Taxonomic review of cestodes of the genus Catenotaenia Janicki, 1904 in Eurasia and molecular phylogeny of the Catenotaeniidae (Cyclophyllidea)

Abstract

This study reviews the taxonomy of cestodes of the genus Catenotaenia Janicki, 1904 (Cyclophyllidea: Catenotaeniidae) in Eurasia and presents the first molecular phylogenetic hypothesis of Catenotaenia, Skrjabinotaenia Ahumyan, 1946 and Meggittina Lynsdale, 1953, all parasites of rodents. The phylogenetic data are based on sequences of 28S ribosomal RNA. The analysis does not support the proposed subfamilial classification of the Catenotaeniidae into Catenotaeniinae Spasskii, 1949 and Skrjabinotaeniinae Genov & Tenora, 1979. Instead, the main division appears to be between Eurasian species and a basal Nearctic species. The results support the monophyly of the Skrjabinotaeniinae but not that of the Catenotaeniinae or Catenotaenia as traditionally understood. It is suggested that the Old World catenotaeniid cestodes appeared in murid rodents and diverged subsequently as Skrjabinotaenia and Meggittina (Skrjabinotaeniinae) in Africa. According to the molecular phylogeny, Eurasian Catenotaenia codiverged with their hosts, with the exception of Catenotaenia dendritica that originated via a host shift from murid rodents to squirrels. The crown clade of Eurasian Catenotaenia consists only of species found in cricetid rodents and the three terminal species only in the Arvicolinae (voles). Phylogenetic structure within the Eurasian Catenotaenia clade suggests seven distinct lineages, three of which are described as new: C. apodemi n. sp. from Apodemus peninsulae (type host) from the Republic of Buryatia and from Apodemus uralensis from the Lower Tunguska River, North-Central Siberia (Russian Federation); C. cricetuli n. sp. from Cricetulus barabensis from the Republic of Buryatia and C. microti n. sp. from Microtus socialis from Kazakhstan. A new genus (Catenotaenioides n. g.) is proposed for C. kirgizica Tokobaev, 1959, a basal species within the Old World clade. Of the various morphological features, proglottid form (short acraspedote proglottids widest at middle vs. elongated craspedote proglottids widest posteriorly) is consistent with the phylogenetic pattern exhibited by catenotaeniid cestodes.

Molecular systematics and evolutionary history of catenotaeniid cestodes (Cyclophyllidea)

“…The crown clade 5 includes species from cricetids only, also indicative of a host shift rather than phyletic coevolution. However, the divergence of clade 5 may be partly due to phyletic coevolution, because the subfamilies Cricetinae (hosts for Catenotaenia cricetuli Haukisalmi, Hardman & Henttonen, 2010) and the Arvicolinae (hosts for the other species in this subclade) are sister groups within the family Cricetidae (Blanga-Kanfi et al, 2009;Steppan, Adkins, & Anderson, 2004). Clade 8 probably originated and diversified in arvicolines (voles) in Eurasia, followed by a colonization of North America with voles of the genus Myodes.…”

“…In other tapeworm families, such as the Anoplocephalidae (also lacking a rostellum), application of DNA sequences has resulted in recognition of several cryptic species and provided grounds for genus-level revisions (Hardman, Haukisalmi, & Beveridge, 2012;Haukisalmi, Hardman, Hardman, Rausch, & Henttonen, 2008;Haukisalmi, Hardman, Hoberg, & Henttonen, 2014;Haukisalmi, Wickström, Henttonen, Hantula, & Gubányi, 2004;Haukisalmi et al, 2009). The only existing molecular systematic study on catenotaeniids (Haukisalmi et al, 2010) concerned mainly the genus Catenotaenia in Eurasia. Based on molecular and morphological evidence, three new species and one new genus (Catenotaenioides) were described.…”

“…However, the subfamily Catenotaeniinae was found to be non-monophyletic due to the deviant basal position of a single North American species of Catenotaenia. The data of Haukisalmi et al (2010) could not, however, be used to properly evaluate the prevailing systematics of catenotaeniids, because of poor representation of North American (Catenotaenia) and African species (Hemicatenotaenia, Skrjabinotaenia and Meggittina), and because it did not include any type species. Further, only one molecular marker (28S nuclear rDNA) was applied.…”

“…This study expands on Haukisalmi et al (2010) and applies two independent DNA markers and includes several additional species, particularly from Africa, to examine the systematic relationships and evolutionary history of catenotaeniids, and hidden diversity in Catenotaenia, Skrjabinotaenia and Meggittina. The material includes the type species of six genera.…”

“…The type species of all six genera, that is, Catenotaenia pusilla, Catenotaenioides kirgizica (Tokobaev, 1959), Pseudocatenotaenia matovi (Genov, 1971), Hemicatenotaenia geosciuri (Ortlepp, 1938), Skrjabinotaenia oranensis and Meggittina baeri Lynsdale, 1953, are included in the present material. Ten of the present 28S nuclear rDNA sequences were published in connection of a previous phylogenetic study (Haukisalmi et al, 2010); other isolates and sequences are new. The 28S sequences of Catenotaenia indica Parihar & Nama, 1977 and P. matovi were kindly provided by D. Timothy J. Littlewood and Andrea Waeschenbach.…”