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Understanding the Biogeography of a Group of Earthworms in The Molecular Phylogenetics and Evolution 61 (2011) 125–135 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Understanding the biogeography of a group of earthworms in the Mediterranean basin—The phylogenetic puzzle of Hormogastridae (Clitellata: Oligochaeta) ⇑ Marta Novo a,b, , Ana Almodóvar a, Rosa Fernández a, Gonzalo Giribet b, Darío J. Díaz Cosín a a Departamento de Zoología y Antropología Física, Facultad de Biología, Universidad Complutense de Madrid. C/José Antonio Nováis, 2, 28040 Madrid, Spain b Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA article info abstract Article history: Traditional earthworm taxonomy is hindered due to their anatomical simplicity and the plasticity of the Received 14 December 2010 characteristics often used for diagnosing species. Making phylogenetic inferences based on these charac- Revised 4 April 2011 ters is more than difficult. In this study we use molecular tools to unravel the phylogeny of the clitellate Accepted 29 May 2011 family Hormogastridae. The family includes species of large to mid-sized earthworms distributed almost Available online 13 June 2011 exclusively in the western Mediterranean region where they play an important ecological role. We analyzed individuals from 46 locations spanning the Iberian Peninsula to Corsica and Sardinia, represent- Keywords: ing the four described genera in the family and 20 species. Molecular markers include mitochondrial Mediterranean basin regions of the cytochrome c oxidase subunit I gene (COI), 16S rRNA and tRNAs for Leu, Ala, and Ser, Hormogastridae Earthworms two nuclear ribosomal genes (nearly complete 18S rRNA and a fragment of 28S rRNA) and two nuclear Molecular phylogeny protein-encoding genes (histones H3 and H4). Analyses of the data using different approaches corrobo- Tree calibration rates monophyly of Hormogastridae, but the genus Hormogaster is paraphyletic and Hormogaster pretiosa appears polyphyletic, stressing the need for taxonomic revisionary work in the family. The genus Vignysa could represent an early offshoot in the family, although the relationships with other genera are uncer- tain. The genus Hemigastrodrilus is related to the Hormogaster elisae complex and both are found in the Atlantic drainage of the Iberian Peninsula and France. From a biogeographic perspective Corsica and Sardinia include members of two separate hormogastrid lineages. The species located in Corsica and Northern Sardinia are related to Vignysa, whereas Hormogaster pretiosa pretiosa, from Southern Sardinia, is closely related to the Hormogaster species from the NE Iberian Peninsula. A molecular dating of the tree using the separation of the Sardinian microplate as a calibration point (at 33 MY) and assuming a model of vicariance indicates that the diversification of Hormogastridae may be ancient, ranging from 97 to 67 Ma. Ó 2011 Elsevier Inc. All rights reserved. 1. Introduction requirements and their supposed old age. Bouché (1972) suggested that hormogastrid earthworms were already present in the Iberian The Mediterranean basin is a hotspot of outstanding biodiver- plate in the Late Cretaceous, occupying areas that would coincide sity and should have priority for conservation policies, and mainly with their present distribution. The edge of the Iberian therefore should benefit from biogeographic and evolutionary Plate underwent drastic changes that affected the Betic–Rifean studies (Blondel and Aronson, 1999; Myers et al., 2000). Numerous range, Balearic Islands, Kabylies, Corsica, Sardinia and Calabria studies have centered on the biogeography of circum-Mediterra- (see Magri et al., 2007). It is in all these areas, once forming a nean groups (e.g., Carranza and Arnold, 2003; Santos et al., 2007; primitive Iberian plate, where hormogastrids should be sought Murienne and Giribet, 2009; Ribera et al., 2010), but only a few for in order to understand their evolutionary and biogeographic have focused on earthworms (Annelida, Clitellata, Oligochaeta) relationships. To date, hormogastrids have been discovered in all (Novo et al., 2009, 2010a), a group of terrestrial invertebrates with these regions, with the exception of the Betic and Rif ranges. a great biogeographical potential due to narrow ecological Hormogastridae currently includes 22 species in four genera (plus eight subspecies or varieties) of large to mid-sized (approxi- ⇑ mately 5–90 cm in length) earthworms distributed almost exclu- Corresponding author at: Departamento de Zoología y Antropología Física, sively in the western Mediterranean (Díaz Cosín et al., 1989; Facultad de Biología, Universidad Complutense de Madrid. C/José Antonio Nováis, 2, 28040 Madrid, Spain. Fax: +34 91 394 49 47. Cobolli-Sbordoni et al., 1992) where they play an important E-mail address: [email protected] (M. Novo). ecological role aerating the soil and recycling nutrients (Bouché, 1055-7903/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2011.05.018 126 M. Novo et