A revision of Peronina Plate, 1893 (Gastropoda : Euthyneura : Onchidiidae) based on mitochondrial and nuclear DNA sequences, morphology and natural history
Tricia C. Goulding A , Shau Hwai Tan B C , Siong Kiat Tan D , Deepak Apte E , Vishal Bhave E , Sumantha Narayana E , Rahul Salunkhe E and Benoît Dayrat A FA Department of Biology, Pennsylvania State University, University Park, PA 16802, USA.
B School of Biological Sciences, Universiti Sains Malaysia, 11800 Penang, Malaysia.
C Centre for Marine and Coastal Studies, Universiti Sains Malaysia, 11800 Penang, Malaysia.
D Lee Kong Chian Natural History Museum, 2 Conservatory Dr, National University of Singapore, 117377, Singapore.
E Bombay Natural History Society, Hornbill House, Shaheed Bhagat Singh Road, Mumbai 400 001, Maharashtra, India.
F Corresponding author. Email: bad25@psu.edu
Invertebrate Systematics 32(4) 803-826 https://doi.org/10.1071/IS17094
Submitted: 26 August 2017 Accepted: 21 March 2018 Published: 16 August 2018
Abstract
Peronina Plate, 1893 is a genus of onchidiids that live on the mud in mangrove forests. Peronina can be identified in the field by the lung opening at the margin between the ventral hyponotum and the dorsal notum, and by the distinctive scalloped notum edge. This genus was previously known only from the holotype of the type species, Peronina alta Plate, 1893, from eastern India. Onchidium tenerum Stoliczka, 1869 is moved to Peronina and applies to the same species as Peronina alta. Peronina species are described using an integrative approach (natural history, comparative anatomy and DNA sequences). Mitochondrial COI and 16S sequences and nuclear ITS2 and 28S sequences are used to independently test species boundaries. Mitochondrial sequences yielded three units separated by a large barcode gap, but nuclear sequences yielded two units. Because these two units are congruent with differences in the male copulatory apparatus, they are accepted as species. Explanations for highly divergent COI haplotypes within one species are discussed. Peronina tenera (Stoliczka, 1869) is distributed in the Bay of Bengal and the Strait of Malacca, while P. zulfigari Goulding & Dayrat, sp. nov. is endemic to the Strait of Malacca. The two species differ internally but are cryptic externally.
Additional keywords: biodiversity, biogeography, comparative morphology, Indo-Malayan, molecular systematics.
References
Bay, L. K., Choat, J. H., van Herwerden, L., and Robertson, D. R. (2004). High genetic diversities and complex genetic structure in an Indo-Pacific tropical reef fish (Chlorurus sordidus): evidence of an unstable evolutionary past? Marine Biology 144, 757–767.| High genetic diversities and complex genetic structure in an Indo-Pacific tropical reef fish (Chlorurus sordidus): evidence of an unstable evolutionary past?Crossref | GoogleScholarGoogle Scholar |
Bowen, B. W., Gaither, M. R., DiBattista, J. D., Iacchei, M., Andrews, K. R., Grant, W. S., Toonen, R. J., and Briggs, J. C. (2016). Comparative phylogeography of the ocean planet. Proceedings of the National Academy of Sciences of the United States of America 113, 7962–7969.
| Comparative phylogeography of the ocean planet.Crossref | GoogleScholarGoogle Scholar |
Bretnall, W. (1919). Onchidiidae from Australia and the South-Western Pacific Islands. Records of the Australian Museum 12, 303–328.
| Onchidiidae from Australia and the South-Western Pacific Islands.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 |
Chou, L. M., and Tan, K. S. (2008). Corals, worms and molluscs. In ‘The Singapore Red Data Book: Threatened Plants and Animals of Singapore. 2nd Edition’. (Eds G. W. H. Davidson, P. K. L. Ng and H. C. Ho.) pp. 39–61. (The Nature Society: Singapore.)
Chou, L. M., Murphy, D. H., and Ng, P. K. L. (1994). Corals, molluscs and other invertebrates. In ‘The Singapore Red Data Book: Threatened Plants and Animals of Singapore’. (Eds P. K. L. Ng and Y. C. Wee.) pp. 52–87. (The Nature Society: Singapore.)
