Eurotatorian paraphyly: Revisiting phylogenetic relationships based on the complete mitochondrial genome sequence of Rotaria rotatoria (Bdelloidea: Rotifera: Syndermata)

Abstract

BackgroundThe Syndermata (Rotifera+Acanthocephala) is one of the best model systems for studying the evolutionary origins and persistence of different life styles because it contains a series of lineage-specific life histories: Monogononta (cyclic parthenogenetic and free-living), Bdelloidea (entirely parthenogenetic and mostly benthic dweller), Seisonidea (exclusively bisexual and epizoic or ectoparasitic), and Acanthocephala (sexual and obligatory endoparasitic). Providing phylogenetic resolution to the question of Eurotatoria (Monogononta and Bdelloidea) monophyly versus paraphyly is a key factor for better understanding the evolution of different life styles, yet this matter is not clearly resolved. In this study, we revisited this issue based on comparative analysis of complete mitochondrial genome information for major groups of the Syndermata.ResultsWe determined the first complete mitochondrial genome sequences (15,319 bp) of a bdelloid rotifer, Rotaria rotatoria. In order to examine the validity of Eurotatoria (Monogononta and Bdelloidea) monophyly/paraphyly, we performed phylogenetic analysis of amino acid sequences for eleven protein-coding genes sampled from a wide variety of bilaterian representatives. The resulting mitochondrial genome trees, inferred using different algorithms, consistently failed to recover Monogononta and Bdelloidea as monophyletic, but instead identified them as a paraphyletic assemblage. Bdelloidea (as represented by R. rotatoria) shares most common ancestry with Acanthocephala (as represented by L. thecatus) rather than with monogonont B. plicatilis, the other representative of Eurotatoria.ConclusionComparisons of inferred amino acid sequence and gene arrangement patterns with those of other metazoan mtDNAs (including those of acanthocephalan L. thecatus and monogonont B. plicatilis) support the hypothesis that Bdelloidea shares most common ancestry with Acanthocephala rather than with Monogononta. From this finding, we suggest that the obligatory asexuality of bdelloideans may have secondarily derived from some other preexisting condition in earlier lineage of rotifers. Providing a more complete assessment of phylogenetic relationships and inferring patterns of evolution of different types of life styles among Syndermata awaits comparisons requiring mitochondrial genome sequencing of Seisonidea.

The complete mitochondrial genome of Pallisentis celatus (Acanthocephala) with phylogenetic analysis of acanthocephalans and rotifers

“…in addition, the monophyly of Ecdysozoa was supported (1.00 BPP), which is a sister clade to lophotrochozoa with high supporting value (1.00 BPP), as reported by other authors (Dunn et al 2008, Min andPark 2009). However, further phylogenetic research should include more taxa in order to resolve phylogenetic relationship among acanthocephalans and rotifers and in-between.…”

“…it appears certain that acanthocephalans are closely related with bdelloids and that they together form a clade with high support value, which then correlates with another group, monogononts in rotifers. this relationship has been supported by analyses using other molecular markers, such as 16s rrNA, 18s rrNA and 28s rrNA (garey et al 1998, garcía-Varela and Nadler 2006, Witek et al 2008, and using mt genes and/or genomes (steinauer et al 2005, Min and Park 2009, Fontaneto and Jondelius 2011, gazi et al 2012, Weber et al 2013. Using also mt genomes, Podsiadlowski et al (2009) included only one species of acanthocephalan (listed as the genus Leptorhynchoides) and a monogonont (Brachionus) in the phylogenetic analysis of lophotrochozoans, but phylogenetic relationship in the syndermata was not even dealt with in their research.…”

“…it is thus indicated that mt genomes in acanthocephalans show certain degree of conservation at least in the gene content and gene order. importantly, with the release of mt genome information from a few species of rotifers (suga et al 2008, Min and Park 2009, lasek-Nesselquist 2012, Weber et al 2013, it becomes possible to analyze the relationship between acanthocephalans and rotifers. Due to the unavailability of some genes in the mt genome of rotifers (lasek-Nesselquist 2012), 9 protein-coding genes were used in the present phylogenetic analysis.…”

Differences in life history characteristics among three sympatric evolutionary species of theRotaria rotatoriacomplex

“…Rotifera is one of the best model organisms for investigating the evolutionary origins and persistence of different life styles because it contains a series of species-specific life histories (Min & Park 2009). …”

Classification of the Acanthocephala

“…their data are consistent with the data contained in numerous related studies based on rNA analysis. For instance, Min and Park (2009) linked the syndermata with the Platyhelminthes as the Platyzoa.…”