Taenia tapeworms: their biology,evolution and socioeconomic significance

A biological context for understanding human pathogens and parasites emanates from evolutionary studies among tapeworms of the genus Taenia. Human taeniasis and cysticercosis represent archaic associations and remain significant challenges for socioeconomic development, public health and food safety, and a continuing threat to animal production on a global basis.     

Morphologic and genetic identification of Taenia tapeworms in Tanzania and DNA genotyping of Taenia solium

Species identification of Taenia tapeworms was performed using morphologic observations and multiplex PCR and DNA sequencing of the mitochondrial cox1 gene. In 2008 and 2009, a total of 1,057 fecal samples were collected from residents of Kongwa district of Dodoma region, Tanzania, and examined microscopically for helminth eggs and proglottids. Of these, 4 Taenia egg positive cases were identified, and the eggs were subjected to DNA analysis. Several proglottids of Taenia solium were recovered from 1 of the 4 cases. This established that the species were T. solium (n = 1) and T. saginata (n = 3). One further T. solium specimen was found among 128 fecal samples collected from Mbulu district in Arusha, and this had an intact strobila with the scolex. Phylegenetic analysis of the mtDNA cox1 gene sequences of these 5 isolates showed that T. saginata was basal to the T. solium clade. The mitochondrial cox1 gene sequences of 3 of these Tanzanian isolates showed 99% similarity to T. saginata, and the other 2 isolates showed 100% similarity to T. solium. The present study has shown that Taenia tapeworms are endemic in Kongwa district of Tanzania, as well as in a previously identified Mbulu district. Both T. solium isolates were found to have an "African/Latin American" genotype (cox1).     

Cryptic diversity in hymenolepidid tapeworms infecting humans

An adult hymenolepidid tapeworm was recovered from a 52-year-old Tibetan woman during a routine epidemiological survey for human taeniasis/cysticercosis in Sichuan, China. Phylogenetic analyses based on sequences of nuclear 28S ribosomal DNA and mitochondrial cytochrome c oxidase subunit 1 showed that the human isolate is distinct from Hymenolepis diminuta and Hymenolepis nana, the common parasites causing human hymenolepiasis. Proglottids of the human isolate were unfortunately unsuitable for morphological identification. However, the resultant phylogeny demonstrated the human isolate to be a sister species to Hymenolepis hibernia from Apodemus mice in Eurasia. The present data clearly indicate that hymenolepidid tapeworms causing human infections are not restricted to only H. diminuta and H. nana.     

A possible nuclear DNA marker to differentiate the two geographic genotypes of Taenia solium tapeworms

Cysticercosis caused by infection with embryonated eggs of the pork tapeworm Taenia solium is an important cause of neurological disease worldwide. Based on the phylogenetic analysis of mitochondrial DNA, the pathogen has been divided into two geographic clades, corresponding to Afro-American and Asian genotypes. In this study the genotyping of T. solium was carried out by using the nuclear DNA sequences of the immunodiagnostic antigen genes Ag1V1 and Ag2. The two geographic genotypes were supported by the Ag2 sequences, especially showing unique substitutions in each of the genotypes. It seems likely that the Ag2 may be a novel nuclear DNA marker to distinguish the two geographic genotypes of T. solium.     

Molecular identification of Taenia tapeworms by Cox1 gene in Koh Kong, Cambodia

We collected fecal samples from 21 individuals infected with Taenia tapeworms in Koh Kong Province, Cambodia, and performed nucleotide sequencing of the cox1 gene and multiplex PCR on the eggs for DNA differential diagnosis of human Taenia tapeworms. Genomic DNA was extracted from the eggs of a minimum number of 10 isolated from fecal samples. Using oligonucleotide primers Ta7126F, Ts7313F, Tso7466F, and Rev7915, the multiplex PCR assay proved useful for differentially diagnosing Taenia solium, Taenia saginata, and Taenia asiatica based on 706, 629, and 474 bp bands, respectively. All of the Taenia specimens from Kho Kong, Cambodia, were identified as either T. saginata (n=19) or T. solium (n=2) by cox1 sequencing and multiplex PCR.     

