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Genetic diversity of Nephtys hombergii (Phyllodocida, Polychaeta) associated with environmental factors in a highly fluctuating ecosystem

Published online by Cambridge University Press:  16 January 2017

Katerina Vasileiadou Open the ORCID record for Katerina Vasileiadou [Opens in a new window] ,
Christina Pavloudi Open the ORCID record for Christina Pavloudi [Opens in a new window] ,
Federica Camisa ,
Irene Tsikopoulou ,
Nina Fragopoulou ,
Georgios Kotoulas  and
Christos Arvanitidis
Katerina Vasileiadou*
Affiliation:
Department of Biology, University of Patras, 26500, Patras, Greece Institute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, Heraklion, 71003, Crete, Greece
Christina Pavloudi
Affiliation:
Institute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, Heraklion, 71003, Crete, Greece Biology Department, University of Crete, Heraklion, 71409, Crete, Greece
Federica Camisa
Affiliation:
Department of Ecological and Biological Sciences-University of Viterbo Largo dell'università s.n.c., blocco C 01100, Viterbo, Italy
Irene Tsikopoulou
Affiliation:
Biology Department, University of Crete, Heraklion, 71409, Crete, Greece
Nina Fragopoulou
Affiliation:
Department of Biology, University of Patras, 26500, Patras, Greece
Georgios Kotoulas
Affiliation:
Institute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, Heraklion, 71003, Crete, Greece
Christos Arvanitidis
Affiliation:
Institute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, Heraklion, 71003, Crete, Greece
*
Correspondence should be addressed to: K. Vasileiadou, Institute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, Heraklion, 71003, Crete, Greece email: kvasileiadou@hcmr.gr
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Abstract

Genetic diversity and population distribution are influenced by environmental factors, yet information is scarce on the interrelations that define dispersal of populations. Transitional water ecosystems are hosting habitats with temporally and spatially variable conditions, which make them very useful in understanding the mechanisms affecting population establishment. For the study, seasonal samples were collected from four lagoons in the lagoonal complex of Amvrakikos Gulf (W Greece). The mitochondrial DNA (COI gene) was analysed from polychaetes of Nephtys hombergii, as it is considered an important component of these assemblages and shows great dispersal ability. The results of the genetic analysis showed intraspecific variability in all the lagoons, with genetic structuring tending to follow a seasonal pattern rather than a spatial one. The results of BIOENV analysis indicated correlation of the observed pattern with the water pH levels, the redox potential and the concentration of phosphate in the sediment. The complexity of the network suggested the enhancement of the local population with more recently established haplotypes. The findings of the study support the necessity of designing management strategies by taking into account genetic diversity and population demography approaches in addition to those based on species and habitats.

Keywords

lagoonsgene flowNephtys hombergiiCOI genetemporal variation
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Issue 4 , June 2018 , pp. 777 - 789
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

