Phylogenetic Pattern, Evolutionary Processes and Species Delimitation in the Genus Echinococcus

Abstract

An accurate and stable alpha taxonomy requires a clear conception of what constitutes a species and agreed criteria for delimiting different species. An evolutionary or general lineage concept defines a species as a single lineage of organisms with a common evolutionary trajectory, distinguishable from other such lineages. Delimiting evolutionary species is a two-step process. In the first step, phylogenetic reconstruction identifies putative species as groups of organisms that are monophyletic (share a common ancestor) and exclusive (more closely related to each other than to organisms outside the group). The second step is to assess whether members of the group possess genetic exchangeability (where cohesion is maintained by gene flow among populations) or ecological exchangeability (where cohesion is maintained because populations occupy the same ecological niche). Recent taxonomic reviews have recognized nine species within the genus Echinococcus. Phylogenetic reconstructions of the relationships between these putative species using mtDNA and nuclear gene sequences show that for the most part these nine species are monophyletic, although there are important incongruences that need to be resolved. Applying the criteria of genetic and ecological exchangeability suggests that seven of the currently recognized species represent evolutionarily distinct lineages. The species status of Echinococcus canadensis and Echinococcus ortleppi could not be confirmed. Coalescent-based analyses represent a promising approach to species delimitation in these closely related taxa. It seems likely, from a comparison of sister species groups, that speciation in the genus has been driven by geographic isolation, but biogeographic scenarios are largely speculative and require further testing.

Introduction

Taeniid tapeworms (Eucestoda: Cyclophyllidae: Taeniidae) are important parasites of people throughout the world. Although as many as 13 genera have been described in the family, the most recent taxonomic revision recognized only four; Hydatigera, Taenia, Versteria, and Echinococcus (Nakao et al., 2013a). The genus Echinococcus is a monophyletic group of species characterized by small adult worms and larvae (metacestodes) with extensive asexual reproduction. Definitive hosts are carnivores, usually canids or felids, and infection is acquired by eating herbivorous or omnivorous intermediate hosts. Humans are accidental intermediate hosts, with the infection being known as echinococcosis or hydatid disease. There are three different types of echinococcosis, which result from infection with different species of Echinococcus and are named for the structure of the metacestode; cystic, alveolar or polycystic. Cystic and alveolar echinococcosis are major public health issues in many countries throughout the world and are recognized as neglected parasitic zoonoses (Moro and Schantz, 2009, Torgerson, 2013).

Classification and nomenclature within the genus Echinococcus have long been controversial topics, but in recent years molecular phylogenetic analyses have promised a resolution to this controversy. In this paper, I will briefly review the taxonomic history and currently accepted taxonomic designations within the genus, attempt to define an appropriate species concept, examine both the phylogenetic and population genetic data that are required to correctly delimit species according to that concept, apply criteria for delimitation to currently described species of Echinococcus and, finally, explore the phenotypic consequences of genetic variation among species.