Molecular phylogeny and systematics of native North American lumbricid earthworms (Clitellata: Megadrili).

Csaba Csuzdi,Tímea Szederjesi,David Esopi,Chih-Han Chang,Tomás Pavlícek,Katalin Szlávecz,Michael Schubert

doi:10.1371/journal.pone.0181504

Abstract

The family Lumbricidae is arguably the most well-known and well-studied earthworm group due to its dominance in the European earthworm fauna and its invasion in temperate regions worldwide. However, its North American members, especially the genus Bimastos Moore, 1893, are poorly understood. We revised the systematics of the genus Bimastos and tested the hypothesis of the monophyly of North American lumbricids using morphological characters and eight molecular markers. Phylogenetic analyses based on our extensive sampling of Bimastos and inclusion of Dendrodrilus and Allolobophoridella indicated a well-supported clade containing Bimastos and Eisenoides Gates, 1969, and provided the first evidence supporting that North American lumbricids are monophyletic. Assuming the available divergence time estimations and dating of land bridges are correct, it would suggest that the ancestor of this clade arrived North America through Beringia or the De Geer route during Late Cretaceous, and since then the clade has diverged from its Eurasian sister group, Eisenia. The peregrine genera Dendrodrilus and Allolobophoridella are nested within the Bimastos clade; we propose to treat them as junior synonyms of the genus Bimastos, and, contradictory to the commonly held belief of being European, they are indeed part of the indigenous North American earthworm fauna. Morphological characters, such as red-violet pigmentation, proclinate U-shaped nephridial bladders and calciferous diverticula in segment 10 further support this placement. The East Mediterranean–Levantine Spermophorodrilus Bouché, 1975 and Healyella Omodeo & Rota, 1989 are nested within the Dendrobaena sensu lato clade; therefore their close relationship with the North American Bimastos is refuted. Species fit the revised diagnosis of Bimastos are reviewed and keyed, and a new species, Bimastos schwerti sp. nov., is described.

Highlights

Earthworms of the family Lumbricidae are native to the Holarctic
To unravel the phylogenetic relationships among Bimastos, Healyella, Spermophorodrilus, Dendrodrilus and Allolobophoridella, and to test the hypothesis that North American lumbricids are monophyletic, we sampled a total of 14 taxa from the above genera, including two Bimastos species reported in Domınguez et al [21], and both of the known species belonging to the North American native genus Eisenoides (Table 1)
Our phylogenetic analyses showed that the genus Bimastos as revised in this study is monophyletic and includes the former Allolobophoridella eiseni and Dendrodrilus rubidus

Summary

Introduction

Earthworms of the family Lumbricidae are native to the Holarctic. They represent a keystone group of macrofauna in temperate soils, with about 30 common species spread globally by human activity [1]. Taking into account previously overlooked morphological characters, including the shape and orientation of nephridial bladders and the structure and position of calciferous glands, Gates [5] argued that the name Bimastos should be restricted only for North American species. In contrast to Gates’ restricted definition of Bimastos to the Nearctic, Zicsi’s concept of Bimastos encompasses species from North America and from the Balkans and the Anatolia, creating a biogeographic puzzle with questions on how this genus achieved its current native range of distribution

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