Genetic characterization of Moniezia species in Senegal and Ethiopia

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Highlights

  • We investigated the genetic diversity of Moniezia tapeworms in Senegal and Ethiopia.

  • Phylogenetic analysis was done with mitochondrial and nuclear gene sequences.

  • Tapeworms of sheep/goat and cattle were M. expansa and M. benedeni, respectively.

  • Three mitochondrial lineages were found in M. expansa.

  • Sequences in databases and this study were different, requiring revision of taxonomy.

Abstract

Genetic diversity of Moniezia spp. from domestic ruminants in Senegal and Ethiopia was investigated based on the nucleotide sequences of mitochondrial cytochrome c oxidase subunit 1 (cox1) and nuclear small subunit ribosomal RNA gene (SSU rDNA). A total of 64 adult tapeworms were collected from sheep, goat and cattle, and the tapeworms from cattle were all morphologically identified as Moniezia benedeni. On the other hand, the tapeworms obtained from sheep and goat were identified as Moniezia expansa or could not be identified because of the lack of diagnostic morphologic character, i.e. interproglottidal glands (IPGs). Phylogenetic analysis based on cox1 gene sequences revealed that the worms from sheep/goat and cattle formed distinct clades, and three mitochondrial lineages were confirmed within the sheep/goat tapeworms. The maximum pairwise divergences among the three mitochondrial linages were about 3% in cox1 and 0.1% in SSU rDNA, while that between the worms from sheep/goat and cattle reached 13% in cox1 and 2.7% in SSU rDNA. All of the three mitochondrial lineages contained tapeworms morphologically identified as M. expansa, and the tapeworms without IPGs were confirmed in one of the three lineages, indicating the tapeworms without IPGs were also M. expansa.

Introduction

Moniezia spp. are intestinal cestodes of ruminants with worldwide distribution. They belong to the family Anoplocephalidae in the order Cyclophyllidea, showing a characteristic body differentiation with scolex, neck and strobila. Scolex and neck are small but strobila is long chain and has species-specific patterning with sexual organs that do not mature at the same time. Anterior to posterior strobila are respectively immature, mature and gravid, with sexual organs repeated in each proglottid. The life cycle of Moniezia species includes oribatids as intermediate hosts, and infected mites are ingested by ruminants. Upon ingestion, larvae actively move to small intestine, attach with their suckers and mature [1]. Moniezia spp. are responsible for monieziasis, a gastrointestinal disorder in ruminant. Although it is generally considered that the pathogenicity of Moniezia tapeworms is mild, especially in adult livestock, gastrointestinal disorders in calves and lambs can provoke economic losses in stockbreeding [2], [3], [4].

Several field surveys in Africa demonstrated that there were many helminthic parasites in the small intestine of herbivorous mammals. Most studies in different ecological zones highlighted that in terms of prevalence, monieziasis remained one of the major helminthic parasites of ruminant [5], [6], [7], [8], [9]. In Senegal, the prevalence of Moniezia spp. was 28% in sheep and 11% in goat [10]. However, this analysis remains to be updated. Epizootic data from the Eastern part of Africa is different. In Ethiopia, Moniezia spp. infections were common in both sheep and goat, and overall prevalence was 61% and 53%, respectively [11].

Until now, the taxonomy of the genus Moniezia has been controversial. Although at least seven species have been described [12], morphological identification of the species is not always easy. Besides, genetic information is available for only three species of the genus, Moniezia expansa, Moniezia benedeni and Moniezia monardi [13]. Morphologically, M. expansa and M. benedeni are distinguishable based on their interproglottidal glands (IPGs) [12]. While M. expansa has the IPGs arranged in a rosette-pattern, M. benedeni has a short continuous linear-pattern of IPGs. However, it is not uncommon to find the worms without IPGs, which cannot be morphologically identified [12], [14]. Therefore, a multiplex PCR for differentiation of these two species has been developed [15]. However, existence of cryptic species in M. benedeni was demonstrated by multilocus enzyme electrophoresis in Australia [14], indicating the importance of investigating the genetic variation among geographic populations for the establishment of reliable identification, as well as for the reevaluation of conventional taxonomy.

The aim of the present study is to identify the species and to investigate the genetic diversity of Moniezia spp. sampled in Africa for the basis of molecular reevaluation of the genus Moniezia.

Section snippets

Collection and preparation of worms

Fresh adult worms were collected from intestines of sheep, goat and cattle in slaughterhouses in Senegal and Ethiopia (Western and Eastern part of Africa) during the wet season of 2011. Host animals were bred in different areas of each country. Senegalese samples were mostly brought from Northern and Eastern part and Ethiopian samples were collected from slaughterhouses located in the Eastern and Central part of the country. Due to slaughterhouse management, intestines from sheep and goat in

Morphology

In Senegal, a total of 49 and 6 adult worms of Moniezia spp. were collected from sheep/goat and cattle, respectively. In Ethiopia, eight and one tapeworms were obtained from sheep and goat, respectively. Morphological observation was conducted for 13 and 9 specimens from Senegal and Ethiopia, respectively. Among 13 Senegalese specimens, 10 were collected from sheep/goat and three were from cattle. Morphological observation revealed that there were three Moniezia morphotypes: with

Discussion

In the present study, genetic diversity of Moniezia spp. from sheep, goat and cattle in Senegal and Ethiopia was investigated. From the morphological point of view, the tapeworms collected from cattle were all identified as M. benedeni. On the other hand, tapeworms obtained from sheeps and goats were identified as M. expansa or could not be identified because of the lack of IPGs. Phylogenetic analysis based on cox1 gene sequences revealed that the tapeworms from sheep/goat and that from cattle

Conflict of interest statement

The authors have no conflicts of interest concerning the work reported in this paper.

Acknowledgments

This study was supported by a Grant-in-Aid for Scientific Research (no. 21256003) from Japan Society for the Promotion of Science (JSPS), JSPS-Asia/Africa Scientific Platform Fund (2006–2011) and the Special Coordination Fund for Promoting Science and Technology from the Ministry of Education, Japan (MEXT) (2010–2012) to A. Ito.

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    These authors contributed equally.

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