Opening Pandora’s box: Clitellum in phylogeny and taxonomy of earthworms

Abstract

The solution to the current contradictions in earthworm taxonomy and phylogeny is a better understanding of the underlying speciation process. The analysis of size and distribution of clitellar segments and that of tubercula pubertatis in the model homoploid genus Lumbricus provides prima facie evidence for the occurrence of the intra-chromosomal autohomoploid hybridization (autohomoploid hybridization=hybridization without changing the ploidy level and taking place between parents from the same panmictic population). The inferred principal mechanism of the autohomoploid hybridization is an unequal crossing recombining paralogous genes organized in a genomic island of divergence (called here “clitellar genomic island of divergence”, CGID). Since clitellar segments constitute a prezygotic reproduction barrier and seem to correspond to the underlying genes at CGID on a one-to-one basis, their analysis helps to illuminate the underlying speciation process. The inferred characteristic features of the autohomoploid hybridization in earthworms are: (1) Presence of CGID; (2) Generation of quantitative changes in CGID leading to speciation by means of unequal crossing over (= separation of the process leading to speciation from the rest of genome); (3) Regulated distribution of breaking points; (4) Intra-lineage hybridizations, and (5) Homeotic character of the CGID genes. As far as we know, this is the first case of autohomoploid hybridization described in animals. Probably, it is not exaggerated to conclude that many earthworm evolutionary lineages (species) originated in the process of the described autohomploid hybridization in the CGID or in the process of inter-chromosomal duplications leading to polyploidization of the whole genome. We do not deny the possible existence of allopatric speciation in earthworms caused, for example, by established geographic or behavioural (e.g., assortative mating) barriers to inter-population gene flow. The major consequences of ignoring autohomoploid hybrid speciation in lumbricid earthworms (and presumably in other earthworm families as well) in phylogenetic analyses are: (i) Incorrect inference of phylogenies by applying bi-furcating-like phylogenetic analysis instead of reticulate analyses as often seen in the low statistical supports for different clades in constructed bifurcating-like phylogenetic trees and for trees topologies (frequently not even tested). (ii) Misinterpretation of taxonomy and phylogeny by using genetic distance as the sole defining criterion.