Systematic revision of the microcystid land snails endemic to Norfolk Island (Gastropoda: Stylommatophora) based on comparative morpho-anatomy and mitochondrial phylogenetics
Isabel T. Hyman A * , Jennifer Caiza A and Frank Köhler AA Australian Museum, 1 William Street, Sydney, NSW 2010, Australia.
Invertebrate Systematics 37(6) 334-443 https://doi.org/10.1071/IS22049
Submitted: 16 September 2022 Accepted: 27 April 2023 Published: 15 June 2023
Abstract
Norfolk Island harbours a rich land snail diversity dominated by the Microcystidae and Helicarionidae that are currently represented by 10 endemic genera and 27 accepted species and subspecies. We comprehensively revise the taxonomy of these taxa using comparative morphology and phylogenetic analyses of the mitochondrial genes COI and 16S. We demonstrate that most ‘helicarionid’ species belong to Microcystidae with only a single species of Helicarionidae present (Dendrolamellaria mathewsi). The Norfolk Island microcystids comprise five major clades. These clades may have independently colonised the Norfolk Island group; however, clarity may only be achieved in a broader phylogenetic context that incorporates the study of extralimital groups. Three clades have radiated in situ into multiple endemic species. Based on our findings, we recognise the previously accepted genera Iredaleoconcha, Nancibella and Roybellia as junior synonyms of Allenoconcha, and Mathewsoconcha and Quintalia as junior synonyms of Advena, based on the close phylogenetic relationships. Furthermore, we confirm the previous treatment of Lutilodix, Parcolena and Dolapex as junior synonyms of Fanulena and Belloconcha as a synonym of Advena, bringing the total number of Norfolk Island microcystid genera to five. Secondly, we provide revised descriptions for each of these genera. Thirdly, we remove Allenoconcha belli, A. mathewsi, A. monspittensis, A. perdepressa and A. royana from the synonymy with Allenoconcha basispiralis. We also remove Helix patescens from synonymy with Quintalia flosculus, treating this as a member of Allenoconcha, and resurrect Advena campbellii nepeanensis and Quintalia stoddartii intermedia as accepted subspecies. Based on comparative morpho-anatomy, we treat Allenoconcha mathewsi and A. monspittensis as junior synonyms of Allenoconcha royana, A. inopina as a junior synonym of Allenoconcha caloraphe, Fanulena fraternus as a junior synonym of F. amiculus, Advena campbellii charon as a synonym of Advena campbellii campbellii, Mathewsoconcha belli, M. compacta and M. norfolkensis as junior synonyms of Advena suteri, M. elevata as a junior synonym of Advena grayi, and M. microstriatum as a junior synonym of Advena phillipii. Lastly, we describe three new species, Allenoconcha evansorum sp. nov., A. margaretae sp. nov. and A. varmani sp. nov. In summary, we accept 27 microcystid species and subspecies all of which are endemic to the Norfolk Island group. We provide recent and historical distribution data for each species and demonstrate that seven species or subspecies are probably extinct. All species are well differentiated in terms of basal branch lengths in the phylogenetic tree, but this distinction is not consistently reflected in the external morphology. Some closely related sister-taxa are very similar in shell morphology whereas others exhibit highly distinctive shells. We hypothesise that these stark differences in shell morphology may result from adaptation to different ecological niches, yet we currently lack a detailed understanding of the underlying evolutionary mechanisms.
ZooBank: urn:lsid:zoobank.org:pub:BEFC0F76-4405-4EE7-9060-B7D9FB84BCB1
Keywords: Euconulidae, Helicarionidae, island radiation, morphology, Pulmonata, speciation, systematics, taxonomy, Trochomorphoidea.
References
Baker HB (1938) Zonitid snails from Pacific Islands, Part 1. Southern genera of Microcystinae. Bernice P. Bishop Museum Bulletin 158, 3-102.
| Google Scholar |
Baker HB (1940) Zonitid snails from Pacific Islands, Part 2. Hawaiian genera of Microcystinae. Bernice P. Bishop Museum Bulletin 165, 105-201.
| Google Scholar |
Baker HB (1941a) Zonitid snails from Pacific Islands, Part 3. Genera other than Microcystinae. Bernice P. Bishop Museum Bulletin 166, 205-346.
| Google Scholar |
Baker HB (1941b) Zonitid snails from Pacific Islands, Part 4. Distribution and indexes. Bernice P. Bishop Museum Bulletin 166, 347-370.