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 |
Dayrat, B. (2005). Towards integrative taxonomy. Biological Journal of the Linnean Society. Linnean Society of London 85, 407–415.
| Towards integrative taxonomy.Crossref | GoogleScholarGoogle Scholar |
Dayrat, B. (2009). Review of the current knowledge of the systematics of Onchidiidae (Mollusca: Gastropoda: Pulmonata) with a checklist of nominal species. Zootaxa 2068, 1–26.
Dayrat, B., and Goulding, T. C. (2017). Systematics of the onchidiid slug Onchidina australis (Mollusca: Gastropoda: Pulmonata). Archiv für Molluskenkunde 146, 121–133.
| Systematics of the onchidiid slug Onchidina australis (Mollusca: Gastropoda: Pulmonata).Crossref | GoogleScholarGoogle Scholar |
Dayrat, B., Conrad, M., Balayan, S., White, T. R., Albrecht, C., Golding, R., Gomes, S. R., Harasewych, M. G., and de Frias Martins, A. M. (2011). Phylogenetic relationships and evolution of pulmonate gastropods (Mollusca): new insights from increased taxon sampling. Molecular Phylogenetics and Evolution 59, 425–437.
| Phylogenetic relationships and evolution of pulmonate gastropods (Mollusca): new insights from increased taxon sampling.Crossref | GoogleScholarGoogle Scholar |
Dayrat, B., Goulding, T. C., Apte, D., Bhave, V., Comendador, J., Quang, N. X., Tan, S. K., and Tan, S. H. (2016). Integrative taxonomy of the genus Onchidium Buchannan, 1800 (Mollusca: Gastropoda: Pulmonata: Onchidiidae). ZooKeys 636, 1–40.
| Integrative taxonomy of the genus Onchidium Buchannan, 1800 (Mollusca: Gastropoda: Pulmonata: Onchidiidae).Crossref | GoogleScholarGoogle Scholar |
Dayrat, B., Goulding, T. C., Apte, D., Bhave, V., and Quang, N. X. (2017). A new genus and four new species of onchidiid slugs from South-East Asia (Mollusca: Gastropoda: Pulmonata: Onchidiidae). Journal of Natural History 51, 1851–1897.
| A new genus and four new species of onchidiid slugs from South-East Asia (Mollusca: Gastropoda: Pulmonata: Onchidiidae).Crossref | GoogleScholarGoogle Scholar |
Emmel, F. J., and Curray, J. R. (1982). A submerged late Pleistocene delta and other features related to sea level changes in the Malacca Strait. Marine Geology 47, 197–216.
| A submerged late Pleistocene delta and other features related to sea level changes in the Malacca Strait.Crossref | GoogleScholarGoogle Scholar |
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.
Fretter, V. (1943). Studies in the functional morphology and embryology of Onchidella celtica (Forbes and Hanley) and their bearing on its relationships. Journal of the Marine Biological Association of the United Kingdom 25, 685–720.
| Studies in the functional morphology and embryology of Onchidella celtica (Forbes and Hanley) and their bearing on its relationships.Crossref | GoogleScholarGoogle Scholar |
Guindon, S., and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.
| A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.Crossref | GoogleScholarGoogle Scholar |
Hassouna, N., Mithot, B., and Bachellerie, J. P. (1984). The complete nucleotide sequence of mouse 28S rRNA gene. Implications for the process of size increase of the large subunit rRNA in higher eukaryotes. Nucleic Acids Research 12, 3563–3583.
| The complete nucleotide sequence of mouse 28S rRNA gene. Implications for the process of size increase of the large subunit rRNA in higher eukaryotes.Crossref | GoogleScholarGoogle Scholar |
Labbé, A. (1934). Les Silicodermés (Labbé) du Muséum d’Histoire Naturelle de Paris. Première partie: classification, formes nouvelles ou peu connues. Annales de l’Institut Océanographique 14, 173–246.
Meyer, C. P., and Paulay, G. (2005). DNA barcoding: error rates based on comprehensive sampling. PLoS Biology 3, 2229–2238.
| DNA barcoding: error rates based on comprehensive sampling.Crossref | GoogleScholarGoogle Scholar |
Milne, I., Wright, F., Rowe, G., Marshal, D. F., Husmeier, D., and McGuire, G. (2004). TOPALi: software for automatic identification of recombinant sequences within DNA multiple alignments. Bioinformatics 20, 1806–1807.
| TOPALi: software for automatic identification of recombinant sequences within DNA multiple alignments.Crossref | GoogleScholarGoogle Scholar |
Palumbi, S. (1996). Nucleic acid II: the polymerase chain reaction. In ‘Molecular Systematics. Second Edition’. (Eds D. Hillis, C. Moritz and B. Mable.) pp. 205–247. (Sinauer Press: Sunderland, MA.)
