The Intertwined Effects of Hydrographic Barriers, Palaeoclimate and Life History on Genetic Structure of Marine Populations: A Case Study of Two Marine Invertebrates


Published: Feb 14, 2023
Keywords:
Mytilus galloprovincialis Palaemon elegans mtDNA microsats Turkish Straits System Black Sea Mediterranean Sea
EVRIM KALKAN TEZCAN
https://orcid.org/0000-0003-0020-2246
ELIZABETH MATHER HEMOND
SELAHATTIN ÜNSAL KARHAN
RAŞIT BILGIN
Abstract

Marine organisms with pelagic planktonic larval stages have high dispersal potential, yet their ranges are restricted by present and historical geographic and oceanographic features. Hydrogeographic features, such as straits and water current patterns, as well as paleoclimate can affect population connectivity, genetic differentiation, and ultimately speciation, but species distributions are also affected by life history characteristics. This study evaluates the effect of the Turkish Straits System (TSS) on the genetic differentiation of two benthic invertebrates with pelagic larvae, the Mediterranean mussel, Mytilus galloprovincialis, and the rockpool prawn, Palaemon elegans, using mitochondrial and nuclear markers (microsatellites for M. galloprovincialis and Histone H3 gene for P. elegans). For both species, the mitochondrial DNA analyses separated the Black Sea and the Eastern Mediterranean (Aegean and Levantine seas) populations into two clusters. In contrast, in both species the nuclear data indicated no differentiation between Black Sea and Eastern Mediterranean populations. The results suggest that for both species, some individuals of Black Sea origin moved south, most likely through the transport of their pelagic larvae via the surface currents of the TSS. However, for the most part, individuals of Mediterranean origin (from Aegean and Levantine seas) were not able to successfully migrate in the opposite direction, though the small differences in the frequencies of migration in this direction indicate the effects of the life history characteristics of the two species on genetic structure.

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References
Aksu, A.E., Hiscott, R.N., Kaminski, M.A., Mudie, P.J., Gillespie, H., et al., 2002. Last glacial-Holocene paleoceanography of the Black Sea and Marmara Sea: stable isotopic, foraminiferal and coccolith evidence. Marine Geology, 190, 119-149.
Avise, J.C., 2000. Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge. Ayers, K.L., Waters, J.M., 2005. Marine biogeographic disjunction in central New Zealand. Marine Biology, 147, 1045-1052.
Ayre, D.J., Minchinton, T.E., Perrin, C., 2009. Does life history predict past and current connectivity for rocky intertidal invertebrates across a marine biogeographic barrier? Molecular Ecology, 18, 1887-1903.
Balabanov, I.P., 2006. Holocene sea-level changes in the northern Black Sea. In: IGCP 521 Second Plenary Meeting, Odessa, Ukraine, 20-28 August, Abstracts volume, pp. 21-23.
Bandelt, H.J., Forster, P., Röhl, A., 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37-48.
Besiktepe, S., Sur, H.I., Özsoy, E., Latif, M.A., Oğuz, T. et al., 1994. The circulation and hydrography of the Marmara Sea. Progress in Oceanography, 34, 285-334.
Bierne, N., David, P., Boudry, P., Bonhomme, F., 2002. Assortative fertilization and selection at larval stage in the mussels Mytilus edulis and M. galloprovincialis. Evolution, 56, 292-298.
Bilgin, R., Utkan, M.A., Kalkan, E., Karhan, S.U., Bekbölet, M., 2015. DNA barcoding of twelve shrimp species (Crustacea: Decapoda) from Turkish seas reveals cryptic diversity. Mediterranean Marine Sciences, 16, 36-45.
Bilgin, R., 2007. Kgtests: a simple Excel Macro program to detect signatures of population expansion using microsatellites. Molecular Ecology Notes, 7 (3), 416-417.
Boissin, E., Micu, D., Janczyszyn-Le Goff, M., Neglia, V., Bat, L. et al., 2016. Contemporary genetic structure and post-glacial demographic history of the black scorpionfish, Scorpaena porcus, in the Mediterranean and the Black seas. Molecular Ecology, 25, 2195-2209.
