A Lessepsian invader round herring (Etrumeus golanii) with high genetic diversity without bottlenecking in the northeastern Mediterranean Sea

In this study, population genetic structure and genetic diversity of round herring in the Turkish seas were determined using sequence data of mitochondrial DNA control region. Round herring, Etrumeus golanii samples were collected from three localities along the Turkish coast of the Mediterranean Sea, (Gulf of Iskenderun and Gulf of Antalya) and southern Aegean Sea (Gulf of Marmaris). Genetic variability was high both within and between the populations based on haplotype diversity values. The results have shown that each population has a high genetic diversity with unique mtDNA haplotypes with unique genetic structure. The most important factor in the emergence of this situation is that populations were considered to have migrated from the Red Sea to the Mediterranean Sea by different fish shoals at different time intervals independently of each other. A general acceptance for explanation of high genetic diversity in the Mediterranean Lessepsian species is the lack of bottleneck due to the consecutive invasions.

PDF

___

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: 190-201. doi: 10.1016/J.JEMBE.2005.12.002
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: 592-595. doi: 10./j.ympev.2009.06.017
Basusta N, Erdem Ü, Mater S (1997). A new Lessepsian immigrant fish species in Iskenderun Bay: Red-eyed Sardine, Etrumeus teres (DeKay, 1842). In: Proceedings of the Mediterranean Fisheries Congress; İzmir, Turkey. pp. 921-924 (in Turkish with an abstract in English).
Boudaya L, Boussellaa W, Derbel H, Neifar L (2016). A new record of the Lessepsian fish Etrumeus golanii (Teleostei: Clupeidae) in the Gulf of Gabes, Tunisia, with notes on its parasites. Cahiers de Biologie Marine 57: 389-395.
Bucciarelli G, Golani D, Bernardi G (2002). Genetic cryptic species as biological invaders: the case of a Lessepsian fish migrant, the hardyhead silverside Atherinomorus lacunosus. Journal of Experimental Marine Biology and Ecology 273: 143-149. doi: 10.1016/S0022-0981(02)00138-7
Chen JZ, Hebert PD (1999). Terminal branch haplotype analysis: a novel approach to investigate newly arisen variants of mitochondrial DNA in natural populations. Mutation Research 434: 219-231. doi: 10.1016/s0921-8777(99)00030-0
Corsini M, Margies P, Kondilatos G, Economidis PS (2005). Lessepsian migration of fishes to the Aegean Sea: first record of Tylerius spinosissimus (Tetraodontidae) from the Mediterranean and six more fish records from Rhodes. Cybium 29: 347-354.
DiBattista JD, Randall JE, Newman SJ, Bowen BW (2014). Round herring (genus Etrumeus) contain distinct evolutionary lineages coincident with a biogeographic barrier along Australia’s southern temperate coastline. Marine Biology 161: 2465-2477. doi: 10.1007/s00227-014-2516-5
Excoffier L, Lischer HEL (2010). Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564- 567. doi: 10.1111/j.1755-0998.2010.02847.x
Excoffier L, Smouse PE, Quattro JM (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479-491.
Falautano M, Castriota L, Andalaro F (2006). First record of Etrumeus teres (Clupeidae) in the Central Mediterranean Sea. Cybium 30: 287-288.
Galil B, Boero, F, Fraschetti S, Piraino S, Campbell M, et al. (2015). The Enlargement of the Suez Canal and Introduction of Non‐ Indigenous Species to the Mediterranean Sea. Limnology and Oceanography Bulletin. 24: 43-45. doi: 10.1002/lob.10036
Golani D (2000). The Lessepsian migrant, the Red-eye round herring Etrumeus teres (DeKay, 1842), a new record from Cyprus. Zoology in the Middle East 20: 61-64. doi: 10.1080/09397140.2000.10637813
Golani D, Öztürk B, Başusta N (2006). The fishes of the eastern Mediterranean. Turkish Marine Research Foundation Publications no. 24. İstanbul, Turkey: Turkish Marine Research Foundation.
