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United States Department of Agriculture

Agricultural Research Service

Title: Phylogeny of Taenia: Species Definitions and Origins of Human Parasites.

Author
item Hoberg, Eric

Submitted to: Parasitology International
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: November 10, 2005
Publication Date: February 14, 2006
Citation: Hoberg, E.P. 2006. Phylogeny of Taenia: species definitions and origins of human parasites. Parasitology International. 50(Supplement):S23-S30.

Interpretive Summary: Establishing hypotheses for species and a capacity to apply a uniform methodology to establish their limits is fundamental in parasitology and all disciplines of biology, however, the “species problem” continues to be difficult to resolve. Accurate recognition of species serves as a basis for studies of diversity and host-parasite assemblages across a continuum from biotic survey and inventory to epidemiology and is a first line of response in diagnostics and medicine. Recognition of species-status implies historical independence and refines our ability to understand patterns and processes at the host-parasite interface, parameters of life history and the distribution of diseases attributable to parasites. In the absence of such information, and interpretations derived from phylogeny, we may tend to extrapolate incorrect biological information from unrelated species and compound errors in identification, diagnosis and regimes for treatment. Current studies among Taenia, and particularly the controversy over T. saginata and T. asiatica further emphasize the need for specific testable hypotheses designed to explore the history of diversification for parasitic groups. Species of Taenia are among the most characteristic tapeworms infecting carnivores and humans as definitive hosts and indeed Taeniidae is unique among the tapeworms in requiring 2 obligate mammalian hosts for transmission; a high percentage (> 80%) of life cycles have been completely elucidated among the approximately 45 species and nominal subspecies of Taenia. Until recently there had been no comprehensive attempts at reconstruction of a phylogeny among these important parasites. Such analyses have allowed us to explore the origins and evolution of those independent species of Taenia that occur in humans (T. saginata, T. asiatica, and T. solium) and to understand the ecological and historical processes serving as determinants of biogeography and host-association. These studies supported the status of T. asiatica as a valid species and diagnosed a relationship as the sister-species of T. saginata. These conclusions contrasted with a diversity of opinions that would subsume T. asiatica as a subspecies. Recognition of a species constitutes a specific and testable hypothesis, is not an arbitrary decision and is most appropriately assessed in the context of phylogenetic or historical data. Considering macrospecies, a process has been outlined by Brooks and McLennan [19] as follows: 1) Discovery: a systematist describes the species; (2) Phylogenetic reconstruction; (3) Evaluation I: do sister-species show geographical overlap- are they sympatric or allopatric (use phylogeny + geographical distributions)? (4) Evaluation II: Are sister- species reproductively isolated based on information from natural history, ecology and reproductive biology? Species may be viewed in the context of microevolutionary and macroevolutionary processes. For instance, microspecies are defined in ecological time and involve populations and contemporary process that are potentially reversible (reticulate). In contrast, macrospecies as exemplified by T. saginata and T. asiatica are divergent lineages resulting from processes in evolutionary time where an ancestor has undergone a permanent split that is non-reversible (non-reticulate). Applying these criteria in evaluation of T. saginata and T. asiatica, it becomes clear that in evolutionary time these represent historical lineages with independent spatial and temporal trajectories, having separated from a common ancestor near 0.78 to 1.71 MYBP in Africa, or Eurasia. In ecological time, sympatry (overlap in geographic ranges), reproductive isolation, and differences in life history evident for T. saginata and T. asiatica as observed in China, and perhaps other regions of Southeast Asia, further serve to validate these taeniids

Technical Abstract: Phylogeny is fundamental as it constrains explanations about history and forms our foundation for recognizing and diagnosing species. In the absence of such a framework taxonomists historically relied on intuitive processes, personal judgment and authority, often embracing a typological view of species that disregarded otherwise unequivocal historical and biological criteria. Species of Taenia are among the most characteristic tapeworms infecting carnivores and humans as definitive hosts and indeed Taeniidae is unique among the Eucestoda in requiring 2 obligate mammalian hosts for transmission; a high percentage (> 80%) of life cycles have been completely elucidated among the approximately 45 species and nominal subspecies of Taenia. Until recently there had been no comprehensive attempts at reconstruction of a phylogeny among these important parasites. Such analyses have allowed us to explore the origins and evolution of those independent species of Taenia that occur in humans (T. saginata, T. asiatica, and T. solium) and to understand the ecological and historical processes serving as determinants of biogeography and host-association. These studies supported the status of T. asiatica as a valid species and diagnosed a relationship as the sister-species of T. saginata. These conclusion contrasted with a diversity of opinions that would subsume T. asiatica as a subspecies. Recognition of a species constitutes a specific and testable hypothesis, is not an arbitrary decision and is most appropriately assessed in the context of phylogenetic or historical data. Considering macrospecies, a process has been outlined by Brooks and McLennan [19] as follows: 1) Discovery: a systematist describes the species; (2) Phylogenetic reconstruction; (3) Evaluation I: do sister-species show geographical overlap- are they sympatric or allopatric (use phylogeny + geographical distributions)? (4) Evaluation II: Are sister- species reproductively isolated based on information from natural history, ecology and reproductive biology? Species may be viewed in the context of microevolutionary and macroevolutionary processes. For instance, microspecies are defined in ecological time and involve populations and contemporary process that are potentially reversible (reticulate). In contrast, macrospecies as exemplified by T. saginata and T. asiatica are divergent lineages resulting from processes in evolutionary time where an ancestor has undergone a permanent split that is non-reversible (non-reticulate). Applying these criteria in evaluation of T. saginata and T. asiatica, it becomes clear that in evolutionary time these represent historical lineages with independent spatial and temporal trajectories, having separated from a common ancestor near 0.78 to 1.71 MYBP in Africa, or Eurasia. In ecological time, sympatry, reproductive isolation, and differences in life history evident for T. saginata and T. asiatica as observed in China, and perhaps other regions of Southeast Asia, further serve to validate these taeniids.

Last Modified: 11/23/2014