| Google Scholar |
Bouchet P, Rocroi J-P, Hausdorf B, Kaim A, Kano Y, Nützel A, Parkhaev P, Schrödl M, Strong EE (2017) Revised classification, nomenclator and typification of gastropod and monoplacophoran families. Malacologia 61(1-2), 1-526.
| Crossref | Google Scholar |
Burns KC (2022) The paradox of island evolution. Journal of Biogeography 49, 248-253.
| Crossref | Google Scholar |
Chiba S (1999) Accelerated evolution of land snails Mandarina in the oceanic Bonin Islands: evidence from mitochondrial DNA sequences. Evolution 53, 460-471.
| Crossref | Google Scholar |
Chiba S (2004) Ecological and morphological patterns in communities of land snails of the genus Mandarina from the Bonin Islands. Journal of Evolutionary Biology 17, 131-143.
| Crossref | Google Scholar |
Chiba S, Cowie RH (2016) Evolution and extinction of land snails on oceanic islands. Annual Review of Ecology, Evolution and Systematics 47, 123-141.
| Crossref | Google Scholar |
Chiba S, Davison A (2007) Shell shape and habitat use in the North-West Pacific land snail Mandarina polita from Hahajima, Ogasawara: current adaptation or ghost of species past? Biological Journal of the Linnean Society 91, 149-159.
| Crossref | Google Scholar |
Cowie RH (2001) Invertebrate invasions on Pacific islands and the replacement of unique native faunas: a synthesis of the land and freshwater snails. Biological Invasions 3, 119-136.
| Crossref | Google Scholar |
Cox JC (1866a) 8. Descriptions of seven new species of Australian land-shells. Proceedings of the Zoological Society of London 1865, 695-697.
| Crossref | Google Scholar |
Cox JC (1866b) Description d’espèces nouvelles provenant d’Australie et des îles Solomon et Norfolk. [Description of new species from Australia and the Solomon and Norfolk Islands.]. Journal de Conchyliologie 14, 45-48 [In French].
| Google Scholar |
Cox JC (1870) Descriptions of seventeen new species of land shells from the South Sea Islands in the cabinet of Mr John Brazier of Sydney. Proceedings of the Zoological Society of London 1870, 81-85.
| Google Scholar |
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294-299.
| Google Scholar |
Goodacre SL (2001) Genetic variation in a Pacific Island land snail: population history versus current drift and selection. Proceedings of the Royal Society of London – B. Biological Sciences 268, 121-126.
| Crossref | Google Scholar |
Goodfriend GA (1986) Variation in land-snail shell form and size and its causes: a review. Systematic Biology 35(2), 204-223.
| Crossref | Google Scholar |
Gray JE (1834) Characters of new species of shells. Proceedings of the Zoological Society of London 1834, 63-68.
| Google Scholar |
Greve C, Gimnich F, Hutterer R, Misof B, Haase M (2012) Radiating on oceanic islands: patterns and processes of speciation in the land snail genus Theba (Risso 1826). PLoS One 7(4), e34339.
| Crossref | Google Scholar |
Gude GK (1913) Definitions of further new genera of Zonitidæ. Proceedings of the Malacological Society of London 10, 389-391.
| Crossref | Google Scholar |
Hausdorf B (1998) Phylogeny of the Limacoidea sensu lato (Gastropoda: Stylommatophora). Journal of Molluscan Studies 64(1), 35-66.
| Crossref | Google Scholar |
Hirano T, Kameda Y, Kimura K, Chiba S (2014) Substantial incongruence among the morphology, taxonomy, and molecular phylogeny of the land snails Aegista, Landouria, Trishoplita, and Pseudobuliminus (Pulmonata: Bradybaenidae) occurring in East Asia. Molecular Phylogenetics and Evolution 70, 171-181.
| Crossref | Google Scholar |
Hirano T, Kameda Y, Kimura K, Chiba S (2015) Divergence in the shell morphology of the land snail genus Aegista (Pulmonata: Bradybaenidae) under phylogenetic constraints. Biological Journal of the Linnean Society 114, 229-241.
| Crossref | Google Scholar |
Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS (2017) UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35(2), 518-522.
| Crossref | Google Scholar |
Hyman IT, Köhler F (2018) Reconciling comparative anatomy and mitochondrial phylogenetics in revising species limits in the Australian semislug Helicarion Férussac, 1821 (Gastropoda: Stylommatophora). Zoological Journal of the Linnean Society 184, 933-968.
