Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE (Open Access)

Morphological and DNA analyses reveal cryptic diversity in Anentome wykoffi (Brandt, 1974) (Gastropoda: Nassariidae), with descriptions of two new species from Thailand

Nithinan Chomchoei A B C , Thierry Backeljau D E , Piyatida Pimvichai F , Ting Hui Ng https://orcid.org/0000-0002-5123-0039 G H and Nattawadee Nantarat https://orcid.org/0000-0003-3317-0041 B C I *
+ Author Affiliations
- Author Affiliations

A PhD Program in Biodiversity and Ethnobiology (International Program), Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, 50200, Thailand.

B Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, 50200, Thailand.

C Applied Parasitology Research Laboratory, Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, 50200, Thailand.

D Royal Belgian Institute of Natural Sciences, Barcoding Facility for Organisms and Tissues of Policy Concern (BopCo), Vautierstraat 29, B-1000 Brussels, Belgium.

E Evolutionary Ecology Group, University of Antwerp, Universiteitsplein 1, B-2610 Antwerp, Belgium.

F Department of Biology, Faculty of Science, Mahasarakham University, Maha Sarakham, 44150, Thailand.

G Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah, Jalan UMS, Kota Kinabalu, 88450, Sabah, Malaysia.

H Lee Kong Chian Natural History Museum, National University of Singapore, 2 Conservatory Drive, 117377, Singapore.

I Environmental Science Research Center, Faculty of Science, Chiang Mai University, Chiang Mai, 50200, Thailand.

* Correspondence to: n_nantarat@yahoo.com

Handling Editor: Gonzalo Giribet

Invertebrate Systematics 37(11) 755-771 https://doi.org/10.1071/IS23019
Submitted: 1 May 2023  Accepted: 6 October 2023  Published: 2 November 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

The assassin snail genus Anentome is widely distributed in South East Asia. In Thailand, the genus comprises at least six species, one of which is Anentome wykoffi, a species that may act as an intermediate host of parasitic trematodes. Recent fieldwork has shown that A. wykoffi is far more common and widespread in Thailand than has been assumed, yet the taxonomy remains poorly known. Therefore, this study explores morphological and DNA sequence (COI and 28S rRNA) variation in A. wykoffi to verify and finetune the taxonomic interpretation of this species. To this end, 12 populations of A. wykoffi were sampled in Thailand. This survey allowed us to preliminarily distinguish three putatively cryptic morphotypes. Shell shape measurements and geometric morphometric analyses revealed significant differences between these morphotypes, whereas SEM observations of the shell sculpture and radula confirmed the consistent separation of the three morphotypes. Finally, a combined phylogenetic and species delimitation analysis of COI and 28S rRNA sequence data showed that the three morphotypes represent three well-supported clades, one of which is sister group to A. cambojiensis. As such, the three morphotypes as defined by (1) the presence or absence of a carinated shoulder, (2) the number of spiral lines on the spira and (3) the pattern of the central cusps on the central radular tooth, are interpreted as three different species under the morphological and phylogenetic species concepts but also likely under the biological species concept, viz. A. wykoffi (sensu stricto), A. longispira sp. nov. and A. khelangensis sp. nov. The three cryptic species are (re)described and the implications of separation are briefly discussed.

ZooBank: urn:lsid:zoobank.org:pub:B39722E6-C915-4FA4-B03B-C15836B0DCAE

Keywords: biodiversity, Gastropoda, Mollusca, morphology, morphometrics, phylogeny, systematics, taxonomy.

References

Adams A (1855) Description of two new genera and several new species of Mollusca, from the collection of Hugh Cuming Esq. Proceedings of the Zoological Society of London 23, 119-124.
| Google Scholar |

Akaike H (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716-723.
| Crossref | Google Scholar |

Brandt RAM (1974) The non-marine aquatic Mollusca of Thailand. Archiv für Molluskenkunde 105, 1-423.
| Google Scholar |

Butboonchoo P, Wongsawad C, Wongsawad P, Chai JY (2020) Morphology and molecular identification of Echinostoma revolutum and Echinostoma macrorchis in freshwater snails and experimental hamsters in upper northern Thailand. The Korean Journal of Parasitology 58, 499-511.
| Crossref | Google Scholar | PubMed |

Chantima K, Chai JY, Wongsawad C (2013) Echinostoma revolutum: freshwater snails as the second intermediate hosts in Chiang Mai, Thailand. The Korean Journal of Parasitology 51, 183-189.
| Crossref | Google Scholar | PubMed |

Chantima K, Suk-Ueng K, Kampan M (2018) Freshwater snail diversity in Mae Lao agricultural basin (Chiang Rai, Thailand) with a focus on larval trematode infections. The Korean Journal of Parasitology 56, 247-257.
| Crossref | Google Scholar | PubMed |

