The making of a (soil) star: phylogenetic relationships of the genus Lumbricus with insight into its evolution and biogeography

Abstract

The widely distributed earthworm genus Lumbricus exhibits significant ecological and morphological diversity, playing essential roles in soil ecosystems. This study presents a comprehensive molecular phylogeny of the genus, incorporating eighteen taxa and four mitochondrial and anuclear marker. The aim was to clarify the phylogenetic relationships within Lumbricus and examine the evolutionary trajectory of bioturbation behaviour and geographic origins.

Phylogenetic analyses revealed three major clades within Lumbricus, with Lumbricus baicalensis emerging as the earliest branching species. Evolutionary relationships suggested that the common ancestor of the genus was an epigeic litter dweller, with epi-anecic traits appearing later in their evolutionary history. Ancestral area reconstruction indicated that the genus originated in France and Central Europe, aligning with previous hypotheses of an Alpine origin. Molecular phylogenetics reinforced the monophyly of the genus, confirming the species status of previously unassessed taxa, such as Lumbricus meliboeus and Lumbricus polyphemus. Additionally, high genetic divergence was found between some infraspecific taxa, suggesting that Lumbricus castaneus var. disjunctus and Lumbricus rubellus castaneoides may represent pseudocryptic species. Previous hypotheses about the giant endemic species Lumbricus badensis evolving from a common ancestor with Lumbricus friendi around the Last Glacial Maximum were not supported by our results.

These findings contributed an evolutionary and biogeographic background to understand the current ecology and distribution of invasive Lumbricus species such as Lumbricus terrestris or Lumbricus castaneus, potentially opening the way to improved management of these impactful species.