| Crossref | Google Scholar |
Hyman IT, Köhler F (2019) Phylogeny and systematic revision of the helicarionid semislugs of eastern Queensland (Stylommatophora, Helicarionidae). Contributions to Zoology 88(4), 351-451.
| Crossref | Google Scholar |
Hyman IT, Köhler F (2020a) Feeling sluggish: the extreme semislugs of Australia (Stylommatophora, Helicarionidae). Journal of Zoological Systematics and Evolutionary Research 58(4), 1021-1057.
| Crossref | Google Scholar |
Hyman IT, Ponder WF (2010) A morphological phylogenetic analysis and generic revision of Australian Helicarionidae (Gastropoda: Pulmonata: Stylommatophora), and an assessment of the relationships of the family. Zootaxa 2462, 1-148.
| Crossref | Google Scholar |
Hyman IT, Ponder WF (2016) Helicarionidae (Gastropoda: Heterobranchia: Stylommatophora) of Lord Howe Island. Molluscan Research 36(2), 84-107.
| Crossref | Google Scholar |
Hyman IT, Ho SYW, Jermiin LS (2007) Molecular phylogeny of Australian Helicarionidae, Euconulidae and related groups (Gastropoda: Pulmonata: Stylommatophora) based on mitochondrial DNA. Molecular Phylogenetics and Evolution 45, 792-812.
| Crossref | Google Scholar |
Hyman IT, de la Iglesia Lamborena I, Köhler F (2017) Molecular phylogenetics and systematic revision of the south-eastern Australian Helicarionidae (Gastropoda, Stylommatophora). Contributions to Zoology 86(1), 51-95.
| Crossref | Google Scholar |
Hyman IT, Caiza J, Köhler F (2023) Dissecting an island radiation: systematic revision of endemic land snails on Lord Howe Island (Gastropoda, Stylommatophora, Microcystidae). Zoological Journal of the Linnean Society 197, 20-75.
| Crossref | Google Scholar |
Invasive Species Council and TierraMar (2021) The Native Plant Communities of Norfolk Island. (Invasive Species Council: Katoomba, NSW, Australia) Available at http://www.norfolkisland.gov.nf/sites/default/files/Report-Plant%20Communities%20of%20Norfolk%20Island-2021.pdf
Iredale T (1913) The land Mollusca of the Kermadec Islands. Proceedings of the Malacological Society of London 10(6), 364-388.
| Crossref | Google Scholar |
Iredale T (1915) Art. XLVIII.—A comparison of the land molluscan faunas of the Kermadec Group and Norfolk Island. Transactions and Proceedings of the New Zealand Institute 47, 498-508.
| Google Scholar |
Iredale T (1945) The land Mollusca of Norfolk Island. Australian Zoologist 11, 46-71.
| Google Scholar |
Jones JG, McDougall I (1973) Geological history of Norfolk and Philip Islands, southwest Pacific Ocean. Journal of the Geological Society of Australia 20(3), 239-254.
| Crossref | Google Scholar |
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14(6), 587-589.
| Crossref | Google Scholar |
Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30(14), 3059-3066.
| Crossref | Google Scholar |
Kisel Y, Barraclough TG (2010) Speciation has a spatial scale that depends on levels of gene flow. The American Naturalist 175(3), 316-334.
| Crossref | Google Scholar |
Köhler F, Bouchet P (2020) On unavailable genus-group names introduced by Tom Iredale for Australian non-marine gastropods: nomenclatural clarifications and descriptions of new genera. Molluscan Research 40, 150-159.
| Crossref | Google Scholar |
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870-1874.
| Crossref | Google Scholar |
MacArthur RH, Wilson EO (1963) An equilibrium theory of insular zoogeography. Evolution 17(4), 373-387.
| Crossref | Google Scholar |
Millien V (2006) Morphological evolution is accelerated among island mammals. PLoS Biology 4(10), e321.
