Different patterns of population structure and genetic diversity of three mesopelagic fishes in the Greek Seas


XENIA SARROPOULOU
https://orcid.org/0000-0003-3671-9693
DIMITRIS TSAPARIS
https://orcid.org/0000-0001-9626-5553
KONSTANTINOS TSAGARAKIS
https://orcid.org/0000-0003-2408-0220
NICHOLAS BADOUVAS
COSTAS S. TSIGENOPOULOS
https://orcid.org/0000-0003-0615-7941
Περίληψη

Mesopelagic fishes are among the most abundant groups of vertebrates on Earth. Despite their unique biological and ecological traits, research in this group has been particularly scarce. The present study investigates the intraspecific genetic diversity of three mesopelagic fishes (Hygophum benoiti, Maurolicus muelleri, and Benthosema glaciale) in the Greek Seas. Analyses of three mitochondrial DNA genes (COI, 12S, and 16S) from a total of 168 samples revealed a lack of genetic structure for M. muelleri and B. glaciale across the studied area. However, H. benoiti specimens from the Corinthian Gulf were differentiated from the rest of the populations, suggesting that the limited connection between the Corinthian and neighboring seas may act as a barrier to gene flow. Furthermore, the COI data of this study were co-analyzed with publicly available sequences, demonstrating lack of phylogeographic structure for all three species through their distribution range. Therefore, even though indications of genetic differentiation were observed, the three mesopelagic fishes are generally characterized by genetic homogeneity, which may be the result of their recent evolutionary history.

Λεπτομέρειες άρθρου
  • Ενότητα
  • Research Article
Λήψεις
Τα δεδομένα λήψης δεν είναι ακόμη διαθέσιμα.
Αναφορές
Alvheim, A.R., Kjellevold, M., Strand, E., Sanden, M., Wiech, M., 2020. Mesopelagic species and their potential contribution to food and feed security-a case study from Norway. Foods, 9 (3), 344.
Avise, J.C., 2000. Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, MA.
Bandelt, H.J., Forster, P., Röhl, A., 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16 (1), 37-48.
Barrett, R.T., Anker-Nilssen, T., Gabrielsen, G.W., Chapdelaine, G., 2002. Food consumption by seabirds in Norwegian waters. ICES Journal of Marine Science, 59 (1), 43-57.
Battaglia, P., Andaloro, F., Consoli, P., Esposito, V., Malara, D. et al., 2013. Feeding habits of the Atlantic bluefin tuna, Thunnus thynnus (L. 1758), in the central Mediterranean Sea (Strait of Messina). Helgoland Marine Research, 67 (1), 97-107.
Bernal, A., Olivar, M.P., Maynou, F., Fernández de Puelles, M.L., 2015. Diet and feeding strategies of mesopelagic fishes in the western Mediterranean. Progress in Oceanography, 135, 1-17.
Bohonak, A.J., 1999. Dispersal, Gene Flow, and Population Structure. The Quaterly Review of Biology, 74 (1), 21-45.
Bouckaert, R., Vaughan, T.G., Barido-Sottani, J., Duchêne, S., Fourment, M. et al., 2019. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology, 15 (4), 1-28.
Bowen, B.W., Shanker, K., Yasuda, N., Maria, M.C., Von Der Heyden, S. et al., 2014. Phylogeography unplugged: Comparative surveys in the genomic era. Bulletin of Marine Science, 90 (1), 13-46.
Caiger, P.E., Lefebve, L.S., Llopiz, J.K., 2021. Growth and reproduction in mesopelagic fishes : a literature synthesis. ICES Journal of Marine Science, 78 (3), 765-781.
Cano, J., Shikano, T., Kuparinen, A., Merilä, J., 2008. Genetic differentiation, effective population size and gene flow in marine fishes: implications for stock management. Journal of Integrative Field Biology, 5, 1-10.
Calò, A., Félix-Hackradt, F.C., Garcia, J., Hackradt, C.W., Rocklin, D. et al., 2013. A review of methods to assess connectivity and dispersal between fish populations in the Mediterranean Sea. Advances in Oceanography and Limnology, 4 (2), 150-175.
Christiansen, H., Dettai, A., Heindler, F.M., Collins, M.A., Duhamel, G. et al., 2018. Diversity of mesopelagic fishes in the Southern Ocean - A phylogeographic perspective using DNA barcoding. Frontiers in Ecology and Evolution, 6 (120), 1-19.
Christiansen, S., Titelman, J., Kaartvedt, S., 2019. Nighttime Swimming Behavior of a Mesopelagic Fish. Frontiers in Marine Science, 6, 787.