Golani D, Azzurro E, Corsini-Foka M, Falautano M, Andaloro F et al. (2007). Genetic bottlenecks and successful biological invasions: the case of a recent Lessepsian migrant. Biology Letters 3: 541-545. doi: 10.1098/rsbl.2007.0308
Hall TA (1999). Bioedit: a user friendly biological sequence aligment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95-98.
Hassan M, Bonhomme F (2005). No reduction in neutral variability of mitochondrial and nuclear genes for a Lessepsian migrant, Upeneus moluccensis. Journal of Fish Biology 66: 865-870. doi: 10.1111/j.0022-1112.2005.00643.x
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: 219-232. doi: 10.1016/S0022-0981(03)00139-4
Hobbs AP-J, Herwerden LV, Jerry RD, Jones PG, Munday LP (2013). High genetic diversity in geographically remote populations of endemic and widespread coral reef Angelfishes (genus: Centropyge). Diversity 5: 39-50.
Kallianiotis A, Lekkas V (2005). First documented report on the Lessepsian migrant Etrumeus teres De Kay, 1842 (Pisces: Clupeidae) in the Greek Sea. Journal of Biological Research 4: 225-229.
Kasapidis P, Peristeraki P, Tserpes G, Magoulas A (2007). A new record of the Lessepsian invasive fish, Etrumeus teres (Osteichthyes: Clupeidae) in the Mediterranean Sea (Aegean, Greece). Aquatic Invasions 2: 152-154. doi: 10.3391/ai.2007.2.2.12
Martinez A, Willoughby JR, Christie MR (2018). Genetic diversity in fishes is influenced by habitat type and life‐history variation. Ecology and Evolution 8: 12022-12031.
Mehanna SF, El-Gammal F (2005). Stock assessment of the round herring, Etrumeus teres (De Kay, 1842) in the Egyptian sector of Red Sea. Indian Journal of Fisheries 52: 377-38.
Osman AGM, Akel EH, Farrag M, Moustafa MA (2011). Reproductive Biology of Round Herring Etrumeus teres (Dekay, 1842) from the Egyptian Mediterranean Water at Alexandria. International Scholarly Research Notices Zoology 2011: 1-12. doi: 10.5402/2011/215950
Romiguier J, Gayral P, Ballenghien M, Bernard A, Cahais V, Chenuil A et al. (2014). Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature 515: 261-263.
Rozas J, Sanchez-Del Barrio, JC, Messeguer X, Rozas R (2003). DnaSP, DNA polymorphizm analyses by the coalescent and other methods. Bioinformatics 19: 2496-2497. doi: 10.1093/ bioinformatics/btg359
Sanders M, Kedidi SM, Hegazy MR (1984). Stock assessment for the round herring (Etrumeus teres) caught by purse seine in the Gulf of Suez. Accession number: XF8546789. Rome, Italy: Food and Agriculture Organization of the United Nations.
Srihari M, Silpa S, Pavan-Kumar A, Tikochinski Y, Golani, D et al. (2021). Characterization of genetic diversity of an invasive Lessepsian Migrant, Nemipterus randalli Russell, 1986 from its native and non-native regions using mitochondrial DNA marker. Mediterranean Marine Science 22: 73-78. doi: 10.12681/mms.23507
Takahata N, Palumbi SR (1985). Extranuclear differentiation and gene flow in the finite island model. Genetics 109: 441-457.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725-2729. doi: 10.1093/ molbev/mst197
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.
Yarmaz A, Balaban C, Türkakın M, Türker-Çakır D (2010). A new record of Lessepsian migrant Etrumeus teres (DeKay, 1842) (Osteichthyes: Clupeidae) from the northern Aegean Sea. Journal of Applied Ichthyology 26: 134-136. doi: 10.1111/j.1439-0426.2009.01365.x
Yılmaz R, Hoşsucu B (2003). Some biological parameters of round herring, Etrumeus teres (DeKay, 1842) in the Gulf of Antalya (Mediterranean Sea). Ege Journal of Fisheries Aquatic Science 20: 1-8.
Zenetos A, Galanidi M (2020). Mediterranean non indigenous species at the start of the 2020s: recent changes. Marine Biodiversity Records 13: 10. doi: 10.1186/s41200-020-00191-4
Zenetos A, Vassilopoulou V, Salomidi M, Poursanidis D (2008). Additions to marine alien fauna of Greek waters (2007 update). Marine Biodiversity Records 1: 1-8. doi: 10.1017/ S1755267207009281