| Crossref | Google Scholar |
Mollusc Specialist Group (1996a) Iredaleoconcha caporaphe. In ‘The IUCN Red List of Threatened Species 1996’. e.T10850A3222453. (International Union for Conservation of Nature and Natural Resources) Available at https://www.iucnredlist.org/species/10850/3222453
Mollusc Specialist Group (1996b) Dolapex amiculus. In ‘The IUCN Red List of Threatened Species 1996’. e.T6782A12805769. (International Union for Conservation of Nature and Natural Resources) Available at https://www.iucnredlist.org/species/6782/12805769
Mollusc Specialist Group (1996c) Lutilodix imitratrix. In ‘The IUCN Red List of Threatened Species 1996’. e.T12415A3341161. (International Union for Conservation of Nature and Natural Resources) Available at https://www.iucnredlist.org/species/12415/3341161
Mollusc Specialist Group (1996d) Panulena perrugosa. In ‘The IUCN Red List of Threatened Species 1996’. e.T15971A5335480. (International Union for Conservation of Nature and Natural Resources) Available at https://www.iucnredlist.org/species/15971/5335480
Mollusc Specialist Group (1996e) Advena campbelli. In ‘The IUCN Red List of Threatened Species 1996’. e.T524A13059373. (International Union for Conservation of Nature and Natural Resources) Available at https://www.iucnredlist.org/species/524/13059373
Mollusc Specialist Group (1996f) Advena charon. In ‘The IUCN Red List of Threatened Species 1996’. e.T525A13059401. (International Union for Conservation of Nature and Natural Resources) Available at https://www.iucnredlist.org/species/525/13059401
Mollusc Specialist Group (1996g) Mathewsoconcha belli. In ‘The IUCN Red List of Threatened Species 1996’. e.T12872A3393617. (International Union for Conservation of Nature and Natural Resources) Available at https://www.iucnredlist.org/species/12872/3393617
Mollusc Specialist Group (1996h) Quintalia stoddartii. In ‘The IUCN Red List of Threatened Species 1996’. e.T19058A8803062. (International Union for Conservation of Nature and Natural Resources) Available at https://www.iucnredlist.org/species/19058/8803062
Mollusc Specialist Group (1996i) Quintalia flosculus. In ‘The IUCN Red List of Threatened Species 1996’. e.T19057A8803034. (International Union for Conservation of Nature and Natural Resources) Available at https://www.iucnredlist.org/species/19057/8803034
Mollusc Specialist Group (1996j) Pittoconcha concinna. In ‘The IUCN Red List of Threatened Species 1996’. e.T17441A7067094. (International Union for Conservation of Nature and Natural Resources) Available at https://www.iucnredlist.org/species/17441/7067094
Morelet A (1866) Diagnoses de coquilles nouvelles de l’Indo-Chine. [Diagnosis of new shells from Indo-China.]. Revue et Magasin de Zoologie 1866, 165-168 [In French].
| Google Scholar |
Morelet A (1875) ‘Séries conchyliologiques comprenant l'énumération de mollusques terrestres et fluviatiles recueillies pendent le cours de différents voyages, ainsi que la description de plusieurs espèces Nouvelles. 4.’ [‘Conchological series comprising the enumeration of terrestrial and freshwater molluscs collected during the course of different voyages, as well as the description of several new species. 4.’] pp. 227–377. (Savy: Paris, France) [In French]
Neuweger D, White P, Ponder WF (2001) Land snails from Norfolk Island sites. Records of the Australian Museum Supplement 27, 115-122.
| Crossref | Google Scholar |
Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating Maximum-Likelihood phylogenies. Molecular Biology and Evolution 32(1), 268-274.
| Crossref | Google Scholar |
Okajima R, Chiba S (2009) Cause of bimodal distribution in the shape of a terrestrial gastropod. Evolution 63, 2877-2887.
| Crossref | Google Scholar |
Pfeiffer L (1846) Descriptions of thirty-six new species of Helix, belonging to the collection of H. Cuming, Esq. Proceedings of the Zoological Society of London 1845, 126-133.
| Google Scholar |
Pfeiffer L (1848) ‘Monographia Heliceorum Viventium. Sistens descriptiones systematicas et criticas omnium huius familiae generum et specierum hodie cognitarum. Volumen primum.’ [‘A Monograph of Living Helices. Containing systematic and critical descriptions of all genera and species of this family known to date. First volume.’] (F.A. Brockhaus: Leipzig, German Confederation) [In Latin]
Pfeiffer L (1878) ‘Nomenclator Heliceorum Viventium qui Continentur Nomina Omnium Hujus Familiae et Generum et Specierum Hodie Cognitarum Disposita ex Affinitate Naturli.’ [‘A Nomenclature of Living Helices Containing the Names of All the Families and Genera and Species Now Known, Arranged by Natural Affinity.’] (Ed. S Clessin) (Sumptibus Theodori Fischeri: Cassellis [Kassel, German Empire]) [In Latin]
Ponder WF, Varman R (1996a) Buffetia retinaculum. In ‘The IUCN Red List of Threatened Species 1996’. e.T3166A9644211. (International Union for Conservation of Nature and Natural Resources) Available at https://www.iucnredlist.org/species/3166/9644211
Ponder WF, Varman R (1996b) Nancibella quintalia. In ‘The IUCN Red List of Threatened Species 1996’. e.T14318A4431366. (International Union for Conservation of Nature and Natural Resources) Available at https://www.iucnredlist.org/species/14318/4431366
Presgraves DC, Glor RE (2010) Evolutionary biology: speciation on islands. Current Biology 20(10), R440-R442.
