Few and far apart: integrative taxonomy of Australian species of Gladiobela and Pagodibela (Conoidea : Raphitomidae) reveals patterns of wide distributions and low abundance
Anders Hallan A , Francesco Criscione
A D , Alexander Fedosov B and Nicolas Puillandre C
+ Author Affiliations
- Author Affiliations
A Australian Museum Research Institute, 1 William Street, Sydney, NSW 2010, Australia.
B A.N. Severtsov Institute of Ecology and Evolution of Russian Academy of Sciences, Leninski Prospect 33, RU-119071 Moscow, Russia.
C Institut Systématique Evolution Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, 57 rue Cuvier, CP 26, F-75005 Paris, France.
D Corresponding author. Email: francesco.criscione@austmus.gov.au
Invertebrate Systematics 35(2) 181-202 https://doi.org/10.1071/IS20017
Submitted: 29 March 2020 Accepted: 1 September 2020 Published: 8 February 2021
Abstract
The deep-sea malacofauna of temperate Australia remains comparatively poorly known. However, a recent influx of DNA-suitable material obtained from a series of deep-sea cruises has facilitated integrative taxonomic study on the Conoidea (Caenogastropoda : Neogastropoda). Building on a recent molecular phylogeny of the conoidean family Raphitomidae, this study focussed on the genera Gladiobela and Pagodibela (both Criscione, Hallan, Puillandre & Fedosov, 2020). We subjected a representative mtDNA cox1 dataset of deep-sea raphitomids to ABGD, which recognised 14 primary species hypotheses (PSHs), 9 of which were converted to secondary species hypotheses (SSHs). Following the additional examination of the shell and hypodermic radula features, as well as consideration of bathymetric and geographic data, seven of these SSHs were recognised as new to science and given full species rank. Subsequently, systematic descriptions are provided herein. Of these, five are attributed to Gladiobela (three of which are endemic to Australia and two more widely distributed) and two are placed in Pagodibela (one endemic to southern Australia and one widespread in the Pacific). The rarity of many ‘turrids’ reported in previous studies is confirmed herein, as particularly indicated by highly disjunct geographic records for two taxa. Additionally, several of the studied taxa exhibit wide Indo-Pacific distributions, suggesting that wide geographic ranges in deep-sea ‘turrids’ may be more common than previously assumed. Finally, impediments to deep-sea ‘turrid’ taxonomy in light of such comparative rarity and unexpectedly wide distributions are discussed.
References
Bouchet, P., and Kantor, Y. I. (2004). New Caledonia: the major centre of biodiversity for volutomitrid molluscs (Mollusca: Neogastropoda: Volutomitridae). Systematics and Biodiversity 1, 467–502.| New Caledonia: the major centre of biodiversity for volutomitrid molluscs (Mollusca: Neogastropoda: Volutomitridae).Crossref | GoogleScholarGoogle Scholar |
Bouchet, P., and Sysoev, A. (2001). Typhlosyrinx-like tropical deep-water turriform gastropods (Mollusca, Gastropoda, Conoidea). Journal of Natural History 35, 1693–1715.
| Typhlosyrinx-like tropical deep-water turriform gastropods (Mollusca, Gastropoda, Conoidea).Crossref | GoogleScholarGoogle Scholar |
Bouchet, P., and Warén, A. (1980). Revision of the north east Atlantic bathyal and abyssal Turridae (Mollusca, Gastropoda). The Journal of Molluscan Studies 46, 1–119.
| Revision of the north east Atlantic bathyal and abyssal Turridae (Mollusca, Gastropoda).Crossref | GoogleScholarGoogle Scholar |
Bouchet, P., Heros, V., Lozouet, P., and Maestrati, P. (2008). A quarter-century of deep-sea malacological exploration in the south and west Pacific: where do we stand? How far to go? In ‘Tropical Deep-Sea Benthos 25’. (Eds V. Héros, R. H. Cowie, and P. Bouchet.) Mémoires du Muséum National d’Histoire Naturelle 196, pp. 9–40. (Publications Scientifiques du Muséum: Paris, France.)
Bouchet, P., Lozouet, P., and Sysoev, A. (2009). An inordinate fondness for turrids. Deep-sea Research – II. Topical Studies in Oceanography 56, 1724–1731.
| An inordinate fondness for turrids.Crossref | GoogleScholarGoogle Scholar |
Bouchet, P., Kantor, Y. I., Sysoev, A., and Puillandre, N. (2011). A new operational classification of the Conoidea (Gastropoda). The Journal of Molluscan Studies 77, 273–308.
| A new operational classification of the Conoidea (Gastropoda).Crossref | GoogleScholarGoogle Scholar |
Burton, E. A. (1998). Carbonate compensation depth. In ‘Geochemistry’. (Eds C. P. Marshall and R. W. Fairbridge.) p. 73 (Springer: Dordrecht, Netherlands.)
