A novel phylogeny for the genus Echinococcus, based on nuclear data, challenges relationships based on mitochondrial evidence

Abstract

The taxonomic status of Echinococcus, an important zoonotic cestode genus, has remained controversial, despite numerous attempts to revise it. Although mitochondrial DNA (mtDNA) has been the source of markers of choice for reconstructing the phylogeny of the genus, results derived from mtDNA have led to significant inconsistencies with earlier species classifications based on phenotypic analysis. Here, we used nuclear DNA markers to test the phylogenic relationships of members of the genus Echinococcus. The analysis of sequence data for 5 nuclear genes revealed a significantly different phylogeny for Echinococcus from that proposed on the basis of mitochondrial DNA sequence data, but was in agreement with earlier species classifications. The most notable results from the nuclear phylogeny were (1) E. multilocularis was placed as basal taxon, (2) all genotypes of Echinococcus granulosus grouped as a monophyletic entity, and (3) genotypes G8 and G10 clustered together. We conclude that the analysis of nuclear DNA data provides a more reliable means of inferring phylogenetic relationships within Echinococcus than mtDNA and suggest that mtDNA should not be used as the sole source of markers in future studies where the goal is to reconstruct a phylogeny that does not only reflect a maternal lineage, but aims to describe the evolutionary history at species level or higher.

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

“…shiquicus, the nuclear DNA phylogenies of Knapp et al (2011) are in agreement with the mtDNA phylogenies of Nakao et al (2007Nakao et al ( , 2013b and Hüttner et al (2008), while the phylogeny of Saarma et al (2009) suggests a different topology. With respect to E. canadensis, all phylogenies indicate a monophyletic origin, except for that based on exon sequences of nuclear DNA genes by Knapp et al (2011), which suggests that the G6 genotype is more closely related to E. ortleppi than to the other genotypes of E. canadensis.…”

“…While phylogenies from mtDNA and some nuclear gene sequences show E. ortleppi as a sister group to the genotypes of E. canadensis (Nakao et al, 2007(Nakao et al, , 2013bSaarma et al, 2009), other nuclear phylogenies are unable to resolve the relationship (Knapp et al, 2011). If the genotypes of E. canadensis are not monophyletic, they clearly cannot be regarded as a single evolutionary species, but if we accept the mtDNA phylogeny as a true reconstruction of evolutionary history, then they may be.…”

“…Le et al, 2002;McManus et al, 2002;Obwaller et al, 2004;Lavikainen et al, 2003Lavikainen et al, , 2006Thompson et al, 2006;Nakao et al, 2007Nakao et al, , 2013bHüttner et al, 2008;Moks et al, 2008) and nuclear DNA sequences (e.g. Lavikainen et al, 2003;Bart et al, 2006;Saarma et al, 2009;Knapp et al, 2011). Figures 1 and 2 show the best current estimates of 9 these phylogenies, from studies using a number of different sequences and a complete (or almost complete) range of described genetic variants.…”

Biology and Systematics of Echinococcus

“…These informal groupings were retained for many years but with the advent of molecular characterization they were shown to be genetically distinct (Thompson and McManus, 2001). PCR-based techniques using a variety of genetic loci, and sequencing of nuclear and mitochondrial DNA, coupled with molecular epidemiological studies in endemic areas, confirmed the genetic and morphological distinctness of the host-adapted strains and revealed phylogenetic relationships which support a robust, meaningful taxonomy based on a previously documented nomenclature (Table 2; Bowles et al, 1994;Cruz-Reyes et al, 2007;Harandi et al, 2002;Huttner et al, 2009;Jenkins et al, 2005Lavikainen et al, 2003Moks et al, 2008;Nakao et al, 2013;Pednekar et al, 2009;Romig et al, 2006Romig et al, , 2015Saarma et al, 2009;Thompson et al, 1995Thompson et al, , 2006Thompson, 2001Thompson, , 2008Thompson and McManus, 2002;Tigre et al, 2016). Interestingly, the nomenclature used for these 'species' conforms to that proposed by observational parasitologists in the 1920se60s, before molecular tools were available to confirm and support their morphological descriptions and epidemiological observations Thompson and McManus, 2002;Thompson, 2008).…”

Echinococcus granulosus infection dynamics in livestock of Greece

“…granulosus is characterized by high genetic diversity; ten variants/genotypes (G1-G10) have been reported (Eckert and Thompson 1997). The taxonomy of the genus Echinococcus has been recently revised based on the complete mitochondrial genome (Nakao et al, 2007) and on nuclear data (Saarma et al, 2009). Thus today, E. granulosus is considered as complex consisting of four species: E. granulosus sensu stricto (s.s.) (G1-G3), E. equinus (G4), E. ortleppi (G5), and E. canadensis (G6- The phylogenetic relations within E. canadensis (G6-G10) remain under controversial discussion.…”