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Molecular Evidence of Intraspecific Variability in Lysidice Ninetta (Polychaeta: Eunicidae) in the Mediterranean Sea

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Molecular Evidence of Intraspecific Variability in Lysidice Ninetta (Polychaeta: Eunicidae) in the Mediterranean Sea Vol. 6: 121–132, 2009 AQUATIC BIOLOGY Printed August 2009 doi: 10.3354/ab00160 Aquat Biol Published online August 4, 2009 OPENPEN ACCESSCCESS Molecular evidence of intraspecific variability in Lysidice ninetta (Polychaeta: Eunicidae) in the Mediterranean Sea Maria Alessandra Iannotta, Maria Cristina Gambi, Francesco Paolo Patti* Laboratory of Functional and Evolutionary Ecology, Stazione Zoologica Anton Dohrn, 8077 Ischia, Napoli, Italy ABSTRACT: A first study of the phylogeography of the polychaete Lysidice ninetta Audouin & Milne- Edwards (Polychaeta: Eunicidae) in the Mediterranean Sea, based on analyses of the molecular mark- ers ITS1 and COI, indicated the occurrence of strong intraspecific variability and possible sibling spe- cies. Here, we report further evidence of the presence of sibling species within L. ninetta, revealed by analysing a new molecular marker (16S rRNA) and supported by preliminary morphological observa- tions. Specimens were collected in association with the seagrass Posidonia oceanica in 6 meadows of the Mediterranean basin; in one of the meadows in which putative siblings co-occurred (Cava meadow off the island of Ischia, Naples, Italy), additional samples were collected for genetic and mor- phological analysis. The mitochondrial region 16S rRNA of 78 specimens revealed 2 haplotypes (nA and nB); morphological characters, associated with these 2 molecular clades were also observed in a sub-set of the analysed specimens of L. ninetta, revealing the presence of 2 morphotypes. The mor- photype termed ‘dark’, characterised by a typical dark colour pattern on the prostomium and first anterior segments, as well as by black aciculae all along the examined body portion, matching quite well with the description of L. ninetta from the Atlantic type locality, corresponded to haplotype nA. The morphotype termed ‘light’, with lighter colouration of the prostomium and first anterior segments, and both black and yellow aciculae on the examined body portion, corresponded to haplotype nB, suggesting the existence of a different species. The hypotheses that can be addressed are the follow- ing: (1) only a single new species (the light morph/genotype) is present, while the dark morph corre- sponds to the original L. ninetta species; (2) both morphs/genotypes (dark and light) are new taxa and need to be fully and properly described; and (3) one or both of the species corresponds to previously described species, synonymised by previous authors as L. ninetta. In all cases there is an urgent need for revision of the genus Lysidice and the nominal species in the Mediterranean Sea basin. This is a complex task far beyond the scope of this work. KEY WORDS: Polychaetes · Eunicidae · 16S rRNA · Mitochondrial DNA · Mediterranean Sea Resale or republication not permitted without written consent of the publisher INTRODUCTION including examples of quite specialized taxa, such as the meiofaunal species (Westheide & Schmidt 2003). In An increasing number of invertebrate species, previ- more recent years, molecular approaches, coupled with ously considered common and/or geographically wide- cladistic analysis, have also shed light on the phyloge- spread, have been identified as ‘siblings’ or species netic relationships among closely related taxa. complexes (Knowlton 1993, Palumbi 1994). Among Often, morphologically very similar species from polychaetes, which represent one of the most speciose relatively distant locations show genetic divergence invertebrate groups and which are widespread in vari- (Schröder & Walsh 2007), while it is less common to de- ous benthic habitats, the number of cryptic species, termine genetic differentiation in taxa sharing a com- since the first ‘classic’ case of the Capitella capitata spe- mon habitat and similar ecological requirements cies complex (Grassle & Grassle 1976), has increased, (Maltagliati et al. 2004, Barluenga et al. 2006). Besides, *Corresponding author. Email: [email protected] © Inter-Research 2009 · www.int-res.com 122 Aquat Biol 6: 121–132, 2009 although few geographical obstacles are faced by presence of sibling species (Iannotta et al. 2007). In the pelagic larvae in the marine realm (Palumbi 1992, present work, a third molecular marker (16S rRNA) has Pechenik 1999), many molecular studies of marine been used to analyse 6 populations from the Mediter- organisms show that genetic divergence may occur at ranean basin. At one of the studied locations where small spatial scales or with minimal morphological such putative siblings co-occurred, the P. oceanica diversifications (Palumbi 1992, Knowlton 1993, 2000, meadow off Ischia (Cava dell’Isola, Naples, Italy), Tarjuelo et al. 2004, Collin 2005, Bleidorn et al. 2006). additional samples were collected in order to perform On the other hand, differences among sibling species preliminary morphological observations. The aim of have often been coupled with differences in life- the present study was to demonstrate the occurrence history traits (e.g. reproductive features, larval devel- of sibling species within L. ninetta and to relate the opment) (Kruse et al. 2003). genetic patterns with distinct morphological features Lysidice ninetta Audouin & Milne Edwards, 1833 that would allow discrimination of potentially different (Polychaeta: Eunicidae) is a polychaete associated with species. In the Mediterranean Sea, various species of various vegetated habitats in the Mediterranean Sea Lysidice have been described (e.g. L. margaritacea (Martin 1987), including Posidonia oceanica meadows, Claparède, 1868), but all of them lack proper formal where the species bores into sheaths (the remains of description and suitable illustration, and were thus former leaf bases persisting along the rhizome) (Gambi synonymised with L. ninetta by Fauvel (1923). In addi- 2000). Eunicida represents one of the higher, morpho- tion, no type material for any of these nominal species logically most well-described clades of polychaetes is available, while the re-description of the type spe- (Struck et al. 2006, Zanol et al. 2007a), but, being an cies for the genus Lysidice (L. ninetta) sampled near order containing 7 recognised families (Eunicidae is the type locality is still in progress (Carrera-Parra et al. one of them) and >900 nominal species in 100 genera 2007 and their unpubl. data). Therefore, the analysis of (Rouse & Pleijel 2006) some uncertainties still persist. the 2 morphotypes described in the present study and Focusing on the taxonomy, phylogeny and ecology of their taxonomic status, with respect to the previous species in the genus Lysidice, data on molecular phy- nominal species, is preliminary and limited; a conclu- logeny have only recently indicated that this genus is sive analysis would require additional material and a paraphyletic with respect to Marphysa and Nicidion, full revision of the genus for the entire Mediterranean. while Nematonereis is nested within the Lysidice This represents a complex task that is far beyond the (Zanol et al. 2007b). In addition, despite the high diver- intended scope of this work. sity of species within the Eunicidae, few data on the reproductive habits of this clade are available, mainly for several species belonging to the genera Palola, MATERIALS AND METHODS Eunice and Marphysa (Wilson 1991, Giangrande 1997) and, only recently, the Lysidice (Gambi & Cigliano Population sampling and morphological observa- 2006). In the Mediterranean Sea, L. ninetta — a warm- tions. Between 2000 and 2007 a total of 78 individuals of temperate and temperate water polychaete (George & Lysidice ninetta were sampled from 6 populations of Hartmann-Schröder 1985, Cantone 1993) — and its co- Posidonia oceanica meadows, distributed among the gener L. collaris — a tropical species and a putative western, central and eastern parts of the Mediterranean migrant from the Red Sea via the Suez canal (Ben- basin (Fig. 1, Table 1). Collection was conducted by Eliahu 1972) — are clearly distinguished by both mor- SCUBA diving and consisted of sampling living ortho- phological (Martin 1987) and molecular data (Iannotta tropous (vertically oriented) shoots of the seagrass et al. 2007). The larvae of L. ninetta can be designated P. oceanica in a depth range of 11 to 28 m and by extract- as Type 1, i.e. warm water, short distance, neritic epi- ing the worms from the leaf sheaths along the rhizomes pelagic, suggesting a pelagic larval stage with limited (Gambi 2000). At one of these study sites, located off dispersal power for the species (Murina 1992, 1997). Ischia (Cava dell’Isola, Tyrrhenian Sea, Naples, Italy) Considering the reproductive biology of L. ninetta in (Fig. 1, Table 1), the 2 possible sibling species co- populations inhabiting Posidonia meadows, the spe- occurred (Iannotta et al. 2007). Therefore, we selected cies shows features that indicate reproduction by this site for additional sampling and also to obtain spec- schizogamy (Gambi & Cigliano 2006) and that are con- imens for the preliminary morphological analyses. sistent with a possible planktotrophic development of Among the 57 individuals collected from this locality, the larvae. Previous genetic results based on both 25 specimens were cut into 2 parts: (1) an anterior sec- mitochondrial (COI) and nuclear (ITS1) data show that tion, including the prostomium and at least the first 30 to L. ninetta is clearly separated from its cogener L. col- 40 segments, was used for morphological observations laris and also show high intraspecific differentiation, and fixed in 4% formalin and
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