Out of Africa: the slow train to australasia

We used mitochondrial DNA (mtDNA) sequences to test biogeographic hypotheses for Patiriella exigua (Asterinidae), one of the world's most widespread coastal sea stars. This small intertidal species has an entirely benthic life history and yet occurs in southern temperate waters of the Atlantic, Indian, and Pacific oceans. Despite its abundance around southern Africa, southeastern Australia, and several oceanic islands, P. exigua is absent from the shores of Western Australia, New Zealand, and South America. Phylogenetic analysis of mtDNA sequences (cytochrome oxidase I, control region) indicates that South Africa houses an assemblage of P. exigua that is not monophyletic (P = 0.04), whereas Australian and Lord Howe Island specimens form an interior monophyletic group. The placement of the root in Africa and small genetic divergences between eastern African and Australian haplotypes strongly suggest Pleistocene dispersal eastward across the Indian Ocean. Dispersal was probably achieved by rafting on wood or macroalgae, which was facilitated by the West Wind Drift. Genetic data also support Pleistocene colonization of oceanic islands (Lord Howe Island, Amsterdam Island, St. Helena). Although many biogeographers have speculated about the role of long-distance rafting, this study is one of the first to provide convincing evidence. The marked phylogeographic structure evident across small geographic scales in Australia and South Africa indicates that gene flow among populations may be generally insufficient to prevent the local evolution of monophyly. We suggest that P. exigua may rely on passive mechanisms of dispersal.     

Out of Africa and into an ice age: on the role of global climate change in the late Pleistocene migration of early modern humans out of Africa

The results from two climate model simulations are used to explore the relationship between North Atlantic sea surface temperatures and the development of African aridity around 100,000 years ago. Through the use of illustrative simulations with an Earth System Climate Model, it is shown that freshwater fluxes associated with ice sheet surges into the North Atlantic, known as Heinrich events, lead to the southward shift of the intertropical convergence zone over Africa. This, combined with the overall increased aridity in the cooler mean climate, leads to substantial changes in simulated African vegetation cover, particularly in the Sahel. We suggest that Heinrich events, which occurred episodically throughout the last glacial cycle, led to abrupt changes in climate that may have rendered large parts of North, East, and West Africa unsuitable for hominin occupation, thus compelling early Homo sapiens to migrate out of Africa.     

Phylogenetic characterisation of Taenia tapeworms in spotted hyenas and reconsideration of the “Out of Africa” hypothesis of Taenia in humans

The African origin of hominins suggests that Taenia spp. in African carnivores are evolutionarily related to the human-infecting tapeworms Taenia solium, Taenia saginata and Taenia asiatica. Nevertheless, the hypothesis has not been verified through molecular phylogenetics of Taenia. This study aimed to perform phylogenetic comparisons between Taenia spp. from African hyenas and the congeneric human parasites. During 2010–2013, 233 adult specimens of Taenia spp. were collected from 11 spotted hyenas in Ethiopia. A screening based on short DNA sequences of the cytochrome c oxidase subunit 1 gene classified the samples into four mitochondrial lineages designated as I–IV. DNA profiles of nuclear genes for DNA polymerase delta (pold) and phosphoenolpyruvate carboxykinase (pepck) showed that lineages II and III can be assigned as two independent species. Common haplotypes of pold and pepck were frequently found in lineages I and IV, suggesting that they constitute a single species. Morphological observations suggested that lineage II is Taenia crocutae, but the other lineages were morphologically inconsistent with known species, suggesting the involvement of two new species. A phylogenetic tree of Taenia spp. was reconstructed by the maximum likelihood method using all protein-coding genes of their mitochondrial genomes. The tree clearly demonstrated that T. crocutae is sister to T. saginata and T. asiatica, whereas T. solium was confirmed to be sister to the brown bear tapeworm, Taenia arctos. The tree also suggested that T. solium and T. arctos are related to two species of Taenia in hyenas, corresponding to lineages I + IV and III. These results may partially support the African origin of human-infecting Taenia spp., but there remains a possibility that host switching of Taenia to hominins was not confined to Africa. Additional taxa from African carnivores are needed for further testing of the “Out of Africa” hypothesis of Taenia in humans.     

