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Coral Reefs

, Volume 35, Issue 1, pp 39–52 | Cite as

Into the depth of population genetics: pattern of structuring in mesophotic red coral populations

  • Federica Costantini
  • Marco Abbiati
Report

Abstract

Deep-sea reef-building corals are among the most conspicuous invertebrates inhabiting the hard-bottom habitats worldwide and are particularly susceptible to human threats. The precious red coral (Corallium rubrum, L. 1758) has a wide bathymetric distribution, from shallow up to 800 m depth, and represents a key species in the Mediterranean mesophotic reefs. Several studies have investigated genetic variability in shallow-water red coral populations, while geographic patterns in mesophotic habitats are largely unknown. This study investigated genetic variability of C. rubrum populations dwelling between 55 and 120 m depth, from the Ligurian to the Ionian Sea along about 1500 km of coastline. A total of 18 deep rocky banks were sampled. Colonies were analyzed by means of a set of microsatellite loci and the putative control region of the mitochondrial DNA. Collected data were compared with previous studies. Both types of molecular markers showed high genetic similarity between populations within the northern (Ligurian Sea and Tuscan Archipelago) and the southern (Tyrrhenian and Ionian seas) study areas. Variability in habitat features between the sampling sites did not affect the genetic variability of the populations. Conversely, the patchy distribution of suitable habitats affected populations’ connectivity within and among deep coral banks. Based on these results and due to the emphasis on red coral protection in the Mediterranean Sea by international institutions, red coral could be promoted as a ‘focal species’ to develop management plans for the conservation of deep coralligenous reefs, a reservoir of marine biodiversity.

Keywords

Corallium rubrum Microsatellites Mediterranean Sea ROV 

Notes

Acknowledgments

We thank the ROV operator S. Canese and the whole crew of the R/V Astrea for their operational and logistical support and the professional divers for Apulia sampling. We thank L. Rugiu for his support in collecting the samples and R. Pugliese for her help with the laboratory work. We are grateful to M. Ponti for helping to draw the map. We are grateful to A. Villamor for her valuable, friendly and helpful support during the different stages of this study. We thank G. Corriero for providing the samples of red coral from the Ionian Sea. This work was financed by Ministero dell’Ambiente e della Tutela del Territorio e del Mare (Project 2010, Studio di popolazioni di Corallo rosso profondo) and by Ministero delle Politiche Agricole, Alimentari e Forestali (Project 2012, Use of ROV in the management of deep C. rubrum populations). We thank project coordinators G. Santangelo and G. Bavestrello, respectively. This study was also supported by the PRIN 2011 project on ‘Coastal bioconstructions: structure, function and management.’ The final version of the manuscript has very much improved thanks to the comments of two anonymous reviewers and G. Tsounis.

References

  1. Abbiati M, Santangelo G, Novelli S (1993) Genetic variation within and between two Tyrrhenian populations of the Mediterranean alcyonarian Corallium rubrum. Mar Ecol Prog Ser 95:245–250CrossRefGoogle Scholar
  2. Abbiati M, Novelli S, Harmelin JC, Santangelo G (1997) Struttura genetica di popolamenti simpatrici e allopatici di corallo rosso. In: Cicogna F, Bavestrello G, Cattaneo-Vietti R (eds) Biologia e tutela del corallo rosso e di altri ottocoralli del Mediterraneo. Ministero delle Politiche Agricole, Rome, pp 5–21Google Scholar
  3. Addamo AM, Reimer JD, Taviani M, Freiwald A, Machordom A (2012) Desmophyllum dianthus (Esper, 1794) in the scleractinian phylogeny and its intraspecific diversity. PLoS ONE 7:e50215PubMedCentralCrossRefPubMedGoogle Scholar
  4. Airoldi L (1998) Roles of disturbance, sediment stress, and substratum retention on spatial dominance in algal turf. Ecology 79:2759–2770CrossRefGoogle Scholar
  5. Airoldi L, Balata D, Beck M (2008) The Gray Zone: relationships between habitat loss and marine diversity and their applications in conservation. J Exp Mar Bio Ecol 366:8–15CrossRefGoogle Scholar
  6. Astraldi M, Gasparini GP (1994) The seasonal characteristics of the circulation of the Tyrrhenian Sea. In La Violette PE (ed) Seasonal and interannual variability of the Western Mediterranean Sea. Coastal and Estuarine Studies 46:115–134Google Scholar
  7. Aurelle D, Ledoux J-B (2013) Interplay between isolation by distance and genetic clusters in the red coral Corallium rubrum: insights from simulated and empirical data. Conserv Genet 14:705–716CrossRefGoogle Scholar
  8. Aurelle D, Ledoux J-B, Rocher C, Borsa P, Chenuil A, Féral J-P (2011) Phylogeography of the red coral (Corallium rubrum): inferences on the evolutionary history of a temperate gorgonian. Genetica 139:855–869CrossRefPubMedGoogle Scholar
  9. Balata D, Piazzi L, Cecchi E, Cinelli F (2005) Variability of Mediterranean coralligenous assemblages subject to local variation in sediment deposition. Mar Environ Res 60:403–421CrossRefPubMedGoogle Scholar
  10. Ballesteros E (2006) Mediterranean coralligenous assemblages:A synthesis of present knowledge. Oceanogr Mar Biol Annu Rev 44:123–195Google Scholar
  11. Bandelt H, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefPubMedGoogle Scholar
  12. Bavestrello G, Bo M, Canese S, Sandulli R, Cattaneo-Vietti R (2014a) The red coral populations of the gulfs of Naples and Salerno: human impact and deep mass mortalities. Ital J Zool 81:552–563CrossRefGoogle Scholar
  13. Bavestrello G, Abbiati M, Angiolillo M, Betti F, Bo M, Canese S, Cattaneo-Vietti R, Cau A, Corriero G, Costantini F, Giusti M, Priori C, Salvati E, Sandulli R, Santangelo G, Tunesi L (2014b) Remotely Operated Vehicles (ROVs) as powerful tools for the evaluation of the conservation status of deep red coral banks. In: Bouafif C, Langar H, Ouerghi A (Eds), UNEP/MAP–RAC/SPA, Proceedings of the second Mediterranean Symposium on the conservation of Coralligenous and other Calcareous Bio- Concretions (Portoroz, Slovenia, 29–30 October 2014). pp 31–36Google Scholar
  14. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, Logiciel sous Windows pour la Génétique des Populations. Laboratorie Génome, Populations, Interactions, CNRS UMR. 5000. Université de Montpellier II, Montpellier, FranceGoogle Scholar
  15. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57:289–300Google Scholar
  16. Bo M, Bava S, Canese S, Angiolillo M, Cattaneo-Vietti R, Bavestrello G (2014) Fishing impact on deep Mediterranean rocky habitats as revealed by ROV investigation. Biol Conserv 171:167–176CrossRefGoogle Scholar
  17. Bo M, Bavestrello G, Canese S, Giusti M, Salvati E, Angiolillo M, Greco S (2009) Characteristics of a black coral meadow in the twilight zone of the central Mediterranean Sea. Mar Ecol Prog Ser 397:53–61CrossRefGoogle Scholar
  18. Bo M, