Register      Login
Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Repeated evolution of an undescribed morphotype of Rhagada (Gastropoda : Camaenidae) from the inland Pilbara, Western Australia

Zoë R. Hamilton https://orcid.org/0000-0002-7914-5602
+ Author Affiliations
- Author Affiliations

School of Biological Sciences, University of Western Australia, Crawley, WA 6009, Australia. Email: zoerhamilton@gmail.com

Invertebrate Systematics 35(2) 203-215 https://doi.org/10.1071/IS20038
Submitted: 19 May 2020  Accepted: 4 September 2020   Published: 8 February 2021

Abstract

An undescribed small, banded morphotype of Rhagada land snails occurs widely in the rocky inland Pilbara region, Western Australia. Phylogenetic analysis of mitochondrial COI and 16S rRNA genes revealed that this novel morphotype is polyphyletic, comprising four distinct major clades, with divergences up to 21.4% at COI. These clades are apparently morphologically cryptic, with no obvious shell differences. Two of these species are associated with the major clade of Rhagada in the Pilbara mainland, one of which appears to be a variant of the larger, more globose species R. pilbarana, which occurs within 20 km proximity. The other two small, banded species are phylogenetically distinct from each other and all other known Rhagada. This small, banded morphotype shows evidence for both plesiomorphy and homoplasy. The morphotype has evolved independently at least twice, and is associated with the reasonably uniform habitat and harsh conditions in the elevated hinterland of the inland Pilbara. The broad distribution of the inland, small, banded morphotype conforms to the pattern of broad-scale uniformity of shells of the more coastal species of Rhagada. Its repeated evolution, however, confirms that the morphological uniformity is not simply because of common ancestry, supporting the theory that shell form in Rhagada is adapted to a broadly homogenous environment. Shell morphology in this genus has been demonstrated on more than one occasion to have the potential to adapt to different available environments, and hence shells should be used with a degree of caution for taxonomic interpretation.


References

Atchley, W. R., and Anderson, D. (1978). Ratios and the statistical analysis of biological data. Systematic Zoology 27, 71–78.
Ratios and the statistical analysis of biological data.Crossref | GoogleScholarGoogle Scholar |

Burghardt, I., and Köhler, F. (2015). Rhagada revisited: on the taxonomy of species from the Kimberley and Dampierland, Western Australia (Pulmonata, Camaenidae). Molluscan Research 35, 37–50.
Rhagada revisited: on the taxonomy of species from the Kimberley and Dampierland, Western Australia (Pulmonata, Camaenidae).Crossref | GoogleScholarGoogle Scholar |

Cain, A. J. (1977). Variation in the spire index of some coiled gastropod shells and its evolutionary significance. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 277, 377–428.
Variation in the spire index of some coiled gastropod shells and its evolutionary significance.Crossref | GoogleScholarGoogle Scholar |

Chiba, S. (1999). Accelerated evolution of land snails Mandarina in the oceanic Bonin Islands: evidence from mitochondrial DNA sequences. Evolution 53, 460–471.
Accelerated evolution of land snails Mandarina in the oceanic Bonin Islands: evidence from mitochondrial DNA sequences.Crossref | GoogleScholarGoogle Scholar | 28565404PubMed |

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.
Ecological and morphological patterns in communities of land snails of the genus Mandarina from the Bonin Islands.Crossref | GoogleScholarGoogle Scholar | 15000656PubMed |

Cook, L. M. (1997). Geographical and ecological patterns in Turkish snails. Journal of Biogeography 24, 409–418.
Geographical and ecological patterns in Turkish snails.Crossref | GoogleScholarGoogle Scholar |

Cowie, R. H. (1995). Variation in species diversity and shell shape in Hawaiian land snails: in situ speciation and ecological relationships. Evolution 49, 1191–1202.
Variation in species diversity and shell shape in Hawaiian land snails: in situ speciation and ecological relationships.Crossref | GoogleScholarGoogle Scholar | 28568515PubMed |

Criscione, F., and Köhler, F. (2013). Conserved shell disguises diversity in Mesodontrachia land snails from the Australian Monsoon Tropics (Gastropoda: Camaenidae). Zoologica Scripta 42, 389–405.
Conserved shell disguises diversity in Mesodontrachia land snails from the Australian Monsoon Tropics (Gastropoda: Camaenidae).Crossref | GoogleScholarGoogle Scholar |

Criscione, F., and Köhler, F. (2014). Molecular phylogenetics and comparative anatomy of Kimberleytrachia Köhler, 2011 – a genus of land snail endemic to the coastal Kimberley, Western Australia with description of new taxa (Gastropoda: Camaenidae). Contributions to Zoology (Amsterdam, Netherlands) 83, 245–267.
Molecular phylogenetics and comparative anatomy of Kimberleytrachia Köhler, 2011 – a genus of land snail endemic to the coastal Kimberley, Western Australia with description of new taxa (Gastropoda: Camaenidae).Crossref | GoogleScholarGoogle Scholar |

Criscione, F., Law, M. L., and Köhler, F. (2012). Land snail diversity in the monsoon tropics of northern Australia: revision of the genus Exiligada Iredale, 1939 (Mollusca: Pulmonata: Camaenidae), with description of 13 new species. Zoological Journal of the Linnean Society 166, 689–722.
Land snail diversity in the monsoon tropics of northern Australia: revision of the genus Exiligada Iredale, 1939 (Mollusca: Pulmonata: Camaenidae), with description of 13 new species.Crossref | GoogleScholarGoogle Scholar |

Davison, A., Blackie, R. L. E., and Scothern, G. P. (2009). DNA barcoding of stylommatophoran land snails: a test of existing sequences. Molecular Ecology Resources 9, 1092–1101.
DNA barcoding of stylommatophoran land snails: a test of existing sequences.Crossref | GoogleScholarGoogle Scholar | 21564847PubMed |

Emberton, K. C. (1995). Sympatric convergence and environmental correlation between two land-snail species. Evolution 49, 469–475.
Sympatric convergence and environmental correlation between two land-snail species.Crossref | GoogleScholarGoogle Scholar | 28565089PubMed |

Folmer, O., Black, M., Hoeh, W., Lutz, R., and 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.
| 7881515PubMed |

Goodacre, S. L., and Wade, C. M. (2001). Patterns of genetic variation in Pacific island land snails: the distribution of cytochrome b lineages among Society Island Partula. Biological Journal of the Linnean Society. Linnean Society of London 73, 131–138.
Patterns of genetic variation in Pacific island land snails: the distribution of cytochrome b lineages among Society Island Partula.Crossref | GoogleScholarGoogle Scholar |

Goodfriend, G. A. (1986). Variation in land-snail shell form and size and its causes: a review. Systematic Zoology 35, 204–223.
Variation in land-snail shell form and size and its causes: a review.Crossref | GoogleScholarGoogle Scholar |

Hamilton, Z. R., and Johnson, M. S. (2015). Hybridization between genetically and morphologically divergent forms of Rhagada (Gastropoda: Camaenidae) snails at a zone of secondary contact) Biological Journal of the Linnean Society. Linnean Society of London 114, 348–362.
Hybridization between genetically and morphologically divergent forms of Rhagada (Gastropoda: Camaenidae) snails at a zone of secondary contact)Crossref | GoogleScholarGoogle Scholar |

Huelsenbeck, J. P., and Ronquist, F. (2001). MrBAYES: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.
MrBAYES: Bayesian inference of phylogeny.Crossref | GoogleScholarGoogle Scholar | 11524383PubMed |

Johnson, M. S., and Black, R. (1991). Growth, survivorship and population size in the land snail Rhagada convicta Cox, 1870 (Pulmonata: Camaenidae) from a semiarid environment in Western Australia. The Journal of Molluscan Studies 57, 367–374.
Growth, survivorship and population size in the land snail Rhagada convicta Cox, 1870 (Pulmonata: Camaenidae) from a semiarid environment in Western Australia.Crossref | GoogleScholarGoogle Scholar |

Johnson, M. S., and Stankowski, S. (2018). Extreme morphological diversity in a single species of Rhagada (Gastropoda: Camaenidae) in the Dampier Archipelago, Western Australia: review of the evidence, revised taxonomy and changed perspective. The Journal of Molluscan Studies 84, 337–344.
Extreme morphological diversity in a single species of Rhagada (Gastropoda: Camaenidae) in the Dampier Archipelago, Western Australia: review of the evidence, revised taxonomy and changed perspective.Crossref | GoogleScholarGoogle Scholar |

Johnson, M. S., Murray, J., and Clarke, B. (2000). Parallel evolution in Marquesan partulid land snails. Biological Journal of the Linnean Society. Linnean Society of London 69, 577–598.
Parallel evolution in Marquesan partulid land snails.Crossref | GoogleScholarGoogle Scholar |