Boissin, E., Stohr, S., Chenuil, A., 2011. Did vicariance and adaptation drive cryptic speciation and evolution of brooding in Ophioderma longicauda (Echinodermata: Ophiuroidea), a common Atlanto-Mediterranean ophiuroid? Molecular Ecology, 20, 4737-4755.
Bolnick, D.I., Fitzpatrick, B.M., 2007. Sympatric speciation: models and empirical evidence. Annual Review of Ecology, Evolution, and Systematics, 38, 459-487.
Bouckaert, R., Heled, J., Kuhnert, D., Vaughan, T., Wu, C-H., et al., 2014. BEAST 2: a software platform for Bayesian evolutionary analysis. PLOS Computational Biology, 10 (4), e1003537. https://doi.org/10.1371/journal.pcbi.1003537
Briggs, J.C., Bowen, B.W., 2012. A realignment of marine biogeographic provinces with particular reference to fish distributions. Journal of Biogeography, 39, 12-30.
Cagatay, M.N., Gorur, N., Algan, O., Eastoe, C.J., Tchapalyga, A., et al. 2002. Late Glacial–Holocene paleoceanography of the Sea of Marmara: timing connections with the Mediterranean and the Black Seas. Marine Geology, 167, 191-206.
Castric, V., Bernatchez, L., Belkhir, K., Bonhomme, F., 2002. Heterozygote deficiencies in small lacustrine populations of brook charr Salvelinus fontinalis Mitchill (Pisces, Salmonidae): a test of alternative hypothesis. Heredity, 89, 27-35.
Cetin, C., Furman, A., Bilgin, R., Kalkan, E., 2015. Cytonuclear discordance in the marbled crab, Pachygrapsus marmoratus (Fabricius, 1787) along the Mediterranean coasts of Turkey. In: Ecology and Evolutionary Biology Symposium, Turkey - Book of Abstracts.
Colgan, D.J., McLauchlan, A., Wilson, G.D.F., Livingston, S.P., et al. 1998. Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Australian Journal of Zoology, 46, 419-437.
Coulson, L.A., 2006. Investigations of Demographic and Ecological Processes Setting the Geographic Range Limit of the Intertidal Whelk, Morula marginalba. Honours, University of Wollongong, NSW, Australia.
Coyne, J.A., Orr, H.A., 2004. Speciation. Sinauer Associates Sunderland, MA.
Cunningham, C.W., Collins, T.M., 1998. Beyond area relationships: extinction and recolonization in molecular marine biogeography. p 297-322. In: Molecular Ecology and Evolution: Approaches and Applications. Schierwater, B., Streit, B., Wagner, G. P., Desalle, R. (Eds.). Birkhauser, Basel, Switzerland.
Dahlgren, T.G., Weinberg, J.R., Halanych, K.M., 2000. Phylogeography of the ocean quahog (Arctica islandica): influences of paleoclimate on genetic diversity and species range. Marine Biology, 137, 487-495.
Deli, T., Kalkan, E., Karhan, S.U., Uzunova, S., Keikhosravi, A. et al., 2018a. Parapatric genetic divergence among deep evolutionary lineages in the Mediterranean green crab, Carcinus aestuarii (Brachyura, Portunoidea, Carcinidae), accounts for a sharp phylogeographic break in the Eastern Mediterranean. BMC Evolutionary Biology, 18 (1), 1-21.
Deli, T., Pfaller, M., Schubart, C.D., 2018b. Phylogeography of the littoral prawn species Palaemon elegans (Crustacea: Caridea: Palaemonidae) across the Mediterranean Sea unveils disparate patterns of population genetic structure and demographic history in the two sympatric genetic types II and III. Marine Biodiversity, 48, 1979-2001.
Deli, T., Pfaller, M., Schubart, C.D., 2017. Phylogeography of the littoral prawn species Palaemon elegans(Crustacea: Caridea: Palaemonidae) across the MediterraneanSea unveils disparate patterns of population genetic structureand demographic history in the two sympatric genetic types II and III. Marine Biodiversity, 48, 1979 - 2001.
Dobretsov, S.V., Miron, G., 2001. Larval and post-larval vertical distribution of them mussel Mytilus edulis in the White Sea. Marine Ecology Progress Series, 218, 179-187.
Edgar, G.J., 2000. Australian Marine Life: The Plants and Animals of Temperate Waters. Reed New Holland, Sydney, Australia. Evanno, G., Regnaut, S., Goudet, J., 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611-2620.
Fincham, A.A., 1977. Larval development of British prawns and shrimps (Crustacea: Decapoda: Natantia). 1. Laboratory methods and a review of Palaemon (Palaeander) elegans Rathke, 1837. Bulletin of the British Museum (Natural History) Zoology, 32, 1-28.
Fu, Y.X., 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915-925.
Funk, D.J., Omland, K.E., 2003. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution, and Systematics, 34, 397-423.
Galarza, J.A., Carreras-Carbonell, J., Macpherson, E., Pascual, M., Roques, S. et al., 2009. The influence of oceanographic fronts and early-life-history traits on connectivity among littoral fish species. Proceedings of the National Academy of Sciences of the United States of America, 106, 1473-1478.
Gallager, S.M., Manuel, J.L., Manning, D.A., O’Dor, R.K., 1996. Ontogenetic changes in the vertical distribution of giant scallop larvae, Placopecten magellanicus, in 9-m deep mesocosms as a function of light, food, and temperature stratification. Marine Biology, 124, 679-692.
Gilg, M.R., Hilbish, T.J., 2003. Patterns of larval dispersal and their effect on the maintenance of a blue mussel hybrid zone in southwestern England. Evolution, 57, 1061-1077.
Goldstien, S. J., Schiel, D. R., Gemmell, N.J., 2006. Comparative phylogeography of coastal limpets across a marine disjunction in New Zealand. Molecular Ecology, 15, 3259-3268.
Gosling, E. M. (Ed.), 1992. Systematics and geographic distribution of Mytilus. The mussel Mytilus: ecology, physiology, genetics and culture. Elsevier, Amsterdam, pp. 1-20.
Gosling, E.M., 1984. The systematic status of Mytilus galloprovincialis in western Europe: a review. Malacologia, 25, 551-568.
Grabowski, M., 2006. Rapid colonization of the Polish Baltic coast by an Atlantic palaemonid shrimp Palaemon elegans Rathke, 1837. Aquatic Invasions, 1, 116-123.
Guo, S. W., Thompson, E.A., 1992. Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics, 48, 361-372.
Hamer, B., Jakšić, Ž., Pavičić-Hamer, D., Perić, L., Medaković, D. et al., 2008. Effect of hypoosmotic stress by low salinity acclimation of Mediterranean mussels Mytilus galloprovincialis on biological parameters used for pollution assessment. Aquatic Toxicology, 89, 137-151.
Harpending, H.C., 1994. Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology, 66, 591-600.
Hefti-Gautschi, B., Pfunder, M., Jenni, L., Keller, V., Ellegren, H., 2009. Identification of conservation units in the European Mergus merganser based on nuclear and mitochondrial DNA markers. Conservation Genetics, 10, 87-99.
Hewitt, G.M., 2004. Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society Biological Science, 359, 183-195.
Hilbish, T.J., Koehn, K., 1985. Dominance in physiological phenotypes and fitness at an enzyme locus. Science, 229, 52-54.
Hiscott, R.N., Aksu, A.E., Mudie, P.J., Marret, F., Abrajano, T. et al., 2007. A gradual drowning of the southwestern Black Sea shelf: Evidence for a progressive rather than abrupt Holocene reconnection with the eastern Mediterranean Sea through the Marmara Sea gateway. Quaternary International, 167 (8), 19-34.
Hoarau, G., Coyer, J.A., Veldsink, J.H., Stam, W.T., Olsen, J.L., 2007. Glacial refugia and recolonization pathways in the brown seaweed Fucus serratus. Molecular Ecology, 16, 3606-3616.
Hoarau, G., Rijnsdorp, A.D., Van Der Veer, H.W., Stam, W.T., Olsen, J.L., 2004. Population structure of plaice (Pleuronectes platessa L.) in northern Europe: a comparison of resolving power between microsatellites and mitochondrial DNA data. Journal of Sea Research, 51, 183-190.
Huvet, A., Boudry, P., Ohresser, M., Delsert, C., Bonhomme, F., 2000. Variable microsatellites in the Pacific Oyster Crassostrea gigas and other cupped oyster species. Animal Genetics, 31, 71-72.
Huyse, T., Van Houdt, J., Volckaert, F.A. M., 2004. Paleoclimatic history and vicariant speciation in the ‘sand goby’ group (Gobiidae, Teleostei). Molecular Phylogenetics and Evolution, 32, 324 - 336.
Inoue, K., Waite, J. H., Matsuoka, M., Odo, S., Harayama, S., 1995. Interspecific variations in adhesive protein sequences of Mytilus edulis, M. galloprovincialis, and M. trossulus. Biology Bulletin, 189, 370-375.
Janas, U., Piłka, M., Lipińska, D., 2013. Temperature and salinity requirements of Palaemon adspersus Rathke, 1837 and Palaemon elegans Rathke, 1837. Do they explain the occurrence and expansion of prawns in the Baltic Sea? Marine Biology Research, 9, 293-300.
Jolly, M.T., Viard, F., Gentil, F., Thiébaut, E., Jollivet, D., 2006. Comparative phylogeography of two coastal polychaete tubeworms in the Northeast Atlantic supports shared history and vicariant events. Molecular Ecology, 15, 1841-1855.
Kalkan, E., Bilgin, R., 2016. The intertwined effects of geographic barriers, palaeoclimate and life history on the distribution of genetic diversity: A case study with two marine species in the Eastern Mediterranean. 3rd Ecology and Evolutionary Biology Symposium, Turkey.
Kalkan, E., Karhan, S.Ü., Bilgin, R., Hemond, E.M., 2016. The Turkish Straits System as a phylogeographic boundary – A literature review. p. 550-569. In: The Sea of Marmara; Marine Biodiversity, Fisheries, Conservation and Governance. Ozsoy, E., Cagatay, M.N., Balkis, N., Balkis, N., Ozturk, B. (Eds.). Turkish Marine Research Foundation [TUDAV], Publication No: 42, Istanbul, Turkey.
Kalkan, E., Karhan, S.U., Yokes, M.B., Bilgin, R., 2013. The Turkish Straits System–phylogeographic break for the caridean shrimp Palaemon elegans (Crustacea: Decapoda). Rapp Comm Int Mer Médit, 40, 775.
Kalkan, E., Kurtulus, A., Maraci, N.O., Bilgin, R., 2011. Is the Bosphorus Strait a barrier to gene flow for the Mediterranean mussel, Mytilus galloprovincialis (Lamarck, 1819)? Marine Biology Research, 7, 690-700.
Kaminski, M.A., Aksu, A.E., Hiscott, R.N., Box, M., Al-Salameen, M. et al., 2002. Late glacial to Holocene benthic foraminifera in the Marmara Sea: implications for Black Sea–Mediterranean Sea connections following the last deglaciation. Marine Geology, 190, 165-202.
Knapp, B. A., 1993. Thalassocracies in Bronze Age eastern Mediterranean trade: Making and breaking a myth. World Archaeology, 24, 332-347.
Knowlton, N., Weigt, L.A., 1998. New dates and new rates for divergence across the Isthmus of Panama. Proceedings of the Royal Society B, Biological Sciences, 265, 2257-2263.
Krijgsrnan, W., Hilgen, F.J., Raffi, I., Sierra, F.J., Wilson, D.S., 1999. Chronology, causes and progression of the Messinian salinity crisis. Nature, 400, 652-655.
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, 1547-1549.
Ladoukakis, E.D., Saavedra, C., Magoulas, A., Zouros, E., 2002. Mitochondrial DNA variation in a species with two mitochondrial genomes: the case of Mytilus galloprovincialis from the Atlantic, the Mediterranean and the Black Sea. Molecular Ecology, 11, 755-769.
Laudien, J., Flint, N.S., van der Bank, F.H., Brey, T., 2003. Genetic and morphological variation in four populations of the surf clam Donax serra (Roding) from southern African sandy beaches. Biochemical Systematics and Ecology, 31, 751-772.