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References

REFERENCES

Abbiati, M. and Maltagliati, F. (1992) Genetic population structure of Neanthes succinea (Polychaeta: Nereididae). Journal of the Marine Biological Association of the United Kingdom 72, 511–517.Google Scholar
Alvarado-Bremer, J., Viñas, J., Mejuto, J., Ely, B. and Pla, C. (2005) Comparative phylogeography of Atlantic bluefin tuna and swordfish: the combined effects of vicariance, secondary contact, introgression, and population expansion. Molecular Phylogenetics and Evolution 36, 169–187.Google Scholar
Anderson, M.J. (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.Google Scholar
Aylagas, E., Borja, A. and Rodríguez-Ezpeleta, N. (2014) Environmental status assessment using DNA metabarcoding: towards a genetics based marine biotic index (gAMBI). PLoS ONE 9, e90529.CrossRefGoogle ScholarPubMed
Barnes, R. (1995) European coastal lagoons: macrotidal versus microtidal contrasts. Biologia Marina Mediterranea 2, 3–7.Google Scholar
Baselga, A. and Fujisawa, T. (2013) Whole-community DNA barcoding reveals a spatio-temporal continuum of biodiversity at species and genetic levels. Nature Communications 4, 1892.Google Scholar
Bilton, D.T., Paula, J. and Bishop, J.D.D. (2002) Dispersal, genetic differentiation and speciation in estuarine organisms. Estuarine, Coastal and Shelf Science 55, 937–952.Google Scholar
Birky, C.W. (2013) Species detection and identification in sexual organisms using population genetic theory and DNA sequences. PLoS ONE 8, e52544.CrossRefGoogle ScholarPubMed
Bisol, P.M., Gallini, A., Prevedello, S., Rianna, E., Bernardinelli, E., Franco, A. and Zane, L. (2007) Low variation at allozyme loci and differences between age classes at microsatellites in grass goby (Zosterisessor ophiocephalus) populations. Hydrobiologia 577, 151–159.Google Scholar
Bray, J.R. and Curtis, J.T. (1957) An ordination of the upland forest community of southern Wisconsin. Ecology Monographs 27, 325–349.Google Scholar
Cancela da Fonseca, L., Costa, A.M. and Bernardo, J.M. (1989) Seasonal variation of benthic and fish communities in a shallow land-locked coastal lagoon (St Andre, SW Portugal). Scientia Marina 53, 663–669.Google Scholar
Chust, G., Albaina, A., Aranburu, A., Borja, Á., Diekmann, O.E., Estonba, A., Franco, J., Garmendia, J.M., Iriondo, M., Muxika, I., Rendo, F., Rodríguez, J.G., Ruiz-Larrañaga, O., Serrão, E.A. and Valle, M. (2013) Connectivity, neutral theories and the assessment of species vulnerability to global change in temperate estuaries. Estuarine, Coastal and Shelf Science 131, 52–63.Google Scholar
Cimmaruta, R., Bondanelli, P. and Nascetti, G. (2005) Genetic structure and environmental heterogeneity in the European hake (Merluccius merluccius). Molecular Ecology 14, 2577–2591.Google Scholar
Clarke, K. and Gorley, R. (2006) PRIMER v6: user manual/tutorial. Plymouth: PRIMER-E UK.Google Scholar
Clarke, K.R. and Ainsworth, M. (1993) A method of linking multivariate community structure to environmental variables. Marine Ecology Progress Series 92, 205–219.Google Scholar
Cognetti, G. and Maltagliati, F. (2004) Strategies of genetic biodiversity conservation in the marine environment. Marine Pollution Bulletin 48, 811–812.Google Scholar
Como, S. and Magni, P. (2009) Temporal changes of a macrobenthic assemblage in harsh lagoon sediments. Estuarine, Coastal and Shelf Science 83, 638–646.CrossRefGoogle Scholar
Excoffier, L. (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Molecular Ecology 13, 853–864.Google Scholar
Excoffier, L. and 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.Google Scholar
Fontaneto, D., Flot, J.F. and Tang, C.Q. (2015) Guidelines for DNA taxonomy, with a focus on the meiofauna. Marine Biodiversity 45, 433–451.CrossRefGoogle Scholar
Fu, Y.X. (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.Google Scholar
Galindo, H.M., Olson, D.B. and Palumbi, S.R. (2006) Seascape genetics: a coupled oceanographic-genetic model predicts population structure of Caribbean corals. Current Biology 16, 1622–1626.Google Scholar
Galindo, H.M., Pfeiffer-Herbert, A.S., McManus, M.A., Chao, Y., Chai, F. and Palumbi, S.R. (2010) Seascape genetics along a steep cline: using genetic patterns to test predictions of marine larval dispersal. Molecular Ecology 19, 3692–3707.Google Scholar
Gamfeldt, L. and Källström, B. (2007) Increasing intraspecific diversity increases predictability in population survival in the face of perturbations. Oikos 116, 700–705.Google Scholar
Gamfeldt, L., Wallén, J., Jonsson, P.R., Berntsson, K.M. and Havenhand, J.N. (2005) Increasing intraspecific diversity enhances settling success in a marine invertebrate. Ecology 86, 3219–3224.Google Scholar
