Expansion of Cyclophyllidea Biodiversity in Rodents of Qinghai-Tibet Plateau and the "Out of Qinghai-Tibet Plateau" Hypothesis of Cyclophyllideans

Abstract

The Cyclophyllidea comprises the most species-rich order of tapeworms (Platyhelminthes, Cestoda) and includes species with some of the most severe health impact on wildlife, livestock, and humans. We collected seven Cyclophyllidea specimens from rodents in Qinghai-Tibet Plateau (QTP) and its surrounding mountain systems, of which four specimens in QTP were unsequenced, representing "putative new species." Their complete mitochondrial (mt) genomes were sequenced and annotated. Phylogenetic reconstruction of partial 28S rDNA, cox1 and nad1 datasets provided high bootstrap frequency support for the categorization of three "putative new species," assigning each, respectively, to the genera Mesocestoides, Paranoplocephala, and Mosgovoyia, and revealing that some species and families in these three datasets, which contain 291 species from nine families, may require taxonomic revision. The partial 18S rDNA phylogeny of 29 species from Taeniidae provided high bootstrap frequency support for the categorization of the "putative new species" in the genus Hydatigera. Combined with the current investigation, the other three known Taeniidae species found in this study were Taenia caixuepengi, T. crassiceps, and Versteria mustelae and may be widely distributed in western China. Estimates of divergence time based on cox1 + nad1 fragment and mt protein-coding genes (PCGs) showed that the differentiation rate of Cyclophyllidea species was strongly associated with the rate of change in the biogeographic scenarios, likely caused by the uplift of the QTP; i.e., species differentiation of Cyclophyllidea might be driven by host-parasite co-evolution caused by the uplift of QTP. We propose an "out of QTP" hypothesis for the radiation of these cyclophyllidean tapeworms.

Keywords: Cyclophyllidea; Qinghai-Tibet Plateau; biogeography; phylogeny; rodents; species differentiation.

FIGURE 1

Maximum likelihood analyses of the four “putative new species” with other Cyclophyllidea species, except for Taeniidae, based on simplified 28S rDNA (A), cox1 (B) and nad1 (C) fragments. Alternating black and gray bands are used to classify different genera in the Taxonomy of NCBI, The Roman numerals to the right of the bands represent outgroup and different genus names (i.e., I: outgroup, II: Mesocestoididae, III: Catenotaeniidae, IV: Dipylidiidae, V: Anoplocephalidae, VI: Paruterinidae, VII: Gryporhynchidae, VIII: Dilepididae, IX: Hymenolepididae, X: Dipylidiidae). The ▲ after the species name represents “putative new species”. Bootstrap frequency support values are stated only for nodes where > 80%.

FIGURE 2

Maximum likelihood analysis of 18S rDNA of family Taeniidae. The ▲ after the species name represents “putative new species.” The outgroup is the same as Figure 1. Bootstrap frequency support values are stated only for nodes where > 80%.

FIGURE 3

The diagram of complete mitochondrial genome of Mesocestoides sp. RKZ08 (A), Paranoplocephala sp. RKZ13 (B), Hydatigera sp. XHPW10 (C), and Mosgovoyia sp. SQ20 (D). The protein-encoding genes are depicted in plum, the tRNAs are depicted in green, the rRNAs are depicted in light green and the non-coding mitochondrial regions (NCRs including LNR and SNR) are depicted in gray. The inferred gene boundaries of them are shown in Table 1.

FIGURE 4

Divergence time construction of concatenated cox1 + nad1 gene (A) and 12 mt PCGs (B) of Cyclophyllidea species. The ▲ after the species name represents “putative new species”. The blue bar represents interval of 95% highest probability density. The time scale bars in different colors shows the extent of the Eocene, Oligocene, Miocene, Pliocene, and Pleistocene period.

FIGURE 5

The number of divergent nodes in every 2 Mya over time based on the divergence time trees of Figure 4. The orange curve represents the change of divergence nodes number based on Figure 4A. The blue curve represents the change of divergence nodes number based on Figure 4B.