Librado, P., Rozas, J., 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
Luttikhuizen, P. C., Campos, J., van Bleijswijk, J., Peijnenburg, K. T. C. A., van der Veer, H. W., 2008. Phylogeography of the common shrimp, Crangon crangon (L.) across its distribution range. Molecular Phylogenetics and Evolution, 46, 1015-1030.
Maggs, C.A., Castilho, R., Foltz, D., Henzler, C., Jolly, M.T. et al., 2008. Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology, 89, 108-122.
Magoulas, A., Tsimenides, N., Zouros, E., 1996. Mitochondrial DNA phylogeny and the reconstruction of the population history of a species: the case of the European anchovy (Engraulis encrasicolus). Molecular Biology and Evolution, 13, 178-190.
Major, C.O., 2002. Non-eustatic controls on sea-level change in semi-enclosed basins. PhD thesis. Columbia University, New York, 223 pp.
Major, C.O., Goldstein, S.L., Ryan, W.B.F., Lericolais, G., Piotrowski, A.M. et al., 2006. The co-evolution of Black Sea level and composition through the last deglaciation and its paleoclimatic significance. Quaternary Science Reviews, 25, 2031-2047.
Mayr, E., Ashlock, P.D., 1991. Principles of Systematic Zoology. McGraw-Hill, New York.
McDonald, J. H., Seed, R., Koehn, R. K., 1991. Allozymes and morphometric characters of three species of Mytilus in the northern and southern hemispheres. Marine Biology, 111, 323-333.
Minchin, D., Gollasch, S., 2002. Vectors - How exotics get around. In: Invasive Aquatic Species of Europe. Distribution, Impacts and Management. p. 183-192. Leppäkoski, E., Gollasch, S., Olenin, S. (Eds.). Kluwer Academic Publishers, Netherlands.
Mutlu, E., 2005. A comparison of the contribution of zooplankton and nekton taxa to the near-surface acoustic structure of three Turkish seas. Marine Ecology, 26, 17-32.
Néraudeau, D., Goubert, E., Lacour, D., Rouchy, J.M., 2001. Changing biodiversity of Mediterranean irregular echinoids from the Messinian to the Present-Day. Palaeogeography, Palaeoclimatology, Palaeoecology, 175, 43-60.
Nilsson, J., Gross, R., Asplund, T., Dove, O., Jansson, H. et al., 2001. Matrilinear phylogeography of Atlantic salmon (Salmo salar L.) in Europe and postglacial colonization of the Baltic Sea area. Molecular Ecology. 10, 89-102.
Oguz, T., Özsoy, E., Latif, M.A., Sur, H. I., Ünlüata, U., 1990. Modeling of hydraulically controlled exchange flow in the Bosphorus Strait. Journal of Physical Oceanography, 20, 945-965.
Oguz, T., Ozturk, B., 2011. Mechanisms impeding natural Mediterranization process of Black Sea fauna. Journal of Black Sea/Mediterranean Environment, 17, 234-253.
Ozturk, B., Ozturk, A.A., 1996. On the biology of the Turkish straits system. In: Dynamics of Mediterranean Straits and Channels. No spécial 17, 205-221. Briand, F. (Ed.). Bulletin de l’Institut océanographique de Monaco.
Palumbi, S.R., 1994. Genetic divergence, reproductive isolation, and marine speciation. Annual Review of Ecology, Evolution, and Systematics, 25, 547-572.
Panin, N., Popescu, I., 2007. The Northwestern Black Sea: Climatic and Sea-Level Changes in the Late Quaternary. p. 387-404. In: The Black Sea Flood Question: Changes in Coastline, Climate, and Human Settlement. Yanko-Hombach, V., Gilbert, A. S., Panin, N., Dolikhanov, P. M. (Eds.), Springer.
Pascual, M., Rives, B., Schunter, C., Macpherson, E., 2017. Impact of life history traits on gene flow: A multispecies systematic review across oceanographic barriers in the Mediterranean Sea. PLoS ONE, 12, 5.
Passamonti, M., Mantovani, B., Scali, V., 1999. Allozymic analysis of some Mediterranean Veneridae (Mollusca: Bivalvia): preliminary notes on taxonomy and systematics of the family. Journal of the Marine Biological Association of the United Kingdom, 79, 899-906.
