Underground evolution: New roots for the old tree of lumbricid earthworms

• First robust phylogeny of the family Lumbricidae (Annelida, Oligochaeta).
• Current Lumbricidae classification and hypotheses of character evolution needs revision.
• Lumbricids emerged in the Lower Cretaceous in the Holarctic region.
• Parthenogenesis arose multiple times in the group.
• Epigeic and anecic earthworms evolved from endogeic ancestors.

Earthworms belonging to the family Lumbricidae are extremely abundant in terrestrial temperate regions. They affect soil properties and nutrient cycling, thus shaping plant community composition and aboveground food webs. Some lumbricids are also model organisms in ecology and toxicology. Despite the intense research efforts dedicated to lumbricids over the last 130 years, the evolutionary relationships and taxonomic classification of these organisms are still subject to great debate. Resolution of their systematics is hampered by the structural simplicity of the earthworm body plan and the existence of cryptic species. We sampled 160 earthworm specimens belonging to 84 lumbricid species (28 genera) and 22 Lumbricoidea outgroups, sequenced two nuclear genes, four mitochondrial genes and seven mitochondrial tRNAs and examined 22 morphological characters. We then applied a combination of phylogenetic methods to generate the first robust genus-level phylogeny of the Lumbricidae. Our results show that the current Lumbricidae classification and the underlying hypotheses of character evolution must be revised. Our chronogram suggests that lumbricids emerged in the Lower Cretaceous in the holarctic region and that their diversification has been driven by tectonic processes (e.g. Laurasia split) and geographical isolation. Our chronogram and character reconstruction analysis reveal that spermathecae number does not follow a gradual pattern of reduction and that parthenogenesis arose from sexual relatives multiple times in the group; the same analysis also indicates that both epigeic and anecic earthworms evolved from endogeic ancestors. These findings emphasize the strong and multiple changes to which morphological and ecological characters are subjected, challenging the hypothesis of character stasis in Lumbricidae.

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