Contreras, T., Olivar, M.P., Bernal, A., Sabatés, A., 2015. Comparative feeding patterns of early stages of mesopelagic fishes with vertical habitat partitioning. Marine Biology, 162 (11), 2265-2277.
Cowen, R.K., Sponaugle, S., 2009. Larval dispersal and marine population connectivity. Annual Review of Marine Science, 1 (1), 443-466.
Darriba, D., Taboada, G.L., Doallo, R., Posada, D., 2012. jModelTest 2: more models, new heuristics and high-performance computing Europe PMC Funders Group. Nature Methods, 9 (8), 772.
Drakopoulos, P.G., Lascaratos, A., 1998. A preliminary study on the internal tides of the gulfs of Patras and Korinthos, Greece. Continental Shelf Research, 18 (12), 1517-1529.
Excoffier, L., Lischer, H.E.L., 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.
Eytan, R.I., Hellberg, M.E., 2010. Nuclear and mitochondrial sequence data reveal and conceal different demographic histories and population genetic processes in caribbean reef fishes. Evolution, 64 (12), 3380-3397.
Friligos, N., Theocharis, A., Georgopoulos, D., 1985. Preliminary chemical and physical observations during summer 1980 on a silled embayment in the Ionian Sea. Vie Milieu, 35, 115-125.
Fu, Y. X., 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147 (2), 915-925.
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 (5), 1473- 1478.
Giménez, J., Marçalo, A., García-Polo, M., García-Barón, I., Castillo, J.J. et al., 2018. Feeding ecology of Mediterranean common dolphins: The importance of mesopelagic fish in the diet of an endangered subpopulation. Marine Mammal Science, 34 (1), 136-154.
Gjoesaeter, J., Kawaguchi, K., 1980. A review of the world resources of mesopelagic fish. FAO Fisheries Technical Papers (FAO), 193, 160 pp.
Gkafas, G.A., Tsigenopoulos, C., Magoulas, A., Panagiotaki, P., Vafidis, D. et al., 2013. Population subdivision of saddled seabream Oblada melanura in the Aegean Sea revealed by genetic and morphometric analyses. Aquatic Biology, 18 (1), 69-80.
Gordeeva, N.V., 2011. On structure of species in pelagic fish: The results of populational-genetic analysis of four species of lanternfish (Myctophidae) from the southern Atlantic. Journal of Ichthyology, 51 (2), 152-165.
Gordeeva, N.V., 2014. Phylogeography, genetic isolation, and migration of deep-sea fishes in the South Atlantic. Journal of Ichthyology, 54 (9), 642-659.
Grant, W.A.S., Bowen, B.W., 1998. Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. Journal of Heredity, 89 (5), 415-426.
Grant, W.S., 2015. Problems and cautions with sequence mismatch analysis and Bayesian skyline plots to infer historical demography. Journal of Heredity, 106 (4), 333-346.
Grimaldo, E., Grimsmo, L., Alvarez, P., Herrmann, B., Tveit, G.M. et al., 2020. Investigating the potential for a commercial fishery in the Northeast Atlantic utilizing mesopelagic species. ICES Journal of Marine Science, 77 (7-8), 2541- 2556.
Habib, K.A., Oh, J., Kim, S., Lee, Y.H., 2012. Divergence and gene flow between the East Sea and the Southeast Atlantic populations of North Pacific light fish Maurolicus japonicus Ishikawa. Genes & Genomics, 34 (6), 609-618.
Hedgecock, D., Barber, P.H., Edmands, S., 2007. Genetic approaches to measuring connectivity. Oceanography, 20 (3), 70-79. Hewitt, G., 2000. The genetic legacy of the Quaternary ice ages. Nature, 405, 907-913.
Imsiridou, A., Papapetrou, M., Tilikidis, A., 2019. Can The Population Structure of Three Greek Marine Species (Sardina pilchardus, Penaeus kerathurus, Mullus barbatus) Become a Tool for Their Future Characterization as PGI Products? Journal of Nutrition, Food and Lipid Science, 1, 54-83.
Irigoien, X., Klevjer, T.A., Røstad, A., Martinez, U., Boyra, G. et al., 2014. Large mesopelagic fishes biomass and trophic efficiency in the open ocean. Nature Communications, 5, 3271.
John, M.A.S., Borja, A., Chust, G., Heath, M., Grigorov, I. et al., 2016. A Dark Hole in Our Understanding of Marine Ecosystems and Their Services : Perspectives from the Mesopelagic Community. Frontiers in Marine Science, 3, 31.
