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An evolutionary estuarine incursion: molecular differentiation and niche separation in Bornean Indothais snails (Rapaninae, Muricidae)

Published online by Cambridge University Press:  16 March 2021

David J. Marshall Open the ORCID record for David J. Marshall [Opens in a new window]  and
Hussein Taha
David J. Marshall*
Affiliation:
Environmental and Life Sciences, Faculty of Science, Universiti Brunei Darussalam, Brunei Darussalam
Hussein Taha
Affiliation:
Environmental and Life Sciences, Faculty of Science, Universiti Brunei Darussalam, Brunei Darussalam
*
Author for correspondence: David J. Marshall, E-mail: [email protected]
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Abstract

Ecological and biogeographic information for marine gastropods has lagged behind taxonomic, molecular and phylogenetic information, limiting understanding of evolutionary processes. We investigated niche separation and speciation in rapinine whelks that represent a rare deep estuarine penetration by muricid gastropods. We studied the genetic and ecological differentiation of four Indothais morphotypes, distributed along a salinity gradient in Brunei (Borneo, South East Asia). Our molecular analyses, based on three mitochondrial genes (COI, 12S rRNA and 16S rRNA) and one nuclear gene (28S rRNA), revealed three species having the following relationship [Indothais rufotincta (Tan & Sigurdsson, 1996), [I. javanica (Philippi, 1848), [I. gradata (Jonas, 1846)]]]. This pattern coincided with their salinity-related distributions, such that I. rufotincta occurred alone in the open coastal waters, and I. javanica and I. gradata extended into the upper estuary. This suggests speciation through divergent selection and local adaptation, specifically synapomorphic low salinity tolerance by I. javanica and I. gradata. The observed intertidal vertical separation where the species co-occur suggests competitive exclusion of the others by the most-recently evolved I. gradata. This species also showed greatest morphological and genetic variation, and unique niche expansion involving feeding on both hard surface and muddy sediment organisms. Our study presents a novel hypothesis for the speciation of these snails.

Keywords

Gastropodmangrovemorphologyniche divergencephylogenyspeciation
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 101 , Issue 2 , March 2021 , pp. 319 - 329
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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References

