First genetic survey on the invasive rayed pearl oyster Pinctada radiata (Leach, 1814) populations of the Balearic Islands (Western Mediterranean)

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Published: Dec 13, 2023
DOI: https://doi.org/10.12681/mms.34195
Keywords:
Invasive species Non-native Balearic Islands Species delimitation Genetic population structure
JOSEBA AGUILO-ARCE
Department of Biology, Universitat de les Illes Balears, Ctra. de Valldemossa km 7.5, 07122 Palma de Mallorca, Spain & (Present address) Department of Bioscience, Biotechnology and Environment, Università degli Studi di Bari Aldo Moro, Via Orabona
JOANA F. FERRAGUT
Department of Biology, Universitat de les Illes Balears, Ctra. de Valldemossa km 7.5, 07122 Palma de Mallorca, Spain
LYDIA PNG-GONZALEZ
Centro Oceanográfico de Baleares (IEO, CSIC), Muelle de Poniente s/n, 07015 Palma de Mallorca, Spain
AINA CARBONELL
Centro Oceanográfico de Baleares (IEO, CSIC), Muelle de Poniente s/n, 07015 Palma de Mallorca, Spain
MARÍA CAPA
Department of Biology, Universitat de les Illes Balears, Ctra. de Valldemossa km 7.5, 07122 Palma de Mallorca, Spain & Balearic Biodiversity Centre, Universitat de les Illes Balears, Ctra. de Valldemossa km 7.5, 07122 Palma de Mallorca, Spain
Abstract

A survey of the invasive pearl oyster Pinctada radiata along the Balearic Archipelago was conducted based on the COI mitochondrial marker. Results confirmed the identity of the specimens as P. radiata. The Balearic populations are certainly of Indo-Pacific origin but not from the Persian Gulf nor from other introduced populations in the eastern or central Mediterranean, therefore the precise origin remains to be discovered. Despite the small number of samples from the Persian Gulf compared to the Mediterranean, the haplotype diversity is higher in the native populations compared to the non-native.

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References
Abbott, R.T., 1974. American Seashells: the marine Mollusca of the Atlantic and Pacific coasts of North America. Second edition. Van Nostrand Reinhold, New York, 663 pp.
Allendorf, F.W., Lundquist, L.L., 2003. Introduction: population biology, evolution, and control of invasive species. Conservation Biology, 17 (1), 24-30.
Azzurro, E., Golani, D., Bucciarelli, G., Bernardi, G., 2006. Genetics of the early stages of invasion of the Lessepsian rabbitfish Siganus luridus. Journal of Experimental Marine Biology and Ecology, 333 (2), 190-201.
Azzurro, E., Nourigat, M., Cohn, F., Ben Souissi, J., Bernardi, G., 2022. Right out of the gate: the genomics of Lessepsian invaders in the vicinity of the Suez Canal. Biological Invasions, 24 (4), 1117-1130.
Ballesteros, E., Marsinyach, E., Bagur, M., Sales, M., Movilla, J. et al., 2020. The pearl oyster Pinctada imbricata radiata (Leach, 1814) (Bivalvia: Pteriidae) reaches Minorca, Balearic Islands. Bolletí de la Societat d’Història Natural de les Balears, 63, 97-108.
Barbieri, M., Maltagliati, F., Di Giuseppe, G., Cristo, B., Lardicci, C. et al., 2011. DNA barcoding identification of the exotic mussel Xenostrobus securis and new records in Western Mediterranean. Biologia Marina Mediterranea, 18 (1), 232.
Barbieri, M.C., Deidun, A., Maltagliati, F., Zenetos, A., Tlig-Zouari, S. et al., 2013. First data on genetic diversity of the small pearl oyster Pinctada radiata (Leach, 1814) in Mediterranean populations by means of the mitochondrial COX1 marker. Commission Internationale pour l’Exploration Scientifique de la Mer Mediterranee, 40, 711.
Barbieri, M., Deidun, A., Maltagliati, F., Castelli, A., 2016. A contribution to the phylogeography of Pinctada imbricata radiata (Leach, 1814) (Bivalvia: Pteriidae) from the Eastern Mediterranean Sea by means of the mitochondrial COI marker. Italian Journal of Zoology, 83 (1), 113-120.
Bariche, M., Bernardi, G., 2009. Lack of a genetic bottleneck in a recent Lessepsian bioinvader, the blue-barred parrotfish, Scarus ghobban. Molecular Phylogenetics and Evolution, 53 (2), 592-595.
