Molecular evidence of host influences on the evolution and spread of human tapeworms

Abstract

The taeniasis/cysticercosis complex is included in the list of neglected zoonotic diseases by the World Health Organization due to its significant impact on public health in tropical areas. Cysticercosis is still endemic in many regions of Asia, Africa and Latin America. Long absent in Europe and in other developed countries, cysticercosis has recently re-emerged in the United States and Canada, due to immigration, travel and local transmission. This has encouraged the use of molecular data to understand better the influence of animal and human hosts on the emergence and spread of Taenia species. The increasing number of mitochondrial sequences now available from human tapeworms and recent advances in computational tools has enabled reconstruction of the biogeography and evolutionary history of these organisms. New molecular data have provided insights into the biogeography of T. solium, T. asiatica and T. saginata. A Bayesian statistical framework using variable evolutionary rates from lineage to lineage has allowed an improved timescale analysis of human tapeworms. The dates of divergence obtained were compared to the timing of evolutionary events in the history of their hosts, based on the hypothesis that Taenia spp. and their hosts share a common history. Herein, we review changes in the definitive and secondary hosts and human interactions that underlie the differentiation and evolution of tapeworms. Species diversification of Taenia seems to be closely linked with the evolution of intermediate hosts in response to climatic events during the Pleistocene. Different genotypes of T. solium emerged when European and Asian wild boar Sus spp. populations diverged. Taenia saginata emerged when wild cattle Bos primigenius evolved and when zebu Bos indicus and taurine Bos taurus ancestors separated. Humans through migrations and later with the development of farming and animal husbandry may have had a significant impact on the spread and diversification of tapeworms. Migrations of Homo erectus from Africa to Asia and later of Homo sapiens facilitated the diversification and dispersal of T. solium and T. saginata populations. The development of animal husbandry, making Sus scrofa and Bos taurus preferential intermediate hosts, led to the worldwide distribution of parasites. New molecular data combined with an innovative dating method allow us to explain the ways in which ancient human migrations promoted the emergence and spread of taeniasis and cysticercosis around the world. Another intriguing phenomenon explained better by our approach is the influence of human settlement on the spread of these parasites in recently inhabited areas. The diverse nature of T. solium currently observed in Madagascar may correspond to multiple imports of the parasite during Austronesian migrations, while in Mexico a recent influence of humans during the colonial period is more likely. Human activities, especially food preparation and husbandry methods, remain responsible for the transmission and persistence of these parasites.

Epidemiology and genetic diversity of Taenia asiatica: a systematic review

“…This diversification might have co-occurred with the arrival of Homo sapiens in Asia, and the introduction of new wild boar populations and/or new breeding and husbandry practices in this region [63,95]. Again, these results indicate a closer relatedness of T. asiatica with T. saginata than with T. solium .…”

Recent advances and perspectives in molecular epidemiology of Taenia solium cysticercosis

“…Disseminated cysticercosis cases are caused mainly in tapeworm carriers themselves by autoinfection even if detection of tapeworm(s) is not always easy (Schantz et al, 1983Margono et al, 2002;Kobayashi et al, 2013;. The only definitive host of T. solium is human, Homo sapiens (de Queiroz and Alkire, 1998;Hoberg et al, 1999Hoberg et al, , 2001Hoberg, 2002Hoberg, , 2006Michelet and Dauga, 2012;Zarlenga et al, 2014a,b). Adult tapeworm matures in the human intestine after eating uncooked pork contaminated with cysticercus or cysticerci.…”

“…Even selfing is only way for fertilization in a single tapeworm infection, it is not clear if fertilization occurs within a single gravid proglottid or between different proglottids or both. As the two genotypes of T. solium were confirmed in Madagascar (Michelet et al, 2010;Michelet and Dauga, 2012), T. solium samples in Madagascar are expected to be ideal for analyzing if there are any out-crossings or not. For such studies, both mitochondrial and nuclear genes have to be compared as it has been done for T. saginata and T. asiatica (Okamoto et al, 2010;Yamane et al, 2012Yamane et al, , 2013.…”

Genetic variation in the Cytbgene of human cerebral Taenia soliumcysticerci recovered from clinically and radiologically heterogeneous patients with neurocysticercosis

“…One of these strains was isolated from Asia and the other strain was isolated from Africa and Latin America ( Okamoto et al 2001 ). The possible reasons for this divergence have been recently explored ( Michelet & Dauga 2012 ). Cytb has also been employed for molecular epidemiological surveys of other parasitic diseases ( Sakuma et al 2012 ) and in the clinical diagnosis of cysticercosis ( Kobayashi et al 2013 ).…”