Molecular phylogeny of Enchytraeidae (Oligochaeta) indicates separate invasions of the terrestrial environment

Enchytraeidae is a family of soil inhabiting small- to medium-sized oligochaete worms using degradable plant material as a food source and primarily adapted to terrestrial or semi-terrestrial environments. The molecular phylogeny based upon both mitochondrial and nuclear genes indicates early segregations of the two genera Enchytraeus and Lumbricillus leaving the remaining genera included in this study as a later segregated major monophyletic branch. Extant members of the two former genera dominate in decaying seaweed in the littoral zone along the sea although members of in particular the genus Enchytraeus have also invaded other habitats. Historically the littoral zone of the sea is undoubtedly the first terrestrial or semi-terrestrial habitat where dead plant material accumulates to any greater extent and Enchytraeus and Lumbricillus may represent early successful attempts to exploit this resource. Inland soils probably had to await the emergence of land plants in order to provide a similar food resource and here the major branch of enchytraeid genera diversified into a high number of species in the numerous decomposer networks of this varied environment. A subdivision into the genera Enchytraeus and Lumbricillus on the one hand and a branch of mainly inland genera on the other is supported by differences in two somewhat neglected morphological features. Firstly, in Enchytraeus and Lumbricillus the testes are enclosed in a testis sac within which the male cells mature, by one possible exception a unique feature among Oligochaeta, The other enchytraeid genera studied and Oligochaeta in general lack this sac and the male cells mature directly in the cavity of the testicular segment. Secondly, species of Enchytraeus and Lumbricillus generally have a higher reproductive output than species of the inland terrestrial branch and this may represent an adaptation to the unpredictable littoral zone compared to the more stable nature of inland habitats. In the older literature the genus Mesenchytraeus is considered to have a basic position within the entire family but our molecular data do not support this expectation. In Enchytraeidae the nephridia are elaborate organs of a characteristic and constant shape covering species from different genera in a pattern following the molecular phylogeny. Other much used morphological features such as shape of setae, anteclitellar origin of the dorsal vessel and various modifications of the intestine have arisen more than once.