Chisholm LA, Morgan JAT, Adlard RD, Whittington ID (2001) Phylogenetic analysis of the Monocotylidae (Monogenea) inferred from 28S rDNA sequences. International Journal for Parasitology 31, 1537-1547.
| Crossref | Google Scholar | PubMed |

Chomchoei N, Wongsawad C, Nantarat N (2018) Investigation of cryptic diversity and occurrence of echinostome metacercariae infection in Anentome helena (von dem Busch, 1847). Asian Pacific Journal of Tropical Medicine 11, 590-596.
| Crossref | Google Scholar |

Chomchoei N, Backeljau T, Segers B, Wongsawad C, Butboonchoo P, Nantarat N (2022) Morphological and molecular characterization of larval trematodes infecting the assassin snail genus Anentome in Thailand. Journal of Helminthology 96, E52.
| Crossref | Google Scholar | PubMed |

Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657-1659.
| Crossref | Google Scholar | PubMed |

Coppois G, De Vos L (1986) Two different striation patterns of the protoconch in Galapagos Bulimulidae: an SEM study. Journal of Molluscan Studies 52, 106-109.
| Crossref | Google Scholar |

Cossmann AE (1901) ‘Essais de Palé oconchologie comparée. Vol. 4. Paris.’ (The Author and Société d’Editions Scientifiques) [In French]

Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
| Crossref | Google Scholar | PubMed |

Dellicour S, Flot JF (2018) The hitchhiker’s guide to single-locus species delimitation. Molecular Ecology Resources 18, 1234-1246.
| Crossref | Google Scholar | PubMed |

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 | PubMed |

Food and Agriculture Organization of the United Nations (2021) Graphic overview: hydrological basins in Asia. Available at https://data.apps.fao.org/catalog/dataset/ee616dc4-3118-4d67-ba05-6e93dd3e962f/resource/14e02901-31b4-4eef-bd48-e848e459a6be

Fujisawa T, Barraclough TG (2013) Delimiting species using single-locus data and the generalized mixed yule coalescent approach: a revised method and evaluation on simulated data sets. Systematic Biology 62, 707-724.
| Crossref | Google Scholar | PubMed |

Galindo LA, Puillandre N, Utge J, Lozouet P, Bouchet P (2016) The phylogeny and systematics of the Nassariidae revisited (Gastropoda, Buccinoidea). Molecular Phylogenetics and Evolution 99, 337-353.
| Crossref | Google Scholar | PubMed |

Galindo LA, Kool HH, Dekker H (2017) Review of the Nassarius pauperus (Gould, 1850) complex (Nassariidae): part 3, reinstatement of the genus Reticunassa, with the description of six new species. European Journal of Taxonomy 2017, 1-43.
| Crossref | Google Scholar |

Guindon S, Delsuc F, Dufayard JF, Gascuel O (2009) Estimating maximum likelihood phylogenies with PhyML. Methods in Molecular Biology 537, 113-137.
| Crossref | Google Scholar | PubMed |

Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42, 182-192.
| Crossref | Google Scholar |

Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111-120.
| Crossref | Google Scholar | PubMed |

Kittivorachate R, Yangyuen C (2004) Molluscs in the Ubolratana Reservoir, Khon Kaen. Kasetsart Journal (Natural Science) 139, 131-139.
| Google Scholar |

Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11, 353-357.
| Crossref | Google Scholar | PubMed |

Köhler F, Seddon M, Bogan AE, Van Tu D, Sri-aroon P, Allen D (2010) Chapter 4. The status and distribution of freshwater molluscs of the Indo-Burma region. In ‘The status and distribution of freshwater biodiversity in Indo-Burma’. (Eds DJ Allen, WRT Darwall, KG Smith) pp. 66–89. (IUCN: Cambridge, UK, and Gland, Switzerland)

Krailas D, Chotesaengsri S, Dechruksa W, Namchote S, Chuanprasit C, Veeravechsukij N, Boonmekam D, Koonchornboon T (2012) Species diversity of aquatic mollusks and their cercarial infections; Khao Yai National Park, Thailand. The Journal of Tropical Medicine and Parasitology 35, 37-47.
| 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 | PubMed |

Lee CT, Huang CW, Hwang CC, Sutcharit C, Jirapatrasilp P (2022) Arboreal snail genus Amphidromus Albers, 1850 of Southeast Asia: shell polymorphism of Amphidromus cruentatus (Morelet, 1875) revealed by phylogenetic and morphometric analyses. PLoS One 17, e0272966.
| Crossref | Google Scholar | PubMed |

Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110-1116.
| Crossref | Google Scholar |

Mekong River Commission (2010) Mekong fisheries and mainstream dams. In ‘Mekong River Commission strategic environmental assessment of hydropower on the Mekong mainstream’. (Ed. E Baran) pp. 1–146. (ICEM: Hanoi, Vietnam)