Bernardi, G., Azzurro, E., Golani, D., Miller, M.R., 2016. Genomic signatures of rapid adaptive evolution in the bluespotted cornetfish, a Mediterranean Lessepsian invader. Molecular ecology, 25 (14), 3384-3396.
Chu, K.H., 2006. Low genetic differentiation among widely separated populations of the pearl oyster Pinctada fucata as revealed by AFLP. Journal of Experimental Marine Biology and Ecology, 333 (1), 140-146.
Clement, M., Posada, D., Crandall, M.C.D.P.K., 2000. TCS: a computer program to estimate gene genealogies. Molecular ecology, 9 (10), 1657-1660.
Combosch, D.J., Collins, T.M., Glover, E.A., Graf, D.L., Harper, E.M. et al., 2017. A family-level tree of life for bivalves based on a Sanger-sequencing approach. Molecular Phylogenetics and Evolution, 107, 191-208.
Cunha, R.L., Blanc, F., Bonhomme, F., Arnaud-Haond, S., 2011. Evolutionary patterns in pearl oysters of the genus Pinctada (Bivalvia: Pteriidae). Marine Biotechnology, 13 (2), 181-192.
Derbali, A., Jarboui, O., Ghorbel, M., 2011. Distribution, abundance and population structure of Pinctada radiata (Mollusca: Bivalvia) in southern Tunisian waters (Central Mediterranean). Cahiers de Biologie Marine, 52 (1), 23-31.
Excoffier, L., Lischer, H.E., 2010. Arlequin suite ver. 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10 (3), 564-567.
Folmer, O., Black, M., Wr, H., 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 (5), 294-299.
Galanidi, M., Aissi, M., Ali, M., Bakalem, A., Bariche, M. et al., 2023. Validated Inventories of Non-Indigenous Species (NIS) for the Mediterranean Sea as Tools for Regional Policy and Patterns of NIS Spread. Diversity, 15 (9), 962.
Gavrilović, A., Piria, M., Guo, X.Z., Jug-Dujaković, J., Ljubučić, A. et al., 2017. First evidence of establishment of the rayed pearl oyster, Pinctada imbricata radiata (Leach, 1814), in the eastern Adriatic Sea. Marine Pollution Bulletin, 125 (1-2), 556-560.
Gofas, S., Zenetos A., 2003. Exotic molluscs in the Mediterranean basin: current status and perspectives. Oceanography and marine biology: an annual review, 41, 237-277.
Giribet, G., Wheeler, W. 2002. On bivalve phylogeny: a highlevel analysis of the Bivalvia (Mollusca) based on combined morphology and DNA sequence data. Invertebrate Biology, 121 (4), 271-324.
Harrington, B., Gould, T., Hurst, N., MenTaLgu, Y, 2004/2005. Inkscape. http://www.inkscape.org/ (Accessed 3 February 2023).
Hassan, M., Harmelin-Vivien, M., Bonhomme, F., 2003. Lessepsian invasion without bottleneck: example of two rabbitfish species (Siganus rivulatus and Siganus luridus). Journal of Experimental Marine Biology and Ecology, 291 (2), 219-232.
Jameson, H.L., 1901. On the identity and distribution of the mother-of-pearl oysters; with a revision of the sub-genus Margaritifera. Proceedings of the Zoological Society of London, 70 (2), 372-394.
Kapli, P., Lutteropp, S., Zhang, J., Kobert, K., Pavlidis, P. et al., 2017. Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics, 33 (11), 1630-1638.
Katoh, K., Rozewicki, J., Yamada, K.D., 2019. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in bioinformatics, 20 (4), 1160-1166.
Kumar, S., Stecher, G., Li, M., Knyaz, C., Tamura, K., 2018. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35 (6), 1547-1549.
Lee, C.E., 2002. Evolutionary genetics of invasive species. Trends in ecology & evolution, 17 (8), 386-391.
Leigh, J.W., Bryant, D., 2015. POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6 (9), 1110-1116.
Meyer, J.B., Cartier, L.E., Pinto-Figueroa, E.A., Krzemnicki, M.S., Hänni, H.A. et al., 2013. DNA fingerprinting of pearls to determine their origins. PloS one, 8 (10), e75606.
Minh, B.Q., Nguyen, M.A.T., von Haeseler, A., 2013. Ultrafast Approximation for Phylogenetic Bootstrap. Molecular Biology and Evolution, 30 (5), 1188-1195.
Monterosato, T.A., 1878. Enumerazione e sinonimia delle conchiglie mediterranee. Giornale de Scienze Naturali ed Economiche de Palermo, 13, 61-115.
MolluscaBase Εds., 2023a. MolluscaBase. Pinctada imbricata Röding, 1798. https://www.marinespecies.org/ aphia.php?p=taxdetails&id=207901 (Accessed 17 November 2023).
