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Molecular Phylogenetics and Systematic Revision of the South-Eastern Australian Helicario- Nidae (Gastropoda, Stylommatophora)

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Molecular Phylogenetics and Systematic Revision of the South-Eastern Australian Helicario- Nidae (Gastropoda, Stylommatophora) Contributions to Zoology, 86 (1) 51-95 (2017) Molecular phylogenetics and systematic revision of the south-eastern Australian Helicario- nidae (Gastropoda, Stylommatophora) Isabel T. Hyman1, Irantzu de la Iglesia Lamborena1, Frank Köhler1, 2 1 Australian Museum, 1 William St, Sydney NSW 2010, Australia 2 E-mail: [email protected] Key words: Helicarionoidea, land snail, mitochondrial DNA, morphology, taxonomy Abstract Significance of morphological and mitochondrial characters in species delimitation ....................................... 63 The south-eastern Australian helicarionid clade currently Species distributions ............................................................... 64 comprises six genera of snails and semislugs united by genital Acknowledgements ........................................................................ 64 characters, including an epiphallic flagellum that produces a References ........................................................................................ 64 spiraling, spinose spermatophore, the absence of an epiphallic Appendix .......................................................................................... 67 caecum, and the presence of at most a very short vagina. We comprehensively revise the taxonomy of this group based on comparative analyses of key morphological features and mito- Introduction chondrial markers COI and 16S, revise the placement of several species described recently on the basis of shell morphology The Helicarionidae is a group of land snails in which alone, and describe new taxa. The snail genus Brevisentis is shell reduction, or limacisation, appears to have evolved monophyletic as currently understood, but includes an additional undescribed species from Wollemi National Park, New South repeatedly (Hyman et al., 2007). As a result this group Wales. Mysticarion is shown to contain four arboreal semislugs harbours a wide range of morphological diversity, and with wide, disjunct ranges, including one new species (Mysti- includes snails with a full shell as well as semislugs, carion obscurior sp. nov.). We synonymise Fastosarion staf- animals with a reduced, ear-shaped shell into which fordorum with Mysticarion hyalinus. The semislug Desidarion they cannot fully retract. The shells of all species, both is synonymised with Parmavitrina, and we describe two new species of this genus, P. flavocarinata sp. nov. and P. maculosa snails and semislugs, are thin and glossy with reduced sp. nov. The semi-arboreal semislug Cucullarion is herein in- sculpture. Early species descriptions were primarily cluded in the south-eastern Australian helicarionid clade based based on shells (e.g., Pfeiffer, 1849, 1850, 1852, 1853; on morphological and genetic evidence, despite its more north- Cox, 1864, 1868, 1871, 1873; Brazier, 1875a, 1875b, erly distribution. Two small semislugs so far placed in Pelopa- 1876b), as was the taxonomic framework put together rion do not group together and a new genus, Ubiquitarion gen. nov., is described for Peloparion iridis. All of these genera, to- in a series of papers by Iredale (1933, 1937a, 1937b, gether with the semislug Helicarion (not included here), form a 1941, 1942), which included descriptions of 19 new, monophyletic radiation endemic to southeastern Australia. mostly monotypic genera. Subsequently, a number of small-scale anatomical investigations into single gen- era or species were published (Dartnall and Kershaw, Contents 1978; Kershaw, 1979, 1981, 1982, 1988; Stanisic, 1993a, 1993b; Scott, 1995), but the underlying taxonomy es- Introduction ...................................................................................... 51 sentially remained unchanged. More recently, a more Material and methods .................................................................... 52 comprehensive overview of Australian Helicarionidae Material ...................................................................................... 52 Morphological studies ............................................................ 52 was undertaken by Hyman and co-authors (Hyman, Molecular studies and phylogenetic analyses .................. 53 2007; Hyman et al., 2007; Hyman and Ponder, 2010, Species identification and delineation ................................ 53 2016) utilizing both morphological data and mitochon- Results ............................................................................................... 54 drial DNA sequences. These studies resulted in the Comparative morphology ...................................................... 