Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-22T21:31:21.988Z Has data issue: false hasContentIssue false
  • English
  • Français

First insights towards the population genetic structure and the phylogeographic status of the horse mussel (Modiolus barbatus) from the eastern Mediterranean

Published online by Cambridge University Press:  27 December 2018

Ioannis A. Giantsis ,
Athanasios Exadactylos ,
Konstantinos Feidantsis  and
Basile Michaelidis
Ioannis A. Giantsis
Affiliation:
Department of Animal Science, Technological Educational Institute of Western Macedonia, 53100, Florina, Greece
Athanasios Exadactylos
Affiliation:
Department of Ichthyology and Aquatic Environment, University of Thessaly, 38446, Volos, Greece
Konstantinos Feidantsis
Affiliation:
Laboratory of Animal Physiology, Department of Zoology, Faculty of Science, School of Biology, University of Thessaloniki, GR-54124 Thessaloniki, Greece
Basile Michaelidis*
Affiliation:
Laboratory of Animal Physiology, Department of Zoology, Faculty of Science, School of Biology, University of Thessaloniki, GR-54124 Thessaloniki, Greece
*
Author for correspondence: B. Michaelidis, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The horse mussel Modiolus barbatus is a marine benthic bivalve, distributed mainly in the Mediterranean basin, that constitutes a fishery product of high economic importance and a promising candidate for aquaculture. The current study provides the first insights regarding the genetic profile of M. barbatus populations from the eastern Mediterranean, by analysis of a partial segment of the mitochondrial COI gene in individuals collected from five sampling localities within the Aegean Sea. To the best of our knowledge, the derived haplotypes represent the first DNA barcodes of M. barbatus from the entire Mediterranean region. Maximum likelihood phylogenetic analysis revealed that M. barbatus from the North Sea and M. barbatus from the eastern Mediterranean may not belong to the same species and as a consequence, there might be three species of the genus Modiolus in Europe. On the other hand, eastern Mediterranean M. barbatus haplotypes were found to be more closely related to the Asian-Pacific Modiolus species. All geographic populations analysed displayed high levels of genetic diversity, in terms of haplotype and nucleotide diversity and a considerable number of unique alleles. Divergence among populations was found at generally low levels, corresponding with the majority of pairwise Fst values not being significant. These findings suggest no population structure and high levels of gene flow, a common feature observed in marine bivalves with long pelagic larval phases.