Barco, A, Claremont, M, Reid, DG, Houart, R, Bouchet, P, Williams, ST, Cruaud, C, Couloux, A and Oliverio, M (2010) A molecular phylogenetic framework for the Muricidae, a diverse family of carnivorous gastropods. Molecular Phylogenetics and Evolution 56, 1025–1039.CrossRefGoogle ScholarPubMed
Bird, MI, Taylor, D and Hunt, C (2005) Palaeoenvironments of insular Southeast Asia during the Last Glacial Period: a savanna corridor in Sundaland? Quaternary Science Reviews 24, 2228–2242.CrossRefGoogle Scholar
Claremont, M, Reid, DG and Williams, ST (2012) Speciation and dietary specialization in Drupa, a genus of predatory marine snails (Gastropoda: Muricidae). Zoologica Scripta 41, 137–149.CrossRefGoogle Scholar
Claremont, M, Vermeij, GJ, Williams, ST and Reid, DG (2013) Global phylogeny and new classification of the Rapaninae (Gastropoda: Muricidae), dominant molluscan predators on tropical rocky seashores. Molecular Phylogenetics and Evolution 66, 91–102.CrossRefGoogle Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) Jmodeltest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
Frey, MA (2010) The relative importance of geography and ecology in species diversification: evidence from a tropical marine intertidal snail (Nerita). Journal of Biogeography 37, 1515–1528.Google Scholar
Frey, MA and Vermeij, GJ (2008) Molecular phylogenies and historical biogeography of a circumtropical group of gastropods (Genus: Nerita): implications for regional diversity patterns in the marine tropics. Molecular Phylogenetics and Evolution 48, 1067–1086.CrossRefGoogle ScholarPubMed
Guindon, S, Dufayard, JF, Lefort, V, Anisimova, M, Hordijk, W and Gascuel, O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.CrossRefGoogle ScholarPubMed
Hossain, MB and Bamber, RN (2013) New record of a wood-boring isopod, Sphaeroma terebrans (Crustacea: Sphaeromatidae) from Sungai Brunei estuary, Brunei Darussalam. Marine Biodiversity Records, Journal of the Marine Biological Association of the United Kingdom 6, e18. doi: 10.1017/S1755267212001261Google Scholar
Hossain, MB, Marshall, DJ and Venkatramanan, S (2014) Sediment granulometry and organic matter content in the intertidal zone of the Sungai Brunei estuarine system, Northwest coast of Borneo. Carpathian Journal of Earth and Environmental Sciences 9, 231–239.Google Scholar
Hossain, MB, Marshall, DJ and Hall-Spencer, J (2019) Epibenthic community variation along an acidified tropical estuarine system. Regional Studies in Marine Science 32, 100888.CrossRefGoogle Scholar
Klussmann-Kolb, A, Dinapoli, A, Kuhn, K, Streit, B and Albrecht, C (2008) From sea to land and beyond: new insights into the evolution of euthyneuran Gastropoda (Mollusca). BMC Evolutionary Biology 8, 57.CrossRefGoogle Scholar
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.CrossRefGoogle ScholarPubMed
Marshall, DJ (2009) Predatory and reproductive responses of the estuarine whelk Thais gradata (Caenogastropoda: Muricidae) to novel colonization by Musculista senhousia (Bivalvia: Mytilidae). Journal of the Marine Biological Association of the United Kingdom 89, 1387–1393.CrossRefGoogle Scholar
Marshall, DJ and Convey, P (2004) Latitudinal variation in niche specificity of ameronothrid mites (Oribatida). Experimental and Applied Acarology 34, 21–35.CrossRefGoogle Scholar
Marshall, DJ and McQuaid, CD (2020) Metabolic regulation, oxygen limitation and heat tolerance in a subtidal marine gastropod reveal the complexity of predicting climate change vulnerability. Frontiers in Physiology. doi: doi.org/10.3389/fphys.2020.01106.CrossRefGoogle Scholar
Marshall, DJ, Santos, JH, Leung, KYM and Chak, WH (2008) Correlations between gastropod shell dissolution and water chemical properties in a tropical estuary. Marine Environmental Research 66, 422–429.CrossRefGoogle Scholar
Marshall, DJ, Proum, S, Hossain, B, Adam, A, Lim, LH and Santos, JH (2016) Ecological responses to fluctuating and extreme marine acidification: lessons from a tropical estuary (the Brunei Estuarine System). Scientia Bruneiana 15, 1–17.CrossRefGoogle Scholar