| Crossref | Google Scholar |
Preston HB (1913) LXV.—Characters of new genera and species of terrestrial Mollusca from Norfolk Island. Annals and Magazine of Natural History 12(72), 522-538.
| Crossref | Google Scholar |
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67(5), 901-904.
| Crossref | Google Scholar |
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12), 1572-1574.
| Crossref | Google Scholar |
Sauer J, Hausdorf B (2009) Sexual selection is involved in speciation in a land snail radiation on Crete. Evolution 63(10), 2535-2546.
| Crossref | Google Scholar |
Schilthuizen M, van Til A, Salverda M, Liew T-S, James SS, bin Elahan B, Vermeulen JJ (2006) Microgeographic evolution of snail shell shape and predator behavior. Evolution 60(9), 1851-1858.
| Crossref | Google Scholar |
Sela I, Ashkenazy H, Katoh K, Pupko T (2015) GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Research 43, W7-W14.
| Crossref | Google Scholar |
Semper C (1870) Erste Familie – Zonitidae [First family – Zonitidae]. In ‘Reisen im Archipel der Philippinen. Zweiter Theil. Wissenschaftliche Resultate. Dritter Band. Landmollusken’ [‘Travel in the Archipelago of the Philippines. Second part. Scientific results. Third volume. Land molluscs’]. pp. 7–80. (CW Kreidel: Wiesbaden, Prussia) [In German]
Sites JW, Marshall JC (2004) Operational criteria for delimiting species. Annual Review of Ecology Evolution and Systematics 35, 199-227.
| Crossref | Google Scholar |
Smith EA (1873) XXXII.—Description of a new species belonging to the genus Vitrina. Annals and Magazine of Natural History 11, 288-289.
| Crossref | Google Scholar |
Smith BJ, Reid S, Ponder WF (2002) Order STYLOMMATOPHORA. In ‘Australian Faunal Directory’. (Australian Biological Resources Study: Canberra, ACT, Australia) Available at https://biodiversity.org.au/afd/taxa/STYLOMMATOPHORA [Verified 28 August 2018]
Solem A (1961) New Caledonian land and fresh-water snails: an annotated check list. Fieldiana: Zoology 41(3), 415-501.
| Google Scholar |
Solem A (1966) Some non-marine mollusks from Thailand, with notes on classification of the Helicarionidae. Spolia Zoologica Musei Hauniensis 24, 1-110.
| Google Scholar |
Stankowski S (2011) Extreme, continuous variation in an island snail: local diversification and association of shell form with the current environment. Biological Journal of the Linnean Society 104(4), 756-769.
| Crossref | Google Scholar |
Suter H (1899) Anatomical notes on Medyla insculpta (Pfr). Proceedings of the Malacological Society of London 3(6), 330-332.
| Google Scholar |
Sykes ER (1900) Non-marine Mollusca of Norfolk and Philip Is. Proceedings of the Malacological Society of London 4, 139-147.
| Google Scholar |
Van Riel P, Jordaens K, Van Houtte N, Martins AMF, Verhagen R, Backeljau T (2005) Molecular systematics of the endemic Leptaxini (Gastropoda: Pulmonata) on the Azores islands. Molecular Phylogenetics and Evolution 37(1), 132-143.
| Crossref | Google Scholar |
Vardinoyannis K, Parmakelis A, Triantis KA, Giokas S (2018) Land molluscs in Greece: the rich, unique, diverse, and unprotected animal models. In ‘Biogeography and Biodiversity of the Aegean. In honour of Prof. Moysis Mylonas’. (Eds S Sfenthourakis, P Pafilis, A Parmakelis, KA Triantis) pp. 47–66. (Broken Hill Publishers Ltd: Cyprus)
Yeung NW, Hayes KA (2018) Biodiversity and extinction of Hawaiian land snails: how many are left now and what must we do to conserve them—a reply to Solem (1990). Integrative and Comparative Biology 58(6), 1157-1169.
| Crossref | Google Scholar |