Costello, M. J., Tsai, P., Wong, P. S., Cheung, A. K. L., Basher, Z., and Chaudhary, C. (2017). Marine biogeographic realms and species endemicity. Nature Communications 8, 1057.
| Marine biogeographic realms and species endemicity.Crossref | GoogleScholarGoogle Scholar | 29051522PubMed |
Criscione, F., Hallan, A., Puillandre, N., and Fedosov, A. E. (2020). Where the snails have no name: a molecular phylogeny of Raphitomidae (Neogastropoda: Conoidea) uncovers vast unexplored diversity in the deep seas of temperate southern and eastern Australia. Zoological Journal of the Linnean Society , zlaa088.
| Where the snails have no name: a molecular phylogeny of Raphitomidae (Neogastropoda: Conoidea) uncovers vast unexplored diversity in the deep seas of temperate southern and eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Fedosov, A. E., and Puillandre, N. (2012). Phylogeny and taxonomy of the Kermia–Pseudodaphnella (Mollusca: Gastropoda: Raphitomidae) genus complex: a remarkable radiation via diversification of larval development. Systematics and Biodiversity 10, 447–477.
| Phylogeny and taxonomy of the Kermia–Pseudodaphnella (Mollusca: Gastropoda: Raphitomidae) genus complex: a remarkable radiation via diversification of larval development.Crossref | GoogleScholarGoogle Scholar |
Fedosov, A. E., Stahlschmidt, P., Puillandre, N., Aznar-Cormano, L., and Bouchet, P. (2017). Not all spotted cats are leopards: evidence for a Hemilienardia ocellata species complex (Gastropoda: Conoidea: Raphitomidae). European Journal of Taxonomy 268, 1–20.
| Not all spotted cats are leopards: evidence for a Hemilienardia ocellata species complex (Gastropoda: Conoidea: Raphitomidae).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.
| 7881515PubMed |
Gonzales, D. T. T., and Saloma, C. P. (2014). A bioinformatics survey for conotoxin-like sequences in three turrid snail venom duct transcriptomes. Toxicon 92, 66–74.
| A bioinformatics survey for conotoxin-like sequences in three turrid snail venom duct transcriptomes.Crossref | GoogleScholarGoogle Scholar |
Gorson, J., Ramrattan, G., Verdes, A., Wright, M. E., Kantor, Y., Rajaram Srinivasan, R., Musunuri, R., Packer, D., Albano, G., Qiu, W. G., and Holford, M. (2015). Molecular diversity and gene evolution of the venom arsenal of Terebridae predatory marine snails. Genome Biology and Evolution 7, 1761–1778.
| Molecular diversity and gene evolution of the venom arsenal of Terebridae predatory marine snails.Crossref | GoogleScholarGoogle Scholar | 26025559PubMed |
Hallan, A., Criscione, F., Fedosov, A. E., and Puillandre, N. (2020). Bouchetispira ponderi n. sp. (Conoidea: Bouchetispiridae), a new deep-sea gastropod from temperate Australia. Molluscan Research 40, 86–92.
| Bouchetispira ponderi n. sp. (Conoidea: Bouchetispiridae), a new deep-sea gastropod from temperate Australia.Crossref | GoogleScholarGoogle Scholar |
Hedley, C. (1922). A revision of the Australian Turridae. Records of the Australian Museum 13, 213–359.
| A revision of the Australian Turridae.Crossref | GoogleScholarGoogle Scholar |
Kantor, Y. I., and Sysoev, A. V. (1991). Sexual dimorphism in the apertural notch of a new species of Gemmula (Gastropoda: Turridae). The Journal of Molluscan Studies 57, 205–209.
| Sexual dimorphism in the apertural notch of a new species of Gemmula (Gastropoda: Turridae).Crossref | GoogleScholarGoogle Scholar |
Kantor, Y. I., and Taylor, J. D. (2002). Foregut anatomy and relationships of raphitomine gastropods (Gastropoda: Conoidea: Raphitominae). Bollettino Malacologico 38, 83–110.
Kantor, Y. I., Puillandre, N., Olivera, B. M., and Bouchet, P. (2008). Morphological proxies for taxonomic decision in turrids (Mollusca, Neogastropoda): a test of the value of shell and radula characters using molecular data. Zoological Science 25, 1156–1170.
| Morphological proxies for taxonomic decision in turrids (Mollusca, Neogastropoda): a test of the value of shell and radula characters using molecular data.Crossref | GoogleScholarGoogle Scholar | 19267627PubMed |
Kantor, Y. I., Fedosov, A. E., and Puillandre, N. (2018). New and unusual deep-water Conoidea revised with shell, radula and DNA characters. Ruthenica 28, 47–82.
Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
| MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar | 27004904PubMed |
López-Vera, E., de la Cortera, E. P. H., Maillo, M., Riesgo-Escovar, J. R., Olivera, B. M., and Aguilar, M. B. (2004). A novel structural class of toxins: the methionine-rich peptides from the venoms of turrid marine snails (Mollusca, Conoidea). Toxicon 43, 365–374.
| A novel structural class of toxins: the methionine-rich peptides from the venoms of turrid marine snails (Mollusca, Conoidea).Crossref | GoogleScholarGoogle Scholar | 15051399PubMed |
MacIntosh, H., Althaus, F., Williams, A., Tanner, J. E., Alderslade, P., Ahyong, S. T., Bax, N., Criscione, F., Crowther, A. L., Farrelly, C. A., Finn, J. K., Goudie, L., Gowlett-Holmes, K., Hosie, A. M., Kupriyanova, E., Mah, C., McCallum, A. W., Merrin, K. L., Miskelly, A., Mitchell, M. L., Molodtsova, T., Murray, A., O’Hara, T. D., O’Loughlin, P. M., Paxton, H., Reid, A. L., Sorokin, S. J., Staples, D., Walker-Smith, G., Whitfield, E., and Wilson, R. S. (2018). Invertebrate diversity in the deep Great Australian Bight (200–5000 m). Marine Biodiversity Records 11, 23.
| Invertebrate diversity in the deep Great Australian Bight (200–5000 m).Crossref | GoogleScholarGoogle Scholar |
Marshall, B. A. (1983). A revision of the Recent Triphoridae of southern Australia (Mollusca: Gastropoda). Records of the Australian Museum 35, 1–119.
Medinskaya, A. (1999). Foregut anatomy of Cochlespirinae (Gastropoda, Conoidea, Turridae). Zoosystema 21, 171–198.
O’Hara, T. D. (2019). The eastern Australian marine parks: biodiversity, assemblage structure, diversity and origin. Report to Parks Australia from the National Environmental Science Program Marine Biodiversity Hub. (Museums Victoria.) Available at https://www.nespmarine.edu.au/system/files/OHara%20Eastern%20Australian%20Marine%20Parks%20-%20biodiversity%20assemblage%20structure%20diversity%20origin_Milestone%205_RPv3%202017.pdf [Verified 9 September 2020].
O’Hara, T. D., Williams, A., Ahyong, S. T., Alderslade, P., Alvestad, T., Bray, D., Burghardt, I., Budaeva, N., Criscione, F., Crowther, A. L., Ekins, M., Eléaume, M., Farrelly, C. A., Finn, J. K., Georgieva, M. N., Graham, A., Gomon, M., Gowlett-Holmes, K., Gunton, L. M., Hallan, A., Hosie, A. M., Hutchings, P., Kise, H., Köhler, F., Konsgrud, J. A., Kupriyanova, E., Lu, C. C., Mackenzie, M., Mah, C., MacIntosh, H., Merrin, K. L., Miskelly, A., Mitchell, M. L., Moore, K., Murray, A., O’Loughlin, P. M., Paxton, H., Pogonoski, J. J., Staples, D., Watson, J. E., Wilson, R. S., Zhang, J., and Bax, N. J. (2020). The lower bathyal and abyssal seafloor fauna of eastern Australia. Marine Biodiversity Records 13, 11.
| The lower bathyal and abyssal seafloor fauna of eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Olivera, B. M., Seger, J., Horvath, M. P., and Fedosov, A. E. (2015). Prey-capture strategies of fish-hunting cone snails: behavior, neurobiology and evolution. Brain, Behavior and Evolution 86, 58–74.
| Prey-capture strategies of fish-hunting cone snails: behavior, neurobiology and evolution.Crossref | GoogleScholarGoogle Scholar | 26397110PubMed |
Powell, A. W. B. (1942). The New Zealand recent and fossil Mollusca of the Family Turridae with general notes on turrid nomenclature and systematics. Bulletin Auckland Institute and Museum 2, 1–188.