Kocher, T.D., Thomas, W.K., Meyer, A., Edwards, S.V., Paabo, S. et al., 1989. Dynamics of mitochondrial DNA evolution in animals: Amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences of the United States of America, 86 (16), 6196-6200.
Kousteni, V., Kasapidis, P., Kotoulas, G., Megalofonou, P., 2015. Strong population genetic structure and contrasting demographic histories for the small-spotted catshark (Scyliorhinus canicula) in the Mediterranean Sea. Heredity, 114 (3), 333-343.
Kristoffersen, J.B., Salvanes, A.G.V., 2009. Distribution, growth, and population genetics of the glacier lanternfish (Benthosema glaciale) in Norwegian waters: Contrasting patterns in fjords and the ocean. Marine Biology Research, 5 (6), 596-604.
Kumar, S., Stecher, G., Tamura, K., 2016. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution, 33 (7), 1870-1874.
Leigh, J. W., Bryant, D., 2015. POPART: Full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6 (9), 1110-1116.
Librado, P., Rozas, J., 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
Miralles, L., Lee, L.S., Borrell, Y., Garcia-Vazquez, E., 2016. Population genetic structure of the European conger (Conger conger) in North East Atlantic and West Mediterranean Sea. Fisheries Research, 174, 245-249.
Modica, L., Cartes, J.E., Velasco, F., Bozzano, A., 2015. Juvenile hake predation on Myctophidae and Sternoptychidae: Quantifying an energy transfer between mesopelagic and neritic communities. Journal of Sea Research, 95, 217-225.
Olivar, M.P., Bernal, A., Molí, B., Peña, M., Balbín, R. et al., 2012. Vertical distribution, diversity and assemblages of mesopelagic fishes in the western Mediterranean. Deep-Sea Research Part I: Oceanographic Research Papers, 62, 53-69.
Olson, D.B., Kourafalou, V.H., Johns, W.E., Samuels, G., Venziani, M., 2007. Aegean surface circulation from a satellite- tracked drifter array. Journal of Physical Oceanography, 37 (7), 1898-1917.
Palumbi, S.R., 1994. Genetic Divergence, Reproductive Isolation, and Marine Speciation. Annual Review of Ecology and Systematics, 25, 547-572.
Palumbi S.R., 1996. Nucleic acids II: the polymerase chain reaction. p. 205-247. In: Molecular Systematics. Hillis, D., Moritz, C., Mable, B. (Eds). 2nd ed. Sinauer Associates Inc, Sunderland, Massachusetts.
Pappalardo, A.M., Cuttitta, A., Sardella, A., Musco, M., Maggio, T. et al., 2015. DNA barcoding and COI sequence variation in Mediterranean lanternfishes larvae. Hydrobiologia, 749 (1), 155-167.
Patarnello, T., Volckaert, F.A.M., Castilho, R., 2007. Pillars of Hercules: Is the Atlantic-Mediterranean transition a phylogeographical break? Molecular Ecology, 16 (21), 4426- 4444.
Plough, L.V., 2016. Genetic load in marine animals: a review. Current Zoology, 62 (6), 567-579.
Rambaut, A., Drummond, A.J., Xie, D., Baele, G., Suchard, M.A., 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67 (5), 901-904.
Ramfos, A., Somarakis, S., Koutsikopoulos, C., Fragopoulu, N., 2005. Summer mesozooplankton distribution in coastal waters of central Greece (eastern Mediterranean). I. Hydrology and group composition. Journal of the Marine Biological Association of the United Kingdom, 85 (4), 755-764.
Ramos-Onsins, S.E., Rozas, J., 2002. Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution, 19 (12), 2092-2100.
Rees, D.J., Byrkjedal, I., Sutton, T.T., 2017. Pruning the Pearlsides: Reconciling morphology and molecules in mesopelagic fishes (Maurolicus: Sternoptychidae). Deep-Sea Research Part II: Topical Studies in Oceanography, 137, 246-257.
Rees, D.J., Poulsen, J.Y., Sutton, T.T., Costa, P.A.S., Landaeta, M.F., 2020. Global phylogeography suggests extensive eucosmopolitanism in Mesopelagic Fishes (Maurolicus: Sternoptychidae). Scientific Reports, 10 (1), 1-12.
Rodriguez-Ezpeleta, N., Álvarez, P., Irigoien, X., 2017. Genetic diversity and connectivity in Maurolicus muelleri in the bay of biscay inferred from thousands of SNP markers. Frontiers in Genetics, 8 (195), 1-8.
Sakellariou, D., Galanidou, N., 2016. Pleistocene submerged landscapes and Palaeolithic archaeology in the tectonically active Aegean region. Geological Society Special Publication, 411 (1), 145-178.