Gouvis, N., Kevrekidis, T. and Koukouras, A. (1997) Temporal changes of a macrobenthic assemblage in Evros Delta (North Aegean Sea). Internationale Revue der gesamten Hydrobiologie und Hydrographie 82, 67–80.Google Scholar
Grasshoff, K., Ehrhardt, M. and Kremling, K. (1983) Methods of seawater analysis. Berlin: Wiley-VHC Verlag.Google Scholar
Gravina, M.F., Ardizzone, G.D., Scaletta, F. and Chimenez, C. (1989) Descriptive analysis and classification of benthic communities in some Mediterranean coastal lagoons (Central Italy). Marine Ecology 10, 141–166.Google Scholar
Gray, J.S. and Elliott, M. (2009) Ecology of marine sediments: from science to management. Oxford: Oxford University Press.Google Scholar
Guelorget, O. and Perthuisot, J. (1983) Le domaine paralique: expressions géologiques, biologiques et économiques du confinement. Paris: Ecole Normale Superieure de Paris .Google Scholar
Hamilton, M.B. (2009) Population genetics. Chichester: Wiley-Blackwell.Google Scholar
Hedges, J.I. and Stern, J.H. (1984) Carbon and nitrogen determinations of carbonate-containing solids. Limnology and Oceanography 29, 657–663.Google Scholar
Katselis, G.N., Moutopoulos, D.K., Dimitriou, E.N. and Koutsikopoulos, C. (2013) Long-term changes of fisheries landings in enclosed gulf lagoons (Amvrakikos gulf, W Greece): influences of fishing and other human impacts. Estuarine, Coastal and Shelf Science 131, 31–40.CrossRefGoogle Scholar
Kevrekidis, T. (2004) Seasonal variation of the macrozoobenthic community structure at low salinities in a Mediterranean lagoon (Monolimni Lagoon, Northern Aegean). International Review of Hydrobiology 89, 407–425.Google Scholar
Kormas, K.A., Nicolaidou, A. and Reizopoulou, S. (2001) Temporal variations of nutrients, chlorophyll a and particulate matter in three coastal lagoons of Amvrakikos Gulf (Ionian Sea, Greece). Marine Ecology 22, 201–213.Google Scholar
Lande, R. (1988) Genetics and demography in biological conservation. Science 241, 1455–1460.Google Scholar
Lawrence, A.J. and Soame, J.M. (2004) The effects of climate change on the reproduction of coastal invertebrates. Ibis 146, 29–39.Google Scholar
Librado, P. and Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.Google Scholar
Liggins, L., Treml, E.A. and Riginos, C. (2013) Taking the plunge: an introduction to undertaking seascape genetic studies and using biophysical models. Geography Compass 7, 173–196.Google Scholar
Loh, P.S., Miller, A.E.J., Reeves, A.D., Harvey, S.M. and Overnell, J. (2008) Assessing the biodegradability of terrestrially-derived organic matter in Scottish sea loch sediments. Hydrology and Earth System Sciences 12, 811–823.Google Scholar
Lorenzo-Carballa, M., Hadrys, H., Cordero-Rivera, A. and Andrés, J.A. (2011) Population genetic structure of sexual and parthenogenetic damselflies inferred from mitochondrial and nuclear markers. Heredity 108, 386–395.Google Scholar
Mallet, B., Martos, F., Blambert, L., Pailler, T. and Humeau, L. (2014) Evidence for isolation-by-habitat among populations of an epiphytic orchid species on a small oceanic island. PLoS ONE 9, e87469.Google Scholar
Maltagliati, F. (2002) Genetic monitoring of brackish-water populations: the Mediterranean toothcarp Aphanius fasciatus (Cyprinodontidae) as a model. Marine Ecology Progress Series 235, 257–262.Google Scholar
Mathivat-Lallier, M.H. and Cazaux, C. (1991) Life-history of Nephtys hombergii in Arachon Bay. Estuarine, Coastal and Shelf Science 32, 1–9.Google Scholar
Olive, P.J.W., Garwood, P.R., Bentley, M.G. and Wright, N. (1981) Reproductive success, relative abundance and population structure of two species of Nephtys in an estuarine beach. Marine Biology 63, 189–196.Google Scholar
Palumbi, S.R. (1992) Marine speciation on a small planet. Trends in Ecology and Evolution 7, 114–118.CrossRefGoogle ScholarPubMed
Parsons, T.R., Maita, Y. and Lalli, C.M. (1984) Manual of chemical and biological methods for seawater analysis. Oxford: Pergamon Press.Google Scholar
Patarnello, T., Volckaert, F.A.M.J. and Castilho, R. (2007) Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Molecular Ecology 16, 4426–4444.Google Scholar
Pérez-Ruzafa, A., Fernández, A.I., Marcos, C., Gilabert, J., Quispe, J.I. and García-Charton, J.A. (2005) Spatial and temporal variations of hydrological conditions, nutrients and chlorophyll a in a Mediterranean coastal lagoon (Mar Menor, Spain). Hydrobiologia 550, 11–27.Google Scholar
Pérez-Ruzafa, A., Marcos, C., Pérez-Ruzafa, I.M., Barcala, E., Hegazi, M.I. and Quispe, J. (2007) Detecting changes resulting from human pressure in a naturally quick-changing and heterogeneous environment: spatial and temporal scales of variability in coastal lagoons. Estuarine, Coastal and Shelf Science 75, 175–188.Google Scholar