Johnson, M. S., O’Brien, E. K., and Fitzpatrick, J. J. (2010). Deep, hierarchal divergence of mitochondrial DNA in Amplirhagada land snails (Gastropoda: Camaenidae) from the Bonaparte Archipelago, Western Australia. Biological Journal of the Linnean Society. Linnean Society of London 100, 141–153.
Deep, hierarchal divergence of mitochondrial DNA in Amplirhagada land snails (Gastropoda: Camaenidae) from the Bonaparte Archipelago, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Johnson, M. S., Hamilton, Z. R., Teale, R., and Kendrick, P. G. (2012). Endemic evolutionary radiation of Rhagada land snails (Pulmonata: Camaenidae) in a continental archipelago in northern Western Australia. Biological Journal of the Linnean Society. Linnean Society of London 106, 316–327.
Endemic evolutionary radiation of Rhagada land snails (Pulmonata: Camaenidae) in a continental archipelago in northern Western Australia.Crossref | GoogleScholarGoogle Scholar |

Johnson, M. S., Stankowski, S., Whisson, C. S., Teale, R. J., and Hamilton, Z. R. (2013). Camaenid land snails on Barrow Island: distributions, molecular phylogenetics and taxonomic revision. The Western Australian Museum 83, 159–171.
Camaenid land snails on Barrow Island: distributions, molecular phylogenetics and taxonomic revision.Crossref | GoogleScholarGoogle Scholar |

Johnson, M. S., Stankowski, S., Kendrick, P. G., Hamilton, Z. R., and Teale, R. J. (2016). Diversity, complementary distributions and taxonomy of Rhagada land snails (Gastropoda: Camaenidae) on the Burrup Peninsula, Western Australia. Invertebrate Systematics 30, 323–334.
Diversity, complementary distributions and taxonomy of Rhagada land snails (Gastropoda: Camaenidae) on the Burrup Peninsula, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Köhler, F., and Criscione, F. (2013a). Small snails in a big place: a radiation in the semi-arid rangelands in northern Australia (Eupulmonata, Camaenidae, Nanotrachia gen. nov.). Zoological Journal of the Linnean Society 169, 103–123.
Small snails in a big place: a radiation in the semi-arid rangelands in northern Australia (Eupulmonata, Camaenidae, Nanotrachia gen. nov.).Crossref | GoogleScholarGoogle Scholar |

Köhler, F., and Criscione, F. (2013b). Plio-Pleistocene out-of-Australia dispersal in a camaenid land snail. Journal of Biogeography 40, 1971–1982.
Plio-Pleistocene out-of-Australia dispersal in a camaenid land snail.Crossref | GoogleScholarGoogle Scholar |

Köhler, F., and Johnson, M. S. (2012). Species limits in molecular phylogenies: a cautionary tale from Australian land snails (Camaenidae: Amplirhagada Iredale, 1933). Zoological Journal of the Linnean Society 165, 337–362.
Species limits in molecular phylogenies: a cautionary tale from Australian land snails (Camaenidae: Amplirhagada Iredale, 1933).Crossref | GoogleScholarGoogle Scholar |

McKenzie, N. L., van Leeuwen, S., and Pinder, A. M. (2009). Introduction to the Pilbara Biodiversity Survey, 2002–2007. Records of the Western Australian Museum 78, 3–89.
Introduction to the Pilbara Biodiversity Survey, 2002–2007.Crossref | GoogleScholarGoogle Scholar |

Morii, Y., Yokoyama, J., Kawata, M., Davison, A., and Chiba, S. (2015). Evidence of introgressive hybridization between the morphologically divergent land snails Ainohelix and Ezohelix. Biological Journal of the Linnean Society. Linnean Society of London 115, 77–95.
Evidence of introgressive hybridization between the morphologically divergent land snails Ainohelix and Ezohelix.Crossref | GoogleScholarGoogle Scholar |

O’Neill, C., Johnson, M. S., Hamilton, Z. R., and Teale, R. J. (2014). Molecular phylogenetics of the land snail genus Quistrachia (Gastropoda: Camaenidae) in northern Western Australia. Invertebrate Systematics 28, 244–257.
Molecular phylogenetics of the land snail genus Quistrachia (Gastropoda: Camaenidae) in northern Western Australia.Crossref | GoogleScholarGoogle Scholar |

Palumbi, S., Martin, A., Romano, S., McMillan, W. O., Stice, L., and Grabowski, G. (1991). ‘The Simple Fool’s Guide to PCR.’ (University of Hawaii: Honolulu, HI, USA.)

