The Parvidrilidae - a diversified groundwater family: description of six new species from southern Europe, and clues for its phylogenetic position within Clitellata (Annelida)

Abstract

The Parvidrilidae Erséus, 1999 constitute the most recently described family of oligochaete microdriles. Prior to this study, Parvidrilus strayeri Erséus, 1999, and Parvidrilus spelaeus Martínez‐Ansemil, Sambugar & Giani, 2002, found in groundwaters of the USA (Alabama) and Europe (Slovenia and Italy), respectively, were the only two species in this family. In this paper, six new species –Parvidrilus camachoi, Parvidrilus gianii, Parvidrilus jugeti, Parvidrilus meyssonnieri, Parvidrilus stochi, and Parvidrilus tomasini– and Parvidrilus gineti (Juget, 1959) comb. nov. are added to the family. With all species being stygobiont, the Parvidrilidae is unique in being the only family of oligochaetes worldwide comprising taxa that are restricted to groundwater habitats. Parvidrilids are exceedingly small worms whose principal morphological characteristics are the presence of hair setae in ventral bundles, the markedly posterior position of setae within the segments, the presence of mid‐dorsal glandular pouches in mesosomial segments, the lateral development of the clitellum, the presence of a single male pore in segment XII, and the presence (or absence) of a single spermatheca. The phylogenetic relationships of the Parvidrilidae within the Clitellata were investigated using the nuclear 18S rRNA gene, and the most representative and taxonomically balanced data set of clitellate families available to date. The data were analysed by parsimony, maximum likelihood, and Bayesian inference. Irrespective of the method used, Parvidrilidae were placed far from Capilloventridae, one family once suggested to be closely related to parvidrilids. Although closer to Enchytraeidae than Phreodrilidae, two other suggested putative sister families, the exact position of Parvidrilidae within Clitellata still remained uncertain in the absence of branch support. The examination of reproductive structures, together with the similarity of other important anatomical traits of the new species herein described, reinforced the idea that phreodrilids were the best candidate to be the sister group to parvidrilids on morphological grounds. A fragment of the mitochondrial cytochrome oxidase I gene, used as a barcode, also genetically characterized a few Parvidrilus species. The observation that two species diverge from each other by high genetic distances, even though their type localities are more or less only 100 km apart, is interpreted in the context of low dispersal abilities of inhabitants of the subterranean aquatic ecosystem, and habitat heterogeneity. The Parvidrilidae appear to be a diversified, Holarctic, and probably widely distributed family in groundwater, but very often overlooked because of the small size and external similarity with the polychaete family Aeolosomatidae of its members. © 2012 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 166, 530–558.

Description of ovary organization and oogenesis in a phreodrilid clitellate

“…However, pherodrilids are not thought to be the closest relatives to Enchytraeidae. Additionally, we have no data about ovary/cyst organization in Opistocystidae and Parvidrilidae; taxa that are also regarded as potentially sister to Phreodrilidae (Černosvitov, ; Timm, ; Erséus, ; Martínez‐Ansemil et al, ). At present no specific phylogenetic conclusions can be drawn based on ovary and germ‐line cyst organization and functioning.…”

“…Briefly, most authors (Erséus, Källersjö, Ekman, & Hovmöller, ; Erséus & Källersjö, ; Sjölin, Erséus & Källersjö, ; Envall, Källersjö & Erséus, ; Erséus, Envall, Marchese & Gustavsson, ) found them as sister to a clade consisting of all analyzed Naididae, whereas Rousset, Plaisance, Erséus, Siddall & Rouse () found A. proboscidea at the tree base, with Capilloventer australis sister to A. proboscidea + all other studied Clitellata. Molecular analyses made by Erséus et al () and Martínez‐Ansemil, Creuzé des Châtelliers, Martin & Sambugar () did not support the idea that Phreodrilidae are closely related to Opistocystidae or Parvidrilidae respectively. However, Martínez‐Ansemil et al () presented morphological data (resemblance of the male ducts in some parvidrilids and most phreodrilids) which strengthen the idea that phreodrilids and parvidrilids may in fact be sister groups.…”

“…Molecular analyses made by Erséus et al () and Martínez‐Ansemil, Creuzé des Châtelliers, Martin & Sambugar () did not support the idea that Phreodrilidae are closely related to Opistocystidae or Parvidrilidae respectively. However, Martínez‐Ansemil et al () presented morphological data (resemblance of the male ducts in some parvidrilids and most phreodrilids) which strengthen the idea that phreodrilids and parvidrilids may in fact be sister groups.…”

“…However, pherodrilids are not thought to be the closest relatives to Enchytraeidae. Additionally, we have no data about ovary/cyst organization in Opistocystidae and Parvidrilidae; taxa that are also regarded as potentially sister to Phreodrilidae (Černosvitov, 1936;Timm, 1981;Erséus, 1999;Martínez-Ansemil et al, 2012 Like other microdriles (Jamieson, 1992), I. bifidus produce macrolecithal oocytes. Ultrastructural analysis suggests that yolk synthesis is mixed, that F I G U R E 7 Schematic comparison of cyst organization and functioning in microdrile clitellates analyzed to date.…”

Fauna Europaea: Annelida - Terrestrial Oligochaeta (Enchytraeidae and Megadrili), Aphanoneura and Polychaeta

“…Martinez-Ansemil et al (2012) have removed it from Aeolosomatidae and placed it in Parvidrilidae ( Parvidrilus gineti ) as species inquirenda .…”