Prashanth, J. R., Brust, A., Jin, A.-H., Alewood, P., Dutertre, S., and Lewis, R. (2014). Cone snail venomics: from novel biology to novel therapeutics. Future Medicinal Chemistry 6, 1659–1675.
| Cone snail venomics: from novel biology to novel therapeutics.Crossref | GoogleScholarGoogle Scholar | 25406006PubMed |
Puillandre, N., Cruaud, C., and Kantor, Y. I. (2010a). Cryptic species in Gemmuloborsonia (Gastropoda: Conoidea). The Journal of Molluscan Studies 76, 11–23.
| Cryptic species in Gemmuloborsonia (Gastropoda: Conoidea).Crossref | GoogleScholarGoogle Scholar |
Puillandre, N., Sysoev, A. V., Olivera, B. M., Couloux, A., and Bouchet, P. (2010b). Loss of planktotrophy and speciation: geographical fragmentation in the deep-water gastropod genus Bathytoma (Gastropoda, Conoidea) in the western Pacific. Systematics and Biodiversity 8, 371–394.
| Loss of planktotrophy and speciation: geographical fragmentation in the deep-water gastropod genus Bathytoma (Gastropoda, Conoidea) in the western Pacific.Crossref | GoogleScholarGoogle Scholar |
Puillandre, N., Lambert, A., Brouillet, S., and Achaz, G. (2012a). ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21, 1864–1877.
| ABGD, Automatic Barcode Gap Discovery for primary species delimitation.Crossref | GoogleScholarGoogle Scholar | 21883587PubMed |
Puillandre, N., Modica, M. V., Zhang, Y., Sirovich, L., Boisselier, M. C., Cruaud, C., Holford, M., and Samadi, S. (2012b). Large-scale species delimitation method for hyperdiverse groups. Molecular Ecology 21, 2671–2691.
| Large-scale species delimitation method for hyperdiverse groups.Crossref | GoogleScholarGoogle Scholar | 22494453PubMed |
Puillandre, N., Koua, D., Favreau, P., Olivera, B. M., and Stoecklin, R. (2012c). Molecular phylogeny, classification and evolution of conopeptides. Journal of Molecular Evolution 74, 297–309.
| Molecular phylogeny, classification and evolution of conopeptides.Crossref | GoogleScholarGoogle Scholar | 22760645PubMed |
Puillandre, N., Bouchet, P., Duda, T. F., Kauferstein, S., Kohn, M., Olivera, B., Watkins, M., and Meyer, C. (2014). Molecular phylogeny and evolution of the cone snails (Gastropoda, Conoidea). Molecular Phylogenetics and Evolution 78, 290–303.
| Molecular phylogeny and evolution of the cone snails (Gastropoda, Conoidea).Crossref | GoogleScholarGoogle Scholar | 24878223PubMed |
Puillandre, N., Fedosov, A. E., Zaharias, P., Aznar-Cormano, L., and Kantor, Y. I. (2017). A quest for the lost types of Lophiotoma (Gastropoda: Conoidea: Turridae): integrative taxonomy in a nomenclatural mess. Zoological Journal of the Linnean Society 181, 243–271.
| A quest for the lost types of Lophiotoma (Gastropoda: Conoidea: Turridae): integrative taxonomy in a nomenclatural mess.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 | 12912839PubMed |
Saitou, N., and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.
| 3447015PubMed |
Simon, C., Franke, A., and Martin, A. (1991). The polymerase chain reaction: DNA extraction and amplification. NATO ASI Series – H. Cell Biology 57, 329–355.
| The polymerase chain reaction: DNA extraction and amplification.Crossref | GoogleScholarGoogle Scholar |
Sysoev, A. (1997). Mollusca Gastropoda: new deep-water turrid gastropods (Conoidea) from eastern Indonesia. Mémoires du Museum National d’Histoire Naturelle 172, 325–355.
Sysoev, A., and Bouchet, P. (2001). New and uncommon turriform gastropods (Gastropoda: Conoidea) from the south-west Pacific. Mémoires du Museum National d’Histoire Naturelle 185, 271–320.
Sysoev, A. V., and Kantor, Y. I. (1990). A new genus and species of ‘Cochlespira-like’ turrids (Gastropoda, Toxoglossa, Turridae). Apex 5, 1–6.
Todd, J. A., and Rawlings, T. A. (2014). A review of the Polystira clade – the Neotropic’s largest marine gastropod radiation (Neogastropoda: Conoidea: Turridae sensu stricto). Zootaxa 3884, 445–491.
| A review of the Polystira clade – the Neotropic’s largest marine gastropod radiation (Neogastropoda: Conoidea: Turridae sensu stricto).Crossref | GoogleScholarGoogle Scholar | 25543802PubMed |
Zaharias, P., Kantor, Y. I., Fedosov, A. E., Criscione, F., Hallan, A., Kano, Y., Bardin, J., and Puillandre, N. (2020). Just the once will not hurt: DNA suggests species lumping over two oceans in deep-sea snails (Cryptogemma). Zoological Journal of the Linnean Society 190, 532–557.
| Just the once will not hurt: DNA suggests species lumping over two oceans in deep-sea snails (Cryptogemma).Crossref | GoogleScholarGoogle Scholar |
