The phylogeny of the Lepocreadioidea (Platyhelminthes, Digenea) inferred from nuclear and mitochondrial genes: Implications for their systematics and evolution

Abstract

The phylogenetic relationships of representative species of the superfamily Lepocreadioidea were assessed using partial lsrDNA and nad1 sequences. Forty-two members of the family Lepocreadiidae, six putative members of the Enenteridae, six gyliauchenid species and one Gorgocephalidae, were studied along with 22 species representing 8 families. The Lepocreadioidea is found to be monophyletic, except for the two species of the putative enenterid genus Cadenatella, which are found to be only distantly related to the lepocreadioids. The Lepocreadioidea is formed of five clades in a polytomy, the Gorgocephalidae, a clade containing the Enenteridae and Gyliauchenidae, a small clade of atypical lepocreadiines and the deep-sea lepidapedine lepocreadiids, a small clade consisting of a freshwater form and a group of shallow-water putative lepidapedines and the final clade includes the remaining lepocreadiids. Thus, the generally accepted concept of the Lepocreadiidae is polyphyletic. The Enenteridae (minus Cadenatella) and the Gyliauchenidae are jointly and individually monophyletic, and are sister groups. The nad1 gene on its own places a deep-sea lepocreadiine with the deep-sea lepidapedines, whereas lsrDNA, combined sequences and morphology place this deep-sea lepocreadiine within a group of typical lepocreadiids. It could not be demonstrated that a significant proportion of sites in the nad1 gene evolved under positive selection; this anomalous relationship therefore remains unexplained. Most deep-sea species are in a monophyletic group, a few of which also occur in shallow waters, retaining some characters of the deep-sea clade. Many lepocreadioid species infect herbivorous fish, and it may be that the recently discovered life-cycle involving a bivalve first intermediate host and metacercariae encysted on vegetation is a common life-cycle pattern. The host relationships show no indication of co-speciation, although the host-spectrums exhibited are not random, with related worms tending to utilize related hosts. There are, however, many exceptions. Morphology is found to be of limited value in indicating higher level relationships. For example, even with the benefit of hindsight the gyliauchenids show little morphological similarity to their sister group, the Enenteridae.

Ultrastructural characters of the spermatozoon of the digenean Hypocreadium caputvadum Kacem et al., 2011 (Lepocreadioidea: Lepocreadiidae), an intestinal parasite of Balistes capriscus in Tunisia

“…According to Bray [17] the Lepocreadioidea include ten families, namely the Lepocreadiidae, Acanthocolpidae, Apocreadiidae, Brachycladiidae, Deropristidae, Enenteridae, Gorgocephalidae, Gyliauchenidae, Liliatrematidae and Megaperidae. Nevertheless, based on molecular analyses, Bray et al [18] and more recently Bray and Cribb [19] re-organized the superfamily Lepocreadioidea. Bray et al [18] found the Lepocreadioidea to be monophyletic and constituted by six well-supported groups, which are presently considered families according to Bray and Cribb [19].…”

“…Nevertheless, based on molecular analyses, Bray et al [18] and more recently Bray and Cribb [19] re-organized the superfamily Lepocreadioidea. Bray et al [18] found the Lepocreadioidea to be monophyletic and constituted by six well-supported groups, which are presently considered families according to Bray and Cribb [19]. These families are the Lepocreadiidae, the Aephnidiogenidae and the Lepidapedidae, which were previously considered by Bray [20] as three subfamilies of the Lepocreadiidae s.l., and the Enenteridae, Gorgocephalidae and Gyliauchenidae.…”

Molecular characterization of three species belongs to the Allocreadioidea, Hemiuroidea and Plagiorchioidea (Platyhelminthes: Trematoda) infecting freshwater fishes in India

“…Genomic DNA was isolated using the DNeasy TM Tissue Kit (Qiagen, Hilden, Germany), following manufacturer's instructions. The 28S ribosomal DNA was amplifi ed using the primers, LSU5 (F) (5′-TAGGTCGACCCGCTGAAYTTAAGCA-3′) (Bray et al, 2009) and 1500R (5′-GCTATCCTGAGGGAAACTTCG-3′) (Tkach et al, 2003) in a 25 μl reaction mixture consist of 3 μl genomic DNA, 4 μl 1 mM deoxyribonucleotide triphosphates (dNTPs, Biotools, Spain), 0.6 μl of each primer, 2.5 μl of 10x Taq buffer (Biotools, Madrid, Spain), 0.5 μl of Taq polymerase (1U; Biotools, Madrid, Spain) and 13.8 μl of distilled water. The PCR cycling profi le were performed in a Mastercycler personal-22331 (Eppendorf, Hamburg, Germany) as follows: an initial denaturation at 94 °C for 3 min, followed by 35 cycles at 94 °C for 40 s, 56 °C for 1 min, 72 °C for 1 min, completed with terminal extension at 72°C for 7 min and then stored at 4 °C.…”

“…In India, for platyhelminthes taxonomy morphological differences have been widely used to discriminate between species. Though, traditional diagnostic tools are now complemented by molecular techniques for resolving the taxonomic confusions coupled with species descriptions (Prasad et al, 2011;Chaudhary et al, 2015;Chaudhary et al, 2016). In India, there is a scarcity of molecular tools in studies of trematode parasites.…”

Editorial: The biodiversity of trematodes of fishes

“…It is striking that, in almost every instance in which groups of trematodes are subjected to molecular phylogenetic analysis, unexpected but plausible changes in our understanding of relationships emerge (e.g. Choudhury et al, 2007;Bray et al, 2009;Cutmore et al, 2013;Pulis et al, 2014;Pinto et al, 2015). Despite this, the field can be considered to be in its infancy with the vast majority of genera and species not yet subjected to molecular phylogenetic analysis.…”