′-ATT AAC CCT CAC TAA ATG ATT TTT TTY TTT YTR ATG CC-3′) and reverse primer (5′-TAA TAC GAC TCA CTA TAA AAA AAA MAM AGA AGA RAA MAC MGT AGT AAT-3′) were used for sequencing reactions (Achatz et al, 2019a , d ). Contiguous sequences were assembled using Sequencher version 4.2 software (GeneCodes Corp., Ann Arbor, Michigan, USA).…”

“…lanceolatum , 17 representatives of the Diplostomidae Poirier, 1886, and 13 taxa of the Strigeidae Railliet, 1919. Suchocyathocotyle crocodili (Yamaguti, 1954) was used as an outgroup based on the phylogeny published by Achatz et al ( 2019d ).…”

“…While significant progress has been recently achieved in the molecular phylogenetics and systematics of the Diplostomoidea Poirier, 1886 and its major constituent lineages (e.g. Blasco-Costa & Locke, 2017 ; Hernández-Mena et al, 2017 ; Locke et al, 2018 ; Achatz et al, 2019b , c , d ; Queiroz et al, 2020 ), the Proterodiplostomidae remains one of the only diplostomoidean families to receive very little attention in molecular phylogenetic studies. This can be partly explained by the logistic challenges of obtaining fresh material from hosts that are often protected and difficult to collect.…”

Digenean trematodes in Hungarian freshwater aquacultures

“…The globally distributed digenean trematode family Cyathocotylidae Mühling, 1896, comprises species with the adult flukes often infecting the intestine of birds, and in more rare cases reptiles, mammals and fishes. The taxon is considered monophyletic representing an ancient digenean lineage ( Achatz et al, 2019 ). The presence of cyathocotylid metacercarie in various freshwater fishes was documented in Czechia ( Kvach et al, 2016 ), Finland ( Näreaho et al, 2017 ), France ( Gettová et al, 2016 ), Slovakia ( Ondračková et al, 2009 ) and Russia ( Kvach et al, 2015 ).…”