Patarnello, T., Volckaert, F.A.M.J., Castilho, R., 2007. Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Molecular Ecolgy, 16, 4426-4444.
Paterno, M., Bat, L., Ben Souissi, J., Boscari, E., Chassanite, A. et al., 2019. A genome-wide approach to the phylogeography of the mussel Mytilus galloprovincialis in the Adriatic and the Black Seas. Frontiers in Marine Science, 6, 566.
Peakall, R., Smouse, P.E., 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6, 288-295.
Peakall, R., Smouse, P.E., 2012. GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research- an update. Bioinformatics, 28, 2537-2539.
Presa, P., Pérez, M., Diz, A.P., 2002. Polymorphic microsatellite markers for blue mussels (Mytilus spp.). Conservation Genetics, 3, 441-443.
Pritchard, J.K., Stephens, M., Donnelly, P., 2000. Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
R Core Team R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna; 2018. Available from: https://www.R-project.org
Rambaut, A., Suchard, M. A., Xie, D., Drummond, A. J., 2014. Tracer v1.6. Available from: http://beast.bio.ed.ac. uk/Tracer.
Ramos-Onsins, S.E., Rozas, J., 2002. Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution, 19, 2092-2100.
Raymond, M., Rousset, F., 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248-249.
Raymond, M., Vääntö, R.L., Thomas, F., Rousset, F., de Meeüs, T. et al., 1997. Heterozygote deficiency in the mussel Mytilus edulis species complex revisited. Marine Ecology Progress Series, 156, 225-237.
Reich, D.E., Goldstein, D.B., 1998. Genetic evidence for a Paleolithic human population expansion in Africa. Proceedings of the National Academy of Sciences, USA, 95, 8119-8123. Reuschel, S., Cuesta, J.A., Schubart, C.D., 2010. Marine biogeographic boundaries and human introduction along the European coast revealed by phylogeography of the prawn Palaemon elegans. Molecular Phylogenetics and Evolution, 55, 765-775.
Rice, W.R., 1989. Analyzing Tables of Statistical Tests. Evolution, 43, 223-5.
Riginos, C., Douglas, K.E., Jin, Y., Shanahan, D.F., Treml, E.A., 2011. Effects of geography and life history traits on genetic differentiation in benthic marine fishes. Ecography, 34, 566-575.
Riginos, C., Nachman, M.W., 2001. Population subdivision in marine environments: the contributions of biogeography, geographical distance and discontinuous habitat to genetic differentiation in a blennioid fish, Axoclinus nigricaudus. Molecular Ecology, 10, 1439-1453.
Riginos, C., Victor, B.C., 2001. Larval spatial distributions and other early life-history characteristics predict genetic differentiation in eastern Pacific blennioid fishes. Proceedings of the Royal Society B: Biological Sciences, 268, 1931-1936.
Rousset, F., 2008. Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Resources, 8, 103-106.
Ryan, W.B.F., Major, C.O., Lericolais, G., Goldstein, S.L., 2003. Catastrophic flooding of the Black Sea. Annual Review of Earth and Planetary Sciences, 31, 525-554.
Saavedra, C., Reyero, M.I., Zouros, E., 1997. Male-dependent doubly uniparental inheritance of mitochondrial DNA and female-dependent sex-ratio in the mussel Mytilus galloprovincialis. Genetics, 145, 1073-1082. Sequencher® version 5.4.6. DNA sequence analysis software, Gene Codes Corporation, Ann Arbor, MI USA. http://www. genecodes.com
Skibinski, D.O.F., Gallagher, C., Beynon, C.M., 1994. Sex limited mitochondrial DNA transmission in the marine mussel Mytilus edulis. Genetics, 138, 801-809.
So, J.J., Uthicke, S., Hamel, J.F., Mercier, A., 2011. Genetic population structure in a commercial marine invertebrate with long-lived lecithotrophic larvae: Cucumaria frondosa (Echinodermata: Holothuroidea). Marine Biology, 158, 859-870.
Stancyk, S.E., Feller, R.J., 1986. Transport of non-decapod invertebrate larvae in estuaries: an overview. Bulletin of Marine Science, 39, 257-268.
