Abstract
The larva of Taeniidae species can infect a wide range of mammals,
causing major public health and food safety hazards worldwide. The
Qinghai-Tibet Plateau (QTP), a biodiversity hotspot, is home to many
species of rodents, which act as the critical intermediate hosts of many
Taeniidae species. In this study, we identified two new larvae ofTaenia spp., named as T. caixuepengi and T.
tianguangfui , collected from the plateau pika (Ochotona
curzoniae ) and the Qinghai vole (Neodon fuscus ), respectively in
QTP, and their mitochondrial genomes were sequenced and annotated.
Phylogenetic trees based on the mitochondrial genome showed thatT. caixuepengi has the closest genetic relationship with T.
pisiformis , while T. tianguangfui was contained in a
monophyletic group with T. crassiceps , T. twitchelli andT. martis . Biogeographic scenarios analysis based on split time
speculated that the speciation ofT. caixuepengi(~5.49 Mya) is due to host switching caused by the
evolution of its intermediate host. Although the reason for T.
tianguangfui (~13.11 Mya) speciation is not clear, the
analysis suggests that it should be infective to a variety of other
rodents following the evolutionary divergence time of its intermediate
host and the range of intermediate hosts of its genetically close
species. This study confirms the species diversity of Taeniidae in the
QTP, and speculates that the uplift of the QTP has not only a profound
impact on the biodiversity of plants and animals, but also that of
parasites.
Keywords: Taenia spp., mtDNA, Qinghai-Tibet Plateau,
Phylogeny, Divergence time
Running head: Two newly identified Taenia spp. in China
Introduction
The most recent molecular phylogenetic analysis has suggested that
the
family Taeniidae (Eucestoda: Cyclophyllidae) should be composed of four
genera:Taenia , Echinococcus , Hydatigera andVersteria (Nakao et al., 2013). Among them, Taenia andEchinococcus species pose a serious public health threat to
humans and animals globally. Terrestrial mammals are crucial to the life
cycle of taeniids. Adult tapeworm of most taeniid species parasitizes
the intestine of carnivores, while their eggs infect the intermediate
host, usually herbivores and omnivores as well as humans, through
fecal-oral route, and develop into larvae, which cause severe health
effects (Deplazes et al., 2019; Jia et al., 2012; Lymbery, 2017; Nakao
et al., 2013).
Before Nakao’s new classification recommendation, Taeniidae was
generally supposed to consist of two valid genera, Taenia andEchinococcus , and the genus Taenia (Linnaeus, 1758) was
demarcated approximately into 42 valid species and three subspecies by
adult and metacestode morphology (Hoberg, 2006; Hoberg et al., 2000;
Nakao et al., 2013). As for Echinococcus , a total of 16 species
and 13 subspecies were described based on morphology before the
widespread application of molecular genetic methods, but most of these
taxa were subsequently regard as invalid (Lymbery, 2017). It is
difficult to distinguish taeniid species according to their
morphological characteristics at different stages of their life cycle,
even by specialists (Flisser et al., 2005; Jia et al., 2012; Mathis &
Deplazes, 2006). Sometimes, morphological characteristics are
substantially influenced by the different intermediate host origins
(Lymbery, 1998).
Mitochondrial (mt) DNA sequence has been recognized among the most
suitable molecular markers of molecular ecology, population genetics,
evolutionary biology and biological differentiation due to its high
mutation rate and maternal inheritance (Jia et al., 2012; Hajibabaei et
al., 2007; Hebert & Gregory, 2005; Will et al., 2005). In the last two
decades, comparative analyses of taeniid mtDNAs have been increasingly
applied to phylogenetic studies, from estimating the evolutionary status
for new species identification and even species reclassification, to
investigating the phylogeography and genetic diversity for tracing the
evolutionary origins of related and identical species (Kinkar et al.,
2018; Nakao et al., 2007; Nakao et al., 2013; Terefe et al., 2014; Xiao
et al., 2005). Among the taeniid family, mt genomes of 36 species and
genotypes have been sequenced and are available on GenBank
(https://www.ncbi.nlm.nih.gov/genbank/ ), providing valuable data
support for phylogenetic studies of Taeniidae.
The shrinkage and fragmentation of wildlife habitats due to human
activities can lead to increased contact between humans or livestock and
wildlife, which potentially increases the risk of transmission of
natural focal disease (Suzán et al., 2008). Rodents, the largest
(~43% of all mammal species) and most widely
distributed group of mammals, act as major vectors of human and domestic
animal diseases (Singla et al., 2008; Wu et al., 2018). The
Qinghai-Tibet Plateau (QTP), one of the biodiversity hotspots on earth,
is habitat to a rich diversity of wild rodent species (Zhou & Ma,
2002), as well as many rodent-eating carnivores (Smith et al., 2019),
creating the conditions for various taeniid species to complete their
life cycles. The high altitude geographic isolation combined with the
geological complexity of the QTP increases the opportunities for genetic
variation and speciation, leading to the continuous discovery of new
species within rodents and Taeniidae (Dahal et al., 2017; Xiao et al.,
2005). However, few studies have involved the population structure and
biodiversity of taeniid species in QTP, except for Echinococcus .
As endangered or protected carnivores are difficult to sample, we
collected metacestode samples of rodents to investigate the biodiversity
and distribution of taeniid species in QTP. In this study, two new mt
genomes of the metacestode samples were firstly sequenced and annotated.
Through the phylogenetic analysis of mt genomes with species in the four
different genera of taeniids, the validity of these two newTaenia spp., named as T.
caixuepengiand T. tianguangfui larvae, were confirmed and their phylogenetic
relationship and evolutionary origin were analyzed.
Materials and methods