Salmenkova, E.A., 2011. New view on the population genetic structure of marine fish. Russian Journal of Genetics, 47 (11), 1279-1287.
Salvanes, A., Kristoffersen, J.B., 2001. Mesopelagic Fishes. p. 1711–1717. In: Encyclopedia of Ocean Sciences. Steele, J.H., Thorpe, S.A., Turekian, K.K (Eds). Academic Press, London.
Schunter, C., Carreras-Carbonell, J., Planes, S., Sala, E., Ballesteros, E., et al., 2011. Genetic connectivity patterns in an endangered species : The dusky grouper (Epinephelus marginatus). Journal of Experimental Marine Biology and Ecology, 401 (1-2), 126-133.
Selkoe, K.A., Henzler, C.M., Gaines, S.D., 2008. Seascape genetics and the spatial ecology of marine populations. Fish and Fisheries, 9 (4), 363-77.
Selkoe, K.A., Aloia, C.C.D., Crandall, E.D., Iacchei, M., Liggins, L. et al., 2016. A decade of seascape genetics : contributions to basic and applied marine connectivity. Marine Ecology Progress Series, 554, 1-19.
Slatkin, M., 1985. Gene flow in natural populations. Annual Review of Ecology and Systematics, 16 (1), 393-430.
Somarakis, S., Isari, S., Machias, A., 2011a. Larval fish assemblages in coastal waters of central Greece: reflections of topographic and oceanographic heterogeneity. Scientia Marina, 75 (3), 605-618.
Somarakis, S., Ramfos, A., Palialexis, A., Valavanis, V.D., 2011b. Contrasting multispecies patterns in larval fish production trace inter-annual variability in oceanographic conditions over the N.E. Aegean Sea continental shelf (Eastern Mediterranean). Hydrobiologia, 670 (1), 275-287.
Stern, N., Douek, J., Goren, M., Rinkevich, B., 2018. With no gap to mind: a shallow genealogy within the world’s most widespread small pelagic fish. Ecography, 41(3), 491-504.
Suneetha, K.B., Salvanes, A.G.V., 2001. Population genetic structure of the glacier lanternfish, Benthosema glaciale (Myctophidae) in Norwegian waters. Sarsia, 86 (3), 203-212.
Tajima, F., 1989. Statistical Method for Testing the Neutral Mutation Hypothesis by DNA Polymorphism. Genetics, 123, 585-595.
Terada, R., Takano, T., Sakuma, K., Narimatsu, Y., Kojima, S., 2018. Phylogeography of the north pacific lightfish Maurolicus japonicus. Plankton and Benthos Research, 13 (4), 180-184.
Torri, M., Pappalardo, A.M., Ferrito, V., Giannì, S., Armeri, G. et al., 2021. Signals from the deep-sea: Genetic structure, morphometric analysis, and ecological implications of Cyclothone braueri (Pisces, Gonostomatidae) early life stages in the Central Mediterranean Sea. Marine Environmental Research, 169, 105379.
Van de Putte, A.P., Van Houdt, J. K.J., Maes, G.E., Hellemans, B., Collins, M.A. et al., 2012. High genetic diversity and connectivity in a common mesopelagic fish of the Southern Ocean: The myctophid Electrona antarctica. Deep-Sea Research Part II, 59-60, 199-207.
Viret, A., Tsaparis, D., Tsigenopoulos, C.S., Berrebi, P., Sabatini, A. et al., 2018. Absence of spatial genetic structure in common dentex (Dentex dentex (Linnaeus, 1758)) in the Mediterranean Sea as evidenced by nuclear and mitochondrial molecular markers. PLoS ONE, 13, 9.
Waples, R.S., 1998. Separating the Wheat From the Chaff : Patterns of Genetic Differentiation in High Gene Flow Species. Journal of Heredity, 89 (5), 438-450.
Ward, R.D., Zemlak, T.S., Innes, B.H., Last, P.R., Hebert, P.D., 2005. DNA barcoding Australia’s fish species. Philosophical Transactions of the Royal Society B: Biological Sciences, 360, 1847-1857.
Zardoya, R., Castilho, R., Grande, C., Favre-Krey, L., Caetano, S. et al., 2004. Differential population structuring of two closely related fish species, the mackerel (Scomber scombrus) and the chub mackerel (Scomber japonicus), in the Mediterranean Sea. Molecular Ecology, 13 (7), 1785-1798.
Τα περισσότερο διαβασμένα άρθρα του ίδιου συγγραφέα(s)