Marshall, DJ, Abdelhady, AA, Teck Wah, TD, Mustapha, N, Godeke, SH, De Silva, LC and Hall-Spencer, JM (2019) Biomonitoring acidification using marine gastropods. Science of Total Environment 692, 833–843.CrossRefGoogle ScholarPubMed
Mohamat-Yusuff, F, Zulkifli, SZ, Ismail, A, Harino, H, Yusoff, MK and Arai, T (2010) Imposex in Thais gradata as a biomarker for TBT contamination on the southern coast of Peninsular Malaysia. Water, Air, Soil Pollution 211, 443–457.CrossRefGoogle Scholar
Monaco, CJ, Bradshaw, CJA, Booth, DJ, Gillanders, BM, Schoeman, DS and Nagelkerken, I (2020) Dietary generalism accelerates arrival and persistence of coral-reef fishes in their novel ranges under climate change. Global Change Biology. https://doi.org/10.1111/gcb.15221CrossRefGoogle ScholarPubMed
Morley, CK, Back, S, Van Rensbergen, P, Crevello, P and Lambiase, JJ (2003) Characteristics of repeated, detached, Miocene–Pliocene tectonic inversion events, in a large delta province on an active margin, Brunei Darussalam, Borneo. Journal of Structural Geology 25, 1147–1169.CrossRefGoogle Scholar
Proum, S, Santos, JH, Lim, LH and Marshall, DJ (2016) Metal accumulation in the tissues and shells of Indothais gradata snails inhabiting soft and hard substrata in an acidified tropical estuary (Brunei, South East Asia). Regional Studies in Marine Science 8, 487–497.CrossRefGoogle Scholar
Proum, S, Harley, C, Steele, M and Marshall, DJ (2017) Aerobic and behavioral flexibility allow estuarine gastropods to flourish in rapidly changing and extreme pH conditions. Marine Biology 164, 97.CrossRefGoogle Scholar
Proum, S, Santos, JH, Lim, L-H and Marshall, DJ (2018) Tidal and seasonal variation in carbonate chemistry, pH and salinity for an acidified, tropical estuarine system. Regional Studies in Marine Science 17, 17–27.CrossRefGoogle Scholar
Raven, JGM (2016) Notes on molluscs from NW Borneo. 3. A revision of Taurasia (Gastropoda, Muricidae) and Preangeria (Gastropoda, Buccinidae) with comments on Semiricinula from NW Borneo. Vita Malacologica 15, 77–104.Google Scholar
Reid, DG, Dyal, P, Lozouet, P, Glaubrecht, M and Williams, ST (2008) Mudwhelks and mangroves: the evolutionary history of an ecological association (Gastropoda: Potamididae). Molecular Phylogenetics and Evolution 47, 680–699.CrossRefGoogle Scholar
Ronquist, F, Teslenko, M, Van Der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Rozas, J, Ferrer-Mata, A, Sanchez-Delbarrio, JC, Guirao-Rico, S, Librado, P, Ramos-Onsins, SE and Sanchez-Gracia, A (2017) DnaSP 6: DNA sequence polymorphism analysis of large datasets. Molecular Biology and Evolution 34, 3299–3302.CrossRefGoogle Scholar
Sela, I, Ashkenazy, H, Katoh, K and Pupko, T (2015) GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Research 43, W7–W14.CrossRefGoogle ScholarPubMed
Strong, EE, Gargominy, O, Ponder, WF and Bouchet, P (2008) Global diversity of gastropods (Gastropoda; Mollusca) in fresh water. Hydrobiologia 595, 149–166.CrossRefGoogle Scholar
Strong, EE, Colgan, DJ, Healy, JM, Lydeard, C, Ponder, WF and Glaubrecht, M (2011) Phylogeny of the gastropod superfamily Cerithioidea using morphology and molecules. Zoological Journal of the Linnean Society 162, 43–89.CrossRefGoogle Scholar
Tan, KS (1999) Imposex in Thais gradata and Chicoreus capucinus (Mollusca, Neogastropoda, Muricidae) from the Straits of Johor: a case study using penis length, area and weight as measures of imposex severity. Marine Pollution Bulletin 39, 295–303.CrossRefGoogle Scholar
Tan, KS and Sigurdsson, JB (1996 a) New species of Thais (Neogastropoda, Muricidae) from Singapore, with a re-description of Thais javanica (Philippi, 1848). Journal of Molluscan Studies 62, 517–535.CrossRefGoogle Scholar
Tan, KS and Sigurdsson, JB (1996 b) Two new species of Thais (Mollusca: Neogastropoda: Muricidae) from Peninsular Malaysia and Singapore, with notes on T. tissoti (Petit, 1852) and T. blanfordi (Melvill, 1893) from Bombay, India. The Raffles Bulletin of Zoology 44, 77–107.Google Scholar
Webb, TJ (2012) Marine and terrestrial ecology: unifying concepts, revealing differences. Trends in Ecology and Evolution 27, 535–541.CrossRefGoogle ScholarPubMed
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