Polytraits Team (2013) A database on biological traits of polychaetes. LifewatchGreece, Hellenic Centre for Marine Research. Available at http://polytraits.lifewatchgreece.eu/Google Scholar
Posada, D. and Crandall, K. (2001) Intraspecific gene genealogies: trees grafting into networks. Trends in Ecology and Evolution 16, 37–45.Google Scholar
Prado, P., Caiola, N. and Ibáñez, C. (2014a) Freshwater inflows and seasonal forcing strongly influence macrofaunal assemblages in Mediterranean coastal lagoons. Estuarine, Coastal and Shelf Science 147, 68–77.CrossRefGoogle Scholar
Prado, P., Vergara, C., Caiola, N. and Ibáñez, C. (2014b) Influence of salinity regime on the food-web structure and feeding ecology of fish species from Mediterranean coastal lagoons. Estuarine, Coastal and Shelf Science 139, 1–10.Google Scholar
Puillandre, N., Lambert, A., Brouillet, S. and Achaz, G. (2011) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21, 1864–1877.Google Scholar
Rainer, S.F. (1991) The genus Nephtys (Polychaeta: Phyllodocida) of northern Europe: a review of species, including the description of N. pulchra sp. n. and a key to the Nephtyidae. Helgoländer Meeresuntersuchungen 45, 65–96.Google Scholar
Ray, N., Currat, M. and Excoffier, L. (2003) Intra-deme molecular diversity in spatially expanding populations. Molecular Biology and Evolution 20, 76–86.Google Scholar
Reizopoulou, S., Thessalou-Legaki, M. and Nicolaidou, A. (1996) Assessment of disturbance in Mediterranean lagoons: an evaluation of methods. Marine Biology 125, 189–197.Google Scholar
Reusch, T.B.H., Ehlers, A., Hämmerli, A. and Worm, B. (2005) Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proceedings of the National Academy of Sciences USA 102, 2826–2831.Google Scholar
Riginos, C. and Liggins, L. (2013) Seascape genetics: populations, individuals and genes marooned and adrift. Geography Compass 7, 197–216.Google Scholar
Rodrigues, F., Valente, S. and González-Wanguemert, M. (2015) Genetic diversity across geographical scales in marine coastal ecosystems: Holothuria arguinensis a model species. Journal of Experimental Marine Biology and Ecology 463, 158–167.Google Scholar
Sanford, E. and Kelly, M.W. (2011) Local adaptation in marine invertebrates. Annual Review of Marine Science 3, 509–535.Google Scholar
Schmidt, H. and Westheide, W. (1994) Isozymes and general protein patterns as taxonomic markers in the taxon Nephtyidae (Annelida Polychaeta). Marine Biology 119, 31–38.Google Scholar
Selkoe, K.A., Watson, J.R., White, C., Ben Horin, T., Iacchei, M., Mitarai, S., Siegel, D.A., Gaines, S.D. and Toonen, R.J. (2010) Taking the chaos out of genetic patchiness: seascape genetics reveals ecological and oceanographic drivers of genetic patterns in three temperate reef species. Molecular Ecology 19, 3708–3726.Google Scholar
Sfriso, A., Birkemeyer, T. and Ghetti, P.F. (2001) Benthic macrofauna changes in areas of Venice lagoon populated by seagrasses or seaweeds. Marine Environmental Research 52, 323–349.CrossRefGoogle ScholarPubMed
Shafer, A.B.A. and Wolf, J.B.W. (2013) Widespread evidence for incipient ecological speciation: a meta-analysis of isolation-by-ecology. Ecology Letters 16, 940–950.Google Scholar
Tajima, F. (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.Google Scholar
Tamura, K., Peterson, D. and Peterson, N. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.Google Scholar
Vandamme, S.G., Maes, G.E., Raeymaekers, J.A., Cottenie, K., Imsland, A.K., Hellemans, B., Lacroix, G., Mac Aoidh, E., Martinsohn, J.T., Martínez, P., Robbens, J., Vilas, R. and Volckaert, F.A. (2014) Regional environmental pressure influences population differentiation in turbot (Scophthalmus maximus). Molecular Ecology 23, 618–636.Google Scholar
Vergara-Chen, C., Gonzalez-Wanguemert, M., Marcos, C. and Perez-Ruzafa, A. (2013) Small-scale genetic structure of Cerastoderma glaucum in a lagoonal environment: potential significance of habitat discontinuity and unstable population dynamics. Journal of Molluscan Studies 79, 230–240.Google Scholar
Vignes, F., Barbone, E., Breber, P., Adamo, R.D., Leonilde, R., Ungaro, N., Focardi, S., Renzi, M. and Basset, A. (2009) Spatial and temporal description of the dystrophic crisis in Lesina lagoon during summer 2008. Transitional Waters Bulletin 3, 47–62.Google Scholar
Yentsch, C.S. and Menzel, D.W. (1963) A method for the determination of phytoplankton chlorophyll and phaeophytin by fluorescence. Deep Sea Research and Oceanographic Abstracts 10, 221–231.Google Scholar
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