Perez, K. E., Defreitas, N., Slapcinsky, J., Minton, R. L., Anderson, F. E., and Pearce, T. A. (2014). Molecular phylogeny, evolution of shell shape, and DNA barcoding in Polygyridae (Gastropoda: Pulmonata) an endemic North American clade of land snails. American Malacological Bulletin 32, 1–31.
Molecular phylogeny, evolution of shell shape, and DNA barcoding in Polygyridae (Gastropoda: Pulmonata) an endemic North American clade of land snails.Crossref | GoogleScholarGoogle Scholar |

Pfenninger, M., Staubach, S., Albrecht, C., Streit, B., and Schwenk, K. (2003). Ecological and morphological differentiation among cryptic lineages in freshwater limpets of the nominal form-group Ancylus fluviatilis (O.F. Müller, 1774). Molecular Ecology 12, 2731–2745.
Ecological and morphological differentiation among cryptic lineages in freshwater limpets of the nominal form-group Ancylus fluviatilis (O.F. Müller, 1774).Crossref | GoogleScholarGoogle Scholar | 12969476PubMed |

Ronquist, F., and Huelsenbeck, J. P. (2003). MrBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
MrBAYES 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 12912839PubMed |

Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBAYES 3.2: Efficient Bayesian phylogenetic inference and model selection across a large model space. Systematic Biology 61, 539–542.
MrBAYES 3.2: Efficient Bayesian phylogenetic inference and model selection across a large model space.Crossref | GoogleScholarGoogle Scholar | 22357727PubMed |

Solem, A. (1985). Camaenid land snails from Western Australia and central Australia (Mollusca: Pulmonata: Camaenidae). V. Remaining Kimberley Genera and Addenda to the Kimberley. Records of the Western Australian Museum 20, 707–981.

Solem, A. (1991). Land snails of the Kimberley rainforest patches and biogeography of all Kimberley land snails. In ‘Kimberley Rainforests of Australia’. (Eds N. L. Mackenzie, R. B. Johnston, and P. G. Kendrick.) pp 145–163. (Surrey Beatty: Sydney, NSW, Australia.)

Solem, A. (1997). Camaenid land snails from western and central Australia (Mollusca: Pulmonata: Camaenidae): VII. Taxa from Dampierland through the Nullarbor. Records of the Western Australian Museum 50, 1461–1906.

Solem, A., and Christensen, C. C. (1984). Camaenid land snail reproductive cycle and growth patterns in semiarid areas of north-western Australia. Australian Journal of Zoology 32, 471–491.
Camaenid land snail reproductive cycle and growth patterns in semiarid areas of north-western Australia.Crossref | GoogleScholarGoogle 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. Linnean Society of London 104, 756–769.
Extreme, continuous variation in an island snail: local diversification and association of shell form with the current environment.Crossref | GoogleScholarGoogle Scholar |

Stankowski, S. (2013). Ecological speciation in an island snail: evidence for the parallel evolution of a novel ecotype and maintenance by ecologically dependent postzygotic selection. Molecular Ecology 22, 2726–2741.
Ecological speciation in an island snail: evidence for the parallel evolution of a novel ecotype and maintenance by ecologically dependent postzygotic selection.Crossref | GoogleScholarGoogle Scholar | 23506623PubMed |

Stankowski, S. (2015). Layers of contingency shroud pervasive ecological divergence in a local radiation of land snails. Biological Journal of the Linnean Society. Linnean Society of London 116, 267–276.
Layers of contingency shroud pervasive ecological divergence in a local radiation of land snails.Crossref | GoogleScholarGoogle Scholar |

Stankowski, S., and Johnson, M. S. (2014). Biogeographic discordance of molecular phylogenetic and phenotypic variation in a continental archipelago radiation of land snails. BMC Evolutionary Biology 14, 2.
Biogeographic discordance of molecular phylogenetic and phenotypic variation in a continental archipelago radiation of land snails.Crossref | GoogleScholarGoogle Scholar | 24393567PubMed |

Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: Molecular Evolutionary Genetic Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
MEGA5: Molecular Evolutionary Genetic Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 21546353PubMed |

Teshima, H., Davison, A., Kuwahara, Y., Yokoyama, J., Chiba, S., Fukuda, T., Ogimura, H., and Kawata, M. (2003). The evolution of extreme shell shape variation in the land snail Ainohelix editha: a phylogeny and hybrid zone analysis. Molecular Ecology 12, 1869–1878.
The evolution of extreme shell shape variation in the land snail Ainohelix editha: a phylogeny and hybrid zone analysis.Crossref | GoogleScholarGoogle Scholar | 12803638PubMed |