Suchanek, T.H., Geller, J.B., Kreiser, B.R., Mitton, J.B., 1997. Zoogeographic distributions of the sibling species Mytilus galloprovincialis and M. trossulus (Bivalvia: Mytilidae) and their hybrids in the North Pacific. Biological Bulletin, 193, 187-194.
Svitoch, A.A., Selivanov, A.O., Yanina, T.A., 2000. Paleohydrology of the Black Sea Pleistocene basin. Water Resources, 27, 655-664.
Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585-595.
Tarnowska, K., Chenuil, A., Nikula, R., Féral, J.P., Wołowicz, M., 2010. Complex genetic population structure of bivalve Cerastoderma glaucum in a highly fragmented lagoon habitat. Marine Ecology Progress Series, 406, 173-184.
Teacher, A.G.F., Shikano, T., Karjalainen, M.E., Merilä, J., 2011. Phylogeography and genetic structuring of European nine-spined sticklebacks (Pungitius pungitius)-mitochondrial DNA evidence. PLoS ONE. 6, 5, e19476. https://doi. org/10.1371/journal.pone.0019476
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., Higgins, D. G., 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876-4882.
Toews, D.P.L., Brelsford, A., 2012. The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology, 16, 3907-3930.
Udekem D’Acoz C., 1999. Inventaire et distribution des crustacés décapodes de l’Atlantique nord-Oriental, de la Méditerranée et des eaux continentales adjacentes au nord de 25°N. Muséum national d’Histoire naturelle, Paris, Patrimoines Naturels (M.N.H.N./S.P.N.), 40, 388 pp.
Unlulata, U., Oguz, T., Latif, M.A., Ozsoy, E., 1990. On the Physical Oceanography of the Turkish Straits. p. 25-60. In: The Physical Oceanography of Sea Straits. In: Pratt, L. J., (Ed.), NATO ASI Series (Mathematical and Physical Sciences), vol 318. Springer, Dordrecht.
Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., Shipley, P., 2004. Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535-538.
Venetis, C., Theologidis, I., Zouros, E., Rodakis, G. C., 2007. A mitochondrial genome with a reversed transmission route in the Mediterranean mussel Mytilus galloprovincialis. Gene, 406, 79-90.
Wachsmann, S., 1998. Seagoing Ships and Seamanship in the Bronze Age Levant. A&M University Press, Texas.
Waldman, B., McKinnon, J.S., 1993. Inbreeding and outbreeding in fishes, amphibians, and reptiles. In: The Natural History of Inbreeding and Outbreeding. Theoretical and Empirical Perspectives. p. 250-282.
Thornhill, N. W. (Ed.), University of Chicago Press, Chicago. Ward, R.D., Woodwark, M., Skibinski, D.O.F., 1994. A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. Journal of Fish Biology, 44, 213-232.
Waters, J.M., McCulloch, G.A., Eason, J.A., 2007. Marine biogeographical structure in two highly dispersive gastropods: implications for trans-Tasman dispersal. Journal of Biogeography, 34, 678-687.
Watterson, G.A., 1986. The homozygosity test after a change in population size. Genetics, 112, 899-907.
Yebra, L., Bonnet, D., Harris, R.P., Lindeque, P.K., Peijnenburg, K.T.C.A., 2011. Barriers in the pelagic: population structuring of Calanus helgolandicus and C. euxinus in European waters. Marine Ecology Progress Series, 428, 135-149.
Yilmaz, I.N., 2008. Zooplankton Dynamics of the Marmara Sea. Ph.D. Thesis. Istanbul University, Institute of Marine Sciences, Istanbul, 120 pp.
Young, C.M., 1995. Behavior and locomotion during the dispersal phase of larval life. p. 249-278. In: Marine invertebrate larvae. McEdward, L., (Eds.) CRC Press, Boca Raton.
Zenkevich, L., 1963. Biology of the seas of the U.S.S.R. Interscience Publishers, New York, 956 pp. Zouros, E., Foltz, D.W., 1984. Possible explanations of heterozygote deficiency in bivalve molluscs. Malacologia, 25, 583-591.