Keywords

Cytochrome oxidase IDNA barcodingMediterranean SeaModiolus barbatusphylogeographyThermaikos Gulf
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 5 , August 2019 , pp. 1111 - 1118
Copyright
Copyright © Marine Biological Association of the United Kingdom 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Banci, KR, Mori, GM, Oliveira, MA, de Paganelli, FL, Pereira, MR and Pinheiro, MAA (2017) Can environmental pollution by metals change genetic diversity? Ucides cordatus (Linnaeus, 1763) as a study case in Southeastern Brazilian mangroves. Marine Pollution Bulletin 116, 440–447.Google Scholar
Barco, A, Raupach, MJ, Laakmann, S, Neumann, H and Knebelsberger, T (2016) Identification of North Sea molluscs with DNA barcoding. Molecular Ecology Resources 16, 288–297.Google Scholar
Castresana, J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.Google Scholar
Cornuet, JM, Santos, F, Beaumont, MA, Robert, CP, Marin, JM, Balding, DJ, Guillemaud, T and Estoup, A (2008) Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24, 2713–2719.Google Scholar
De La Rosa-Velez, J, Farfan, C and Cervantes-Franco, MA (2000) Geographic pattern of genetic variation in Modiolus capax (Conrad, 1837) from the Gulf of California. Ciencias Marinas 26, 585–606.Google Scholar
Drummond, AJ, Suchard, MA, Xie, D and Rambaut, A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.Google Scholar
Excoffier, L, Laval, G and Schneider, S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics 1, 47–50.Google 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.Google Scholar
Giantsis, IA, Abatzopoulos, TJ, Angelidis, P and Apostolidis, AP (2014 a) Mitochondrial control region variability in Mytilus galloprovincialis populations from the Central-Eastern Mediterranean Sea. International Journal of Molecular Sciences 15, 11614–11625.Google Scholar
Giantsis, IA, Kechagia, S and Apostolidis, AP (2015) Evaluating the genetic status of the IUCN vulnerable endemic Macedonian shad (Alosa macedonica, Vinciguerra, 1921) from Lake Volvi. Journal of Applied Ichthyology 31, 184–187.Google Scholar
Giantsis, IA, Mucci, N, Randi, E, Abatzopoulos, TJ and Apostolidis, AP (2014 b) Microsatellite variation of mussels (Mytilus galloprovincialis) in central and eastern Mediterranean: genetic panmixia in the Aegean and the Ionian Seas. Journal of the Marine Biological Association of the United Kingdom 94, 797–809.Google Scholar
Geraghty, PT, Williamson, JE, Macbeth, WG, Wintner, SP, Harry, AV, Ovenden, JR and Gillings, MR (2013) Population expansion and genetic structure in Carcharhinus brevipinna in the Southern Indo-Pacific. PLoS ONE 8, e75169.Google Scholar
Gérard, K, Bierne, N, Borsa, P, Chenuil, A and Féral, J-P (2008) Pleistocene separation of mitochondrial lineages of Mytilus spp. mussels from northern and southern hemispheres and strong genetic differentiation among southern populations. Molecular Phylogenetics and Evolution 49, 84–91.Google Scholar
Gutierrez, AP, Turner, F, Gharbi, K, Talbot, R, Lowe, NR, Peñaloza, C and Houston, RD (2017) Development of a medium density combined-species SNP array for Pacific and European oysters (Crassostrea gigas and Ostrea edulis). G3: Genes, Genomes, Genetics 7, 2209–2218.Google Scholar
Halanych, KM, Vodoti, ET, Sundberg, P and Dahlgren, TG (2013) Phylogeography of the horse mussel Modiolus modiolus. Journal of the Marine Biological Association of the United Kingdom 93, 1857–1869.Google Scholar
Hassan, AA, El Nahas, SM, Kumar, S, Godithala, PS and Roushdy, K (2009) Mitochondrial D-loop nucleotide sequences of Egyptian river buffalo: variation and phylogeny studies. Livestock Science 125, 37–42.Google Scholar
Hebert, PDN, Cywinska, A, Ball, SL and De Waard, JR (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London: Series B Biological Sciences 270, 313–321.Google Scholar
Kaouèche, M, Bahri-Sfar, L, González-Wangüemert, M, Pérez-Ruzafa, Á and Ben Hassine, O (2011) Allozyme and mtDNA variation of white seabream Diplodus sargus populations in a transition area between western and eastern Mediterranean basins (Siculo-Tunisian Strait). African Journal of Marine Science 33, 79–90.Google Scholar
Kartavtsev, YP and Nikiforov, SM (1993) Evaluation of the effective size of the Pacific mussel Mytilus trossulus populations from Peter the Great Bay, Sea of Japan based on allele frequency variability among allozyme loci. Russian Journal of Genetics 29, 476–489. In Russian, translated into English.Google Scholar
