Phylogeny of slug species of the genus Arion: evidence of monophyly of Iberian endemics and of the existence of relict species in Pyrenean refuges

Abstract

The Iberian Peninsula contains the majority of the Paleartic land slug species of the genus Arion, which exhibits diverse taxonomic problems. The present study investigated Arion taxonomy on the basis of analyses of the mitochondrial ND1 gene and nuclear internal transcribed spacer 1 (ITS1) sequences. The Iberian endemic species were monophyletically clustered in two divergent sister clades. The topotype specimens of Arion lusitanicus and the closely related species Arion nobrei and Arion fuligineus, as well as Arion hispanicus and Arion flagellus, were grouped into an ÔAtlanticÕ clade, whereas Arion baeticus, Arion gilvus, Arion anguloi, Arion wiktori and Arion paularensis were included in a ÔContinental-MediterraneanÕ clade. Calibration of mutation rate in the ND1 gene suggested that the divergence of these two clades occurred around the Pliocene-Pleistocene boundary, with subsequent speciation events during the Pleistocene. A group of ancestral and divergent endemic species with distribution centred in the Pyrenean mountain range (Arion molinae, Arion lizarrusti, Arion antrhacius and Arion iratii) arose in the Pliocene and survived through the Pleistocene in geographically confined small populations. Arion lusitanicus showed up to be polyphyletic: specimens, sampled outside the geographic range of the topotype in the north-western Iberian Peninsula, were included in a non-monophyletic clade together with the widely distributed species Arion ater and Arion rufus. The divergent species with a wide European distribution (Arion subfuscus, Arion hortensis, Arion fagophilus and Arion intermedius) were located in basal positions in all topologies. The evolutionary history of these slug species (highly sensitive to climatic factors, with capacity for both outcrossing and selfing, and with low dispersal ability) appears to have been moulded by Pliocene-Pleistocene climate events and by the rugged topography of southern Europe, giving rise to repeated cycles of population isolation during periods of glaciation alternating with interglacial expansions limited by geographic barriers.

Towards the unravelling of the slug <i>A. ater–A. rufus</i> complex (Gastropoda Arionidae): new genetic approaches

“…In this way our results shed light on discussions about these taxa being considered different morphological forms (Quinteiro et al, 2005), subspecies (Evans, 1986) or species (Bank et al, 2007) because of their very similar morphological characteristics. Our results also highlight the usefulness of the mPTP species delimitation software in difficult cases such as the A. ater-A.…”

“…For example, A. ater is in general black coloured and A. rufus is orange, while another species of the genus (A. vulgaris) is brown; thus specimens of dark brown can be misidentified (Roth et al, 2012), although the morphology of their genitalia separates clearly these species (Hatteland et al, 2015). Genetically, their phylogenetic relationships were initially not clear and they were even proposed to be eco-types (Quinteiro et al, 2005), but more recently it has been suggested that A. ater and A. rufus are probably independent monophyletic clades (Rowson et al, 2014). But the fact remains that they belong to different phylogenetic clades and does not establish that they are actually different species.…”

Locomotor activity of two sympatric slugs: implications for the invasion success of terrestrial invertebrates

“…Arion rufus is ecologically and morphologically similar to A. lusitanicus. The two species are only unambiguously distinguishable from each other by genetic means or by differences in the color patterns during juvenile stages (Bogon 1990, Quinteiro et al 2005). …”

Floral herbivory of an invasive slug on a native weed

“…Arion lusitanicus (= Arion vulgaris Moquin-Tandon) is a west European species probably originating from the north of the Iberian Peninsula (Quintero et al 2005). It spread throughout Europe and became established in the Czech Republic in 1991 (Horsák & Dvořák 2003).…”