54 addition of several new species and genera as well as Molecular analyses .................................................................. 56 Discussion ......................................................................................... 61 evidence to support the monophyly of some smaller Phylogenetic relationships and genus-level taxonomy .... 61 subgroups among the Australian Helicarionidae. How- Systematic significance of reproductive characteristics 62 ever, only around a quarter of Australia’s estimated Downloaded from Brill.com10/10/2021 07:13:38PM via free access 52 Hyman et al. – South-eastern Australian Helicarionidae 150 described species was included in these studies, 2010). While the relationships among the Helicarioni- with a high proportion from New South Wales (NSW), dae are in general poorly understood, this southeastern leaving the taxonomic structure of the entire group Australian clade, comprising the genera Helicarion still unclear. Stanisic et al. (2010) documented the Férussac, 1821, Mysticarion Iredale, 1941, Desidarion basic shell morphology and distributions of the NSW Iredale, 1941, Parmavitrina Iredale, 1937, Peloparion and Queensland (Qld) helicarionids and described 47 Iredale, 1937 and Brevisentis Hyman, 2007, groups to- new species and 15 new genera based exclusively on gether with strong support based on both morphology their shell. This has raised the number of described and on mitochondrial phylogeny (Hyman et al., 2007; species in Australia to 102. However, for more than Hyman and Ponder, 2010). The southernmost genus, half of these no anatomical data are known and their Helicarion, is found from Tasmania to central NSW phylogenetic relationships have essentially remained and will be the subject of a future paper. The remaining unresolved. five currently recognized genera and one additional Numerous studies in Australian land snail groups, genus, Cucullarion Stanisic, 1998, including the such as the Camaenidae, have revealed the presence of fourteen species they contain, form the subject of this both widespread conservatism in shell morphology, revision. and in other cases, high levels of convergence (Stan- Anatomical data are available for eight species kowski, 2011; Criscione and Köhler, 2013a; Köhler and (Stanisic, 1998; Hyman, 2007; Hyman and Ponder, Criscione, 2015). Shell characters, such as shape, size 2010); however, the remaining six species, some of and colour, appear to be closely linked to the adapta- which were recently described by Stanisic et al. (2010), tion to different habitat types, and therefore may be are known only by their shell morphology. For several constrained by environment or lifestyle rather than by of these species a single specimen has been sequenced shared ancestry. Hence, these characters cannot reliably previously (COI and 16S; Hyman et al., 2007), for a be used as a sole basis for a phylogenetic classification. phylogenetic study that was not concerned with re- There is evidence that shell reduction has evolved sev- solving the species-level taxonomy. Herein, we com- eral times in the Helicarionidae (Hyman et al., 2007). prehensively revise the taxonomy relationships of these As well as casting further doubt on the reliability of six helicarionid genera from southeastern Australia shell morphology in this group, this convergence in based on comparative examination of the anatomy and shell and body shape suggests that care must also be morphology of all described species and some cur- taken with the examination of anatomical characters, rently undescribed candidate taxa as well as analyses which are usually accepted as more reliable than shell of partial sequences of the mitochondrial genes cy- morphology. During the process of limacisation, the tochrome c oxidase subunit I (COI) and 16S rRNA size of the pallial cavity is reduced and some repro- (16S) that sought to estimate the amounts of mitochon- ductive and digestive organs are moved into the foot. drial differentiation within and between species and to This can lead to convergence in anatomical characters; resolve their phylogenetic relationships. for example, many semislugs have developed an addi- tional oesophageal crop, which is not present in snails (Tillier, 1984; Hyman and Ponder, 2010). The need to Material and methods fit reproductive organs into a reduced space may also lead to convergence in genital morphology. For this Material reason, the use of molecular data, which already under- pins much of modern taxonomy, is crucial to reliably This study is based on the examination of ethanol-pre- resolve the systematic relationships among helicario- served specimens and supplementary dry material nids. from the Australian Museum (AM), the Queensland The majority of Australian species live in rainforest Museum (QM) and Museum Victoria (MV), including habitats along the eastern coast. Although this group’s freshly collected material from eastern NSW and highest
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