Neiber MT, Glaubrecht M (2019) Oligohalinophila, a new genus for the brackish water assassin snail Canidia dorri Wattebled, 1886 from Vietnam (Buccinoidea: Nassariidae: Anentominae). Journal of Molluscan Studies 85, 280-283.
| Crossref | Google Scholar |

Nerurkar S, Shimpi GG, Apte D (2020) First record of Nassarius fuscus (Hombron & Jacquinot, 1848) from the west coast of India, with the description of its sister species Nassarius arewarensis n. sp. (Buccinoidea: Nassariidae). Journal of Molluscan Studies 86, 240-248.
| Crossref | Google Scholar |

Olivier L, Schneiderman M (1956) A method for estimating the density of aquatic snail populations. Experimental Parasitology 5, 109-117.
| Crossref | Google Scholar | PubMed |

Puillandre N, Brouillet S, Achaz G (2021) ASAP: Assemble Species by Automatic Partitioning. Molecular Ecology Resources 21, 609-620.
| Crossref | Google Scholar | PubMed |

Rohlf FJ (2015) The tps series of software. Hystrix, the Italian Journal of Mammalogy 26(9), 9-12.
| Crossref | Google Scholar |

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539-542.
| Crossref | Google Scholar | PubMed |

Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large datasets. Molecular Biology and Evolution 34, 3299-3302.
| Crossref | Google Scholar | PubMed |

Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406-425.
| Crossref | Google Scholar | PubMed |

San Mauro D, Agorreta A (2010) Molecular systematics: a synthesis of the common methods and the state of knowledge. Cellular and Molecular Biology Letters 15, 311-341.
| Crossref | Google Scholar | PubMed |

Stanicka A, Maciaszek R, Cichy A, Templin J, Świderek W, Żbikowska E, Labecka AM (2022) Unwanted ‘hitchhikers’ of ornamental snails: a case report of digeneans transported via the international pet trade. The European Zoological Journal 89, 601-607.
| Crossref | Google Scholar |

Strong EE, Galindo LA, Kantor YI (2017) Quid est Clea helena? Evidence for a previously unrecognized radiation of assassin snails (Gastropoda: Buccinoidea: Nassariidae). PeerJ 5, e3638.
| Crossref | Google Scholar | PubMed |

Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A (2018) Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evolution 4, vey016.
| Crossref | Google Scholar | PubMed |

Sullivan J (2005) Maximum-likelihood methods for phylogeny estimation. Methods in Enzymology 395, 757-779.
| Crossref | Google Scholar |

Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673-4680.
| Crossref | Google Scholar | PubMed |

von dem Busch G (1847) Melania. In ‘Abbildungen und beschreibungen neuer oder wenig gekannter conchylien, unter mithülfe mehrer deutscher conchyliologen’. (Ed. RA Philippi) p. 170. (T. Fischer: Cassel) [In German]

Wiroonpan P, Chontananarth T, Purivirojkul W (2021) Cercarial trematodes in freshwater snails from Bangkok, Thailand: prevalence, morphological and molecular studies, and human parasite perspective. Parasitology 148, 366-383.
| Crossref | Google Scholar | PubMed |

Wiroonpan P, Chontananarth T, Chai JY, Purivirojkul W (2022) High diversity of trematode metacercariae that parasitize freshwater gastropods in Bangkok, Thailand, and their infective situations, morphologies and phylogenetic relationships. Parasitology 149, 913-933.
| Crossref | Google Scholar | PubMed |

Yang J, Zhang S (2011) The radular morphology of Nassariidae (Gastropoda : Caenogastropoda) from China. Chinese Journal of Oceanology and Limnology 29, 1023-1032.
| Crossref | Google Scholar |

Yodsiri S, Wongpakam K, Ardharn A, Senakun C, Khumkratok S (2017) Population genetic structure and genetic diversity in twisted-jaw fish, Belodontichthys truncatus Kottelat & Ng, 1999 (Siluriformes : Siluridae), from Mekong basin. International Journal of Zoology 2017, 1-7.
| Google Scholar |

Yutemsuk N, Krailas D, Anancharoenkit C, Phanpeng L, Dechruksa W (2017) Trematode infections of freshwater snails genus Clea A. Adams, 1855 in the reservoir of lower northeast Thailand. Joint International Tropical Medicine Meeting 6, 7-16.
| Google Scholar |

Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 2869-2876.
| Crossref | Google Scholar | PubMed |

Zou S, Li Q, Kong L, Yu H, Zheng X (2011) Comparing the usefulness of distance, monophyly and character-based dna barcoding methods in species identification: a case study of Neogastropoda. PLoS One 6, e26619.
| Crossref | Google Scholar | PubMed |