MolluscaBase Εds., 2023b. MolluscaBase. Pteria loveni (Dunker, 1879). https://www.marinespecies.org/ aphia.php?p=taxdetails&id=208447 (Accessed 17 November 2023).
MolluscaBase Εds., 2023c. MolluscaBase. Pinctada martensii (Dunker, 1880). https://www.marinespecies.org/ aphia.php?p=taxdetails&id=592603 (Accessed 17 November 2023).
Parker, I.M., Rodriguez, J., Loik, M.E., 2003. An evolutionary approach to understanding the biology of invasions: local adaptation and general‐purpose genotypes in the weed Verbascum thapsus. Conservation biology, 17 (1), 59-72.
Png-Gonzalez, L., Aguilo-Arce, J., Vázquez-Luis, M., Carbonell, A., 2021. New occurrence of Pinctada imbricata radiata (Leach, 1814) in the Balearic Archipelago (NW Mediterranean Sea). BioInvasions Records, 10 (4), 853-858.
Pons-Moyà, J. Pons, G.X., 2001. Primera cita de Pinctada radiata (Leach, 1814) (Mollusca: Bivalvia: Pteriidae) a les Illes Balears. Llibre de ponencies i resums III Jornades del Medi Ambient de les Illes Balears, Societat d’Historia Natural de les Balears, 126-127.
Rambaut, A., 2006. FigTree. http.tree.bio.ed.ac.uk/software/ figtree (Accessed 3 February 2023). Rius, M., Turon, X., Bernardi, G., Volckaert, F.A., Viard, F., 2015. Marine invasion genetics: from spatio-temporal patterns to evolutionary outcomes. Biological Invasions, 17, 869-885.
Röding, P.F., 1798. Museum Boltenianum sive Catalogus cimeliorum e tribus regnis naturæ quæ olim collegerat Joa. Fried Bolten, M. D. p. d. per XL. annos proto physicus Hamburgensis. Pars secunda continens Conchylia sive Testacea univalvia, bivalvia & multivalvia. Trapp, Hamburg, viii, 199 pp.
Ruiz, G.M., Carlton, J.T., Grosholz, E.D., Hines, A.H., 1997. Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. American zoologist, 37 (6), 621-632.
Scuderi, D., Balistreri, P., Germanà, A., 2019. Are Pinctada radiata (Leach, 1814) and Pinctada fucata (Gould, 1850) (Bivalvia Pteriidae) only synonyms or really different species? The case of some Mediterranean populations. Biodiversity Journal, 10 (4), 415-426.
Tamura, K., Nei, M., 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10 (3), 512-526.
Tëmkin, I., 2010. Molecular phylogeny of pearl oysters and their relatives (Mollusca, Bivalvia, Pterioidea). BMC Evolutionary Biology, 10 (1), 1-28.
Tsirintanis, K., Azzurro, E., Crocetta, F., Dimiza, M., Froglia, C. et al., 2022. Bioinvasion impacts on biodiversity, ecosystem services, and human health in the Mediterranean Sea. Aquatic Invasions, 17 (3), 308-352.
Wada, K.T., Tëmkin, I., 2008. Taxonomy and phylogeny. p. 37- 76. In: The pearl oyster. Southgate, P.C., Lucas, J.S. (Eds). Elsevier, Oxford.
Zenetos, A., Gofas, S., Russo, G., Templado, J., 2004. CIESM Atlas of Exotic Species in the Mediterranean. Vol. 3. Molluscs. F. Briand, Ed., CIESM Publishers, Monaco, 376 pp.
Zenetos, A., Albano, P.G., López Garcia, E., Stern, N., Tsiamis, K. et al., 2022a. Established non-indigenous species increased by 40% in 11 years in the Mediterranean Sea. Mediterranean Marine Science, 23 (1), 196-212.
Zenetos, A., Albano, P., Garcia, E.L., Stern, N., Tsiamis, K. et al., 2022b. Corrigendum to the Review Article (Medit. Mar. Sci. 23/1 2022, 196-212): Established non-indigenous species increased by 40% in 11 years in the Mediterranean Sea. Mediterranean Marine Science, 23 (4), 876-878.
Zenetos, A., Tsiamis, K., Galanidi, M., Carvalho, N., Bartilotti, C. et al., 2022c. Status and Trends in the Rate of Introduction of Marine Non-Indigenous Species in European Seas. Diversity, 14 (12), 1077.
Zhang, J., Kapli, P., Pavlidis, P., Stamatakis, A., 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29 (22), 2869-2876.