Pfenninger, M., Cordellier, M., and Streit, B. (2006). Comparing the efficacy of morphologic and DNA-based taxonomy in the freshwater gastropod genus Radix (Basommatophora, Pulmonata). BMC Evolutionary Biology 6, 100.
| Comparing the efficacy of morphologic and DNA-based taxonomy in the freshwater gastropod genus Radix (Basommatophora, Pulmonata).Crossref | GoogleScholarGoogle Scholar |
Pinceel, J., Jordaens, K., and Backeljau, T. (2005). Extreme mtDNA divergences in a terrestrial slug (Gastropoda, Pulmonata, Arionidae): accelerated evolution, allopatric divergence and secondary contact. Journal of Evolutionary Biology 18, 1264–1280.
| Extreme mtDNA divergences in a terrestrial slug (Gastropoda, Pulmonata, Arionidae): accelerated evolution, allopatric divergence and secondary contact.Crossref | GoogleScholarGoogle Scholar |
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 |
Stoliczka, F. (1869). The malacology of Lower Bengal. Journal of the Asiatic Society of Bengal 38, 86–111.
Stringer, B. L. (1963). Embryology of the New Zealand Onchidiidae and its bearing on the classification of the group. Nature 197, 621–622.
| Embryology of the New Zealand Onchidiidae and its bearing on the classification of the group.Crossref | GoogleScholarGoogle Scholar |
Swofford, D. L. (2002). ‘PAUP: Phylogenetic Analysis Using Parsimony, Version 4.0b10.’ (Sinauer: Sunderland, MA.)
Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
| MEGA6: molecular evolutionary genetics analysis version 6.0.Crossref | GoogleScholarGoogle Scholar |
Thomaz, D., Guiller, A., and Clarke, B. (1996). Extreme divergence of mitochondrial DNA within species of pulmonate land snails. Proceedings. Biological Sciences 263, 363–368.
| Extreme divergence of mitochondrial DNA within species of pulmonate land snails.Crossref | GoogleScholarGoogle Scholar |
Plate, L. H. von (1893). Studien über opisthopneumone Lungenschnecken, II. Die Oncidiiden. Zoologische Jahrbucher. Abteilung fur Anatomie und Ontogenie der Tiere 7, 93–234.
Vonnemann, V., Schrödl, M., Klussmann-Kolb, A., and Wägele, H. (2005). Reconstruction of the phylogeny of the Opisthobranchia (Mollusca: Gastropoda) by means of 18S and 28S rRNA gene sequences. The Journal of Molluscan Studies 71, 113–125.
| Reconstruction of the phylogeny of the Opisthobranchia (Mollusca: Gastropoda) by means of 18S and 28S rRNA gene sequences.Crossref | GoogleScholarGoogle Scholar |
Wade, C. M., and Mordan, P. B. (2000). Evolution within the gastropod molluscs; using the ribosomal RNA gene-cluster as an indicator of phylogenetic relationships. The Journal of Molluscan Studies 66, 565–570.
| Evolution within the gastropod molluscs; using the ribosomal RNA gene-cluster as an indicator of phylogenetic relationships.Crossref | GoogleScholarGoogle Scholar |
White, T. R., Conrad, M. M., Tseng, R., Balayan, S., Golding, R., de Frias Martins, A., and Dayrat, B. A. (2011). Ten new complete mitochondrial genomes of pulmonates (Mollusca: Gastropoda) and their impact on phylogenetic relationships. BMC Evolutionary Biology 11, 295.
| Ten new complete mitochondrial genomes of pulmonates (Mollusca: Gastropoda) and their impact on phylogenetic relationships.Crossref | GoogleScholarGoogle Scholar |
Woodroffe, C. D., and Grindrod, J. (1991). Mangrove biogeography: the role of Quaternary environmental and sea-level change. Journal of Biogeography 18, 479–492.
| Mangrove biogeography: the role of Quaternary environmental and sea-level change.Crossref | GoogleScholarGoogle Scholar |