al. / Molecular Phylogenetics and Evolution 61 (2011) 125–135 1972). Traditionally, earthworm systematics has been based All individuals were washed in distilled water and preserved in principally on morpho-anatomical features (Bouché, 1972; Sims ca. 96% EtOH at À20 °C for subsequent molecular work. A portion and Gerard, 1999). Nevertheless, their taxonomy, and specifically of the integument (ca. 25 mg) was carefully cleaned under a that of hormogastrids has remained unstable and their phyloge- stereomicroscope to remove soil particles and associated fauna. netic relationships are uncertain because of the low number of Subsequently, integument samples were hydrated and preserved characters available for study (Pop et al., 2003; Álvarez, 1977). at À80 °C until DNA extraction. The shape and number of spermathecae have been used as taxonomic characters, but they can vary with developmental stage. 2.2. DNA extraction, gene amplification and sequencing Other characters used in species diagnoses, such as the extension of the clitellum or the developmental degree of tubercula puberta- Total genomic DNA was extracted from a tissue sample from the tis, also show ontogenetic and reproductive differences. Although integument using the DNeasy Tissue Kit (QIAGEN) eluting twice morphology still has an important role for species recognition in with 70 lL of buffer. Molecular markers included mitochondrial re- hormogastrids (Omodeo, 1956; Bouché, 1972; Qiu and Bouché, gions of the cytochrome c oxidase subunit I gene (COI), 16S rRNA 1998), the degree of homoplasy in many characters is high, gene and tRNA Leu, Ala, and Ser, two nuclear ribosomal genes probably reflecting high levels of phenotypic plasticity. (complete 18S rRNA and a fragment of 28S rRNA) and two nuclear In two recent studies, Novo et al. (2009, 2010a) detected high protein-encoding genes (histone H3 and histone H4) (see Table 1 genetic diversity among populations of the Hormogaster elisae for primer information). We also tried amplifying the Internal species complex in the central Iberian Peninsula, as well as be- Transcribed Spacer gene (ITS) in two fragments with the primers: tween this species complex and other hormogastrid species. These 9F: 50–GTA GGT GAA CCT GCG GAA GG–30 (Carranza, 1997) and studies questioned the status of H. elisae as a valid species and 5.8Srev: 50–GCG TTC AAA GAC TCG ATG ATT C–30 for ITS1 and discussed its affinities within the family. In order to re-evaluate 5.8Sfor: 50–GAA TCA TCG AGT CTT TGA ACG C–30 and 28Srev: the status of H. elisae, and to test species and genus delimitations 50–GTT AGT TTC TTT TCC TCC GCT T–30 for ITS2, but only ITS1 in Hormogastridae, we expanded both taxon sampling and the was consistently amplified, and only in two of the populations number of molecular markers and inferred the phylogenetic studied (CER: Hormogaster sp. and GRA: Hormogaster eserana). Only history of the family by using data from nine molecular markers. two nucleotide changes were detected among them. We also used geological events occurring during the evolution of Polymerase chain reactions (PCR) (50 lL) included 0.6 lLof the Mediterranean basin as a calibration point to provide an template DNA, 1 lM of each primer, 200 lM of dNTPs (Invitrogen), estimate of the age of diversification of the family. 1X PCR buffer containing 1.5 mM MgCl2 (Applied Biosystems,) and 1.25 units of AmpliTaq DNA polymerase (Applied Biosystems). DMSO (1 lL) was included for the 28S rRNA reaction. PCR reactions 2. Materials and methods were carried out using a GeneAmp Multicycler Ep gradient (Eppen- dorf), and involved an initial denaturation step (5 min at 95 °C) fol- 2.1. Sampling and morphological study lowed by 35 or 40 cycles including denaturation at 95 °C for 30 s, annealing (ranging from 49 °Cto60°C) for 30 s or 1 min, and Mature individuals, representing 20 of the 22 described species of extension at 72 °C for 1 min, with a final extension step at 72 °C Hormogastridae, were collected from 30 localities in the Iberian Pen- for 7 min. PCR products were resolved by 1% agarose gel electro- insula, France (including Corsica) and Sardinia, including the type phoresis, visualized by ethidium bromide fluorescence and purified locality of each known species. Additional data from the study of using MultiScreen PCR Plates and a Vacuum Manifold (Millipore). Novo et al. (2010a) in Central Spain were included, making for a total The purified products were sequenced directly with the same pri- of 46 localities (Tables S1 and S2, Fig. 1). We included an immature mer pairs used for amplification. Each sequence reaction contained specimen collected near the shore of the Ter river (approximately a total volume of 10 lL including 3 lL of the PCR product, 0.32 lM 9 km from Girona, Spain) that was analyzed for allozymes in Cob- of one of the PCR primer pairs, 0.25 lL of ABI BigDye 5X sequencing olli-Sbordoni et al. (1992), and identified as Hormogaster pretiosa cf. buffer and 0.5 lL of ABI BigDye Terminator (Applied Biosystems).
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