Katsikatsou, M, Anestis, A, Pörtner, HO, Kampouris, T and Michaelidis, B (2011) Field studies on the relation between the accumulation of heavy metals and metabolic and HSR in the bearded horse mussel Modiolus barbatus. Comparative Biochemistry and Physiology Part C 153, 133–140.Google Scholar
Koehn, RK (1978) Physiology and biochemistry of enzyme variation: the interface of ecology and population genetics. In Brussard, PF (ed.), Ecological Genetics: The Interface. New York, NY: Springer, pp. 51–72.Google Scholar
Koehn, RK, Milkman, R and Mitton, JB (1976) Population genetics of marine pelecypods. IV. Selection, migration and genetic differentiation in the blue mussel Mytilus edulis. Evolution 30, 2–32.Google Scholar
Krestenitis, YN, Kombiadou, KD and Androulidakis, YS (2012) Interannual variability of the physical characteristics of North Thermaikos Gulf (NW Aegean Sea). Journal of Marine Systems 96–97, 132–151.Google Scholar
Leigh, JW and Bryant, D (2015) PopART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.Google Scholar
Ladoukakis, ED and Zouros, E (2017) Evolution and inheritance of animal mitochondrial DNA: rules and exceptions. Journal of Biological Research (Greece) 24, 1–7.Google Scholar
Lallias, D, Stockdale, R, Boudry, P, Lapegue, S and Beaumont, AR (2009) Characterization of ten microsatellite loci in the blue mussel Mytilus edulis. Journal of Shellfish Research 28, 547–551.Google Scholar
Larraín, MA, Díaz, NF, Lamas, C, Uribe, C and Araneda, C (2014) Traceability of mussel (Mytilus chilensis) in southern Chile using microsatellite molecular markers and assignment algorithms: exploratory survey. Food Research International 62, 104–110.Google Scholar
Larsson, J, Lönn, M, Lind, EE, Świeżak, J, Smolarz, K and Grahn, M (2016) Sewage treatment plant associated genetic differentiation in the blue mussel from the Baltic Sea and Swedish west coast. PeerJ 4, e2628.Google Scholar
Lok, A, Acarli, S, Serdar, S, Kose, A and Goulletquer, P (2006) Growth and survival rates of bearded horse mussel (Modiolus barbatus Linne, 1758) in Mersin Bay (Turkey). Israeli Journal of Aquaculture 58, 55–61.Google Scholar
Olson, DB, Kourafalou, VH, Johns, WH, Samuels, G and Veneziani, M (2007) Aegean surface circulation from a satellite-tracked drifter array. Journal of Physical Oceanography 37, 1898–1917.Google Scholar
Peharda, M, Ezgeta-Balić, D, Davenport, J and Vrgoč, N (2013) The potential for aquaculture of the bearded horse mussel (Modiolus barbatus) and Noah's Ark shell (Arca noae) in southern Croatia. Aquaculture International 21, 639–653.Google Scholar
Poppe, GT and Goto, Y (2000) European Seashells, Volume II: Scaphopoda, Bivalvia, Cephalopoda. Hackenheim: Conch Books.Google Scholar
Robicheau, BM, Powell, AE, Del Bel, L, Breton, S and Stewart, DT (2017) Evidence for extreme sequence divergence between the male- and female-transmitted mitochondrial genomes in the bivalve mollusc, Modiolus modiolus (Mytilidae). Journal of Zoological Systematics and Evolutionary Research 55, 89–97.Google Scholar
Rozas, J, Ferrer-Mata, A, Sánchez-Delbarrio, JC, Guirao-Rico, S, Librado, P, Ramos-Onsins, SE and Sánchez-Gracia, A (2017) DnaSP 6: DNA sequence polymorphism analysis of large datasets. Molecular Biology and Evolution 34, 3299–3302.Google Scholar
Sanna, D, Cossu, P, Dedola, GL, Scarpa, F, Maltagliati, F, Castelli, A and Casu, M (2013) Mitochondrial DNA reveals genetic structuring of Pinna nobilis across the Mediterranean Sea. PLoS ONE 8, e67372.Google Scholar
Tajima, F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.Google Scholar
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.Google Scholar
Wu, LM, Bai, ZY, Liu, XJ, Jin, C, Yin, H and Li, JL (2016) Comparative analysis of shell color variety and genetic structure among five high-quality freshwater pearl mussel populations. Genetics and Molecular Research 15, 1–12.Google Scholar
Ye, Y, Li, J, Wu, C, Xu, M and Guo, B (2012) Genetic analysis of mussel (Mytilus coruscus) populations on the coast of East China Sea revealed by ISSR-PCR markers. Biochemical Systematics and Ecology 45, 1–6.Google Scholar
Ye, YY, Wu, CW and Li, JJ (2015) Genetic population structure of Macridiscus multifarius (Mollusca: Bivalvia) on the basis of mitochondrial markers: strong population structure in a species with a short planktonic larval stage. PLoS ONE 10, 1–13.Google Scholar
Supplementary material: Image

Giantsis et al. supplementary material

Figure S1

Download Giantsis et al. supplementary material(Image)
Image 2.9 MB
Supplementary material: File

Giantsis et al. supplementary material

Table S1

Download Giantsis et al. supplementary material(File)
File 14.6 KB