Integrative Taxonomy of the Bubble Snails (Cephalaspidea, Heterobranchia) Inhabiting a Promising Study Area: The Coastal Sicilian Faro Lake (Southern Italy)

Abstract

The worldwide diffused bubble snails, Haminoeidae, although characterized by an extreme morphological homogeneity, display the most diverse radiation inside the order Cephalaspidea. This hidden diversity within the family Haminoeidae was recently unraveled by molecular studies, which helped to understand the evolutionary history of this group by clarifying some aspects of its systematics. In fact, the type genus Haminoea W. Turton and Kingston (1830) was proved to be polyphyletic and, consequently, the genus Haminoea sensu stricto was restricted to the Mediterranean, Atlantic and East Pacific species, with the Mediterranean Haminoea hydatis Linnaeus (1758) as the type taxon. However, at the specie rank, many aspects need to be clarified, especially concerning the Mediterranean fauna. Due to low reliability of macro-morphological characters, the minimal quantity of molecular data currently available on Mediterranean specimen adds to the lack of molecular comparison in most reports. Based on such considerations, Haminoea species from an interesting Mediterranean study area, Faro Lake, a Sicilian coastal lake that is considered a hot spot for both alien and endemic marine Heterobranchia, have been studied using an integrative taxonomic approach. Eleven Mediterranean specimens belonging to four Haminoea bubble snails have been collected, identified and compared with samples from other localities, integrating ecological, morphological, anatomical (reproductive apparatus) and molecular data. Based on molecular investigations carried out on three different molecular markers (H3, 16S and COI), the morphological identifications of the species collected in the Faro Lake have been confirmed, and 37 new sequences are provided for future comparisons. Furthermore, results from this integrative systematic study shed light on the phylogenetic relationships occurring in this group of bubble snails that could be useful in identifying valid diagnostic morphological characters. Haminoea hydatis and H. navicula were confirmed to be close to each other, with H. orteai as sister to them and with H. orbignyana as the basal taxon. Given external morphological features are unreliable with species identification in Haminoea genus open questions on the geographical distribution of the species and on their ranges of intraspecific variability have yet to be addressed and further in-depth studies are needed. Finally, the presence of three sympatric Haminoea species, two of which are considered native or long-time naturalized, along with other occasional congeneric species, and the absence of the introduced invasive Haloa japonica, reflects both the resilience and stochastic space-temporal dynamics of Faro Lake. This confirms it as an inexhaustible source of case-studies.