Phylogenetic relationships within Echinococcus and Taenia tapeworms (Cestoda: Taeniidae): an inference from nuclear protein-coding genes

The family Taeniidae of tapeworms is composed of two genera, Echinococcus and Taenia, which obligately parasitize mammals including humans. Inferring phylogeny via molecular markers is the only way to trace back their evolutionary histories. However, molecular dating approaches are lacking so far. Here we established new markers from nuclear protein-coding genes for RNA polymerase II second largest subunit (rpb2), phosphoenolpyruvate carboxykinase (pepck) and DNA polymerase delta (pold). Bayesian inference and maximum likelihood analyses of the concatenated gene sequences allowed us to reconstruct phylogenetic trees for taeniid parasites. The tree topologies clearly demonstrated that Taenia is paraphyletic and that the clade of Echinococcus oligarthrus and Echinococcusvogeli is sister to all other members of Echinococcus. Both species are endemic in Central and South America, and their definitive hosts originated from carnivores that immigrated from North America after the formation of the Panamanian land bridge about 3 million years ago (Ma). A time-calibrated phylogeny was estimated by a Bayesian relaxed-clock method based on the assumption that the most recent common ancestor of E. oligarthrus and E. vogeli existed during the late Pliocene (3.0 Ma). The results suggest that a clade of Taenia including human-pathogenic species diversified primarily in the late Miocene (11.2 Ma), whereas Echinococcus started to diversify later, in the end of the Miocene (5.8 Ma). Close genetic relationships among the members of Echinococcus imply that the genus is a young group in which speciation and global radiation occurred rapidly.     

A loop-mediated isothermal amplification method for a differential identification of Taenia tapeworms from human: Application to a field survey

In this study, we applied a loop-mediated isothermal amplification method for identification of human Taenia tapeworms in Tibetan communities in Sichuan, China. Out of 51 proglottids recovered from 35 carriers, 9, 1, and 41 samples were identified as Taenia solium, Taenia asiatica and Taenia saginata, respectively. Same results were obtained afterwards in the laboratory, except one sample. These results demonstrated that the LAMP method enabled rapid identification of parasites in the field surveys, which suggested that this method would contribute to the control of Taenia infections in endemic areas.     

Out of Africa: The Success Story of Tilapias

Beveridge M.C.M. & B.J. McAndrew (ed.) 2000. Tilapias: biology and exploitation. Fish and Fisheries Series 25, Kluwer Academic Publishers, Dordrecht. 505 pp. U.S. $180.00 (harbound), $53.00 (paper)     

Out of South America: multiple origins of non-native apple snails in Asia

Apple snails (Ampullariidae: Pomacea ) native to the New World have become agricultural and environmental pests widely in southern and eastern Asia since their introduction in about 1980. Although their impacts have been extensively documented, considerable confusion persists regarding their identities and geographical origins. Efforts to resolve the confusion have suffered from inadequate taxonomic and geographical sampling from both native and introduced ranges. Using phylogenetic and genealogical methods, we analysed 610–655 bp of cytochrome c oxidase subunit I DNA sequences from 783 apple snails from 164 Asian locations and 57 native South American locations. In Asia, we found four species of Pomacea in two clades: (1) Pomacea canaliculata and P. insularum , and (2) P. scalaris and P. diffusa . Parsimony networks and mismatch distributions indicate that the non-native ranges of the two most widespread species, P. canaliculata and P. insularum , probably result from multiple introductions. Molecular analyses are consistent with early accounts; non-native P. canaliculata populations trace back to multiple locations in Argentina and have probably been introduced more than once. In contrast, P. insularum was probably introduced from Brazil and Argentina independently. Multiple introductions may, in part, explain the success and rapid spread of these two species. Unlike P. canaliculata and P. insularum , P. scalaris and P. diffusa were probably introduced through the aquarium trade, derived originally from Argentina and Brazil, respectively. Possible physiological, ecological, and native range differences among these four species highlight the importance of accurate identification in understanding invasion patterns and processes, which is vital in developing and implementing management strategies.     

Out of Africa and back again

If the genusHomo did indeed originate in Africa, then it must have spread by about 2 m.y. ago into Asia where it is represented at 1.8 m.y. ago byHomo erectus fossils. This latter species in turn eventually spread back into Africa, as indicated by the 1.4 m.y. old OH 9 calvaria from Olduvai, and into Europe, as indicated by the 800,000 year old Ceprano calvaria from Italy. These hominids are associated only with Oldowan style artefacts of cores, choppers and flakes and were apparently not conversant with Acheulean handaxe technology. It seems that they most probably evolved viaHomo heidelbergensis into the Neanderthals. Meanwhile, a completely separate development originating withHomo ergaster of about 1.7 m.y. ago in Africa and possessing Acheulean handaxe technology evolved via such forms as Ndutu and Steinheim intoHomo sapiens.