Characterization of Taenia madoquae and Taenia regis from carnivores in Kenya using genetic markers in nuclear and mitochondrial DNA, and their relationships with other selected taeniids

Abstract

In the present study, we have extended earlier taxonomic, biochemical and experimental investigations to characterize two species of Taenia from carnivores in Kenya by use of the sequences of a variable domain (D1) of nuclear ribosomal DNA and the cytochrome c oxidase subunit 1 and NADH dehydrogenase 1 genes of mitochondrial DNA. Emphasis was placed on the characterization of Taenia madoquae from the silver-backed jackal (Canis mesomelas) and Taenia regis from the lion (Panthera leo), given the previous absence of any DNA sequence data for them, and on assessing their genetic relationships with socioeconomically important taeniids. The study showed that T. regis was genetically most closely related to T. hydatigena, and T. madoquae to T. serialis, T. multiceps or T. saginata. The present findings provide a stimulus for future work on the systematic relationships and epidemiology of lesser-known taeniid cestodes in Africa and other continents, employing mitochondrial sequence data sets.

Introduction

Species of Taenia (Cestoda: Taeniidae) are harboured, as adult tapeworms, in the small intestines of carnivorous or human definitive hosts, and are transmitted to intermediate mammalian hosts where they become established as larval stages in tissues, causing significant disease (cysticercosis or coenuriasis) [1]. A number of species of Taenia have public health and economic impact, because they are zoonotic and cause losses to the meat industry due to the condemnation of infected offal or meat [2], [3], [4], [5]. The specific identification of taeniids is central to their control as well as to investigating their life cycles, ecology and epidemiology, and is usually based on a combination of ecological, biological and morphological criteria, including the morphology of the adult stage (such as the number, size and shape of the rostellar hooks, the distribution of the testes, the shape of the cirrus-sac and its extent relative to the longitudinal osmoregulatory canals, the presence or absence of a vaginal sphincter, the location of the genital pore along the segment margin and the number of principal lateral branches of the gravid uterus), the morphology and type of asexual reproduction of the larval stage, and the level of host specificity in different geographical regions [6], [7], [8], [9], [10], [11]. However, unequivocal identification based on these criteria is often difficult.

Biochemical and traditional molecular approaches (e.g., multilocus enzyme electrophoresis (MEE) and restriction fragment length polymorphism (RFLP) combined with Southern blot) have assisted in the genetic characterization and identification of Taenia spp. from different hosts [12], [13]. Recently, techniques, such as partial or whole mitochondrial genome sequencing, based on the use of the polymerase chain reaction (PCR) [14] have found broader applicability, mainly because their sensitivity permits the analysis of particular genes from tiny amounts of DNA from fresh, frozen or even ethanol fixed parasite material [15], [16]. While there is significant DNA sequence information for taeniids of socioeconomic importance, there are limited data for the lesser-known species, particularly those from Africa (reviewed in [6], [11]). In the present study, we extend earlier studies [17], [18], in order to characterize different species of Taenia from carnivores in Kenya using sequences from one nuclear ribosomal and two mitochondrial DNA regions. Emphasis was placed on the characterization of Taenia madoquae from the silver-backed jackal (Canis mesomelas) and Taenia regis from the lion (Panthera leo), and on assessing their genetic relationships with socioeconomically important taeniids.