The disjunct distribution of relict earthworm genera clarifies the early historical biogeography of the Lumbricidae (Crassiclitellata, Annelida)

Abstract

The historical biogeography of the Lumbricidae, the main Palearctic earthworm family, may be linked to the paleogeography of their putative ancestral range in Iberia–southeastern France–Corsica–Sardinia. Although molecular phylogenetics has recently been used to analyze most endemic genera in this area, the genus Kritodrilus has not yet been studied. The generotype Kritodrilus calarensis and other closely related species inhabit southeastern France. However, other species from the Iberian Peninsula (e.g., Kr. osellai) have been assigned to Kritodrilus, the same for the Vindobonic (Hungarian–Austrian–Czech–Slovakian) Dendrobaena mrazeki. In order to unravel the paleobiogeographic, evolutionary, and taxonomic significance of Kritodrilus, the aforementioned species (and three potential relatives) were sequenced for seven molecular markers. Molecular phylogenetic inference recovered a clade of French Kritodrilus (including Et. setusmontanus) closely related to the Northwestern Iberian Galiciandrilus and Compostelandrilus, the latter being a sister clade to the Vindobonic species (described as a new genus). Time‐calibrated phylogenetic inference estimated that these three clades diverged around 55 Ma. Ecological niche models for these clades were mainly influenced by the same environmental variables, but showed non‐overlapping highly suitable areas (except for Kritodrilus). Ancestral area reconstruction inferred the origin of the Lumbricidae in Corsica–Sardinia and the Iberian Peninsula, with eventual expansion eastwards toward France, Central Europe, and the Carpato‐Balkanic area. For Kritodrilus and its relatives, this expansion may have been contemporaneous with the Paleocene–Eocene thermal maximum. Later climatic changes may explain the strikingly disjunct ranges. This work highlights the evolutionary and biogeographic significance of these isolated earthworm lineages and the importance of their preservation.

Evaluating the Conservation Status of a North-Western Iberian Earthworm (Compostelandrilus cyaneus) with Insight into Its Genetic Diversity and Ecological Preferences

“…In addition, these terranes, which constituted a continuous landmass from the Cretaceous to the Oligocene-Miocene [ 26 ], have been suggested to be the center of origin of both sister families due to the presence of several early-branching genera [ 27 , 28 ]. Two of these genera, Galiciandrilus Domínguez, Aira, Porto, Díaz Cosín & Pérez-Losada 2017 and Compostelandrilus Domínguez, Aira, Porto, Díaz Cosín & Pérez-Losada 2017, are isolated in the NW Iberian Peninsula but appear to be closely related to Kritodrilus Bouché 1972 and Vindoboscolex Marchán 2021 in a surprisingly disjunct distribution [ 29 ]. This suggests that these taxa are relics of a formerly widely distributed lineage whose range may have contracted due to climate changes or replacement by other earthworm genera.…”

First molecular evidence of hybridization in endosymbiotic ciliates (Protista, Ciliophora)

“…The evolution of lumbricid earthworms has been largely driven by paleoclimatic and paleogeographic events (e.g., Pérez-Losada et al, 2011 ; Fernández et al, 2013 ; Domínguez et al, 2015 ; James et al, 2021 ). Central Europe is the ancestral area for a large portion of known lumbricid genera, whose diversification was very likely shaped by range expansion and retraction due to global climatic changes from the Paleocene–Eocene epochs to the Pleistocene ( Marchán et al, 2021 ). Both epigeic and anecic earthworms evolved multiple times from endogeic ancestors, which suggests subsoil-dwelling, temporary and horizontally oriented burrow systems, and geophagy (feeding on soil) to represent the ground pattern of lumbricid earthworms ( Domínguez et al, 2015 ).…”

Perspectives in Earthworm Molecular Phylogeny: Recent Advances in Lumbricoidea and Standing Questions

“…These three genera have been recently found to be related to Kritodrilus (Bouche 1972) (whose type species was included in molecular analyses for the first time (Marchán et al 2021a)) and surprisingly, to the newly described Central European genus Vindoboscolex [48]. The unlikely phylogenetic relationship of those isolated genera has provided some new insight into the early evolution of the Lumbricidae; an early branching clade would have occupied a wide area ranging from Galicia to Hungary and, subsequently, been fragmented into relict, geographically restricted clades.…”

“…Paleogeographic events and their correlation with splits between sister taxa have been implemented as an alternative to fossils [44,45], yet this approach has been criticized as relying on the assumption of vicariance; divergence between taxa being older than the paleogeographic event cannot be ruled out, resulting in divergence time estimation that are in practice only a minimum estimate. External substitution rates (obtained from previous analyses) should be used with caution as substitution rates for the same gene change between taxa even within the same family [22]; they often come from vicariance-based analyses [46] but they have also been obtained from more robust fossil-based analyses [47,48].…”

“…Likewise, the formation of the Mediterranean Sea and the uplift of the Pyrenees and the Alps appear to have been key for the diversification of Hormogastridae and Lumbricidae. The origin of both can be found in the terrane, which consisted in the Northeastern Iberian Peninsula, Southern France, Corsica, and Sardinia [48,70]. Their latter eastward expansion, which led to the vast diversification of genera such as Dendrobaena, Eisenia, or Octodrilus, as well as the colonization of North America by the genera Eisenoides (Gates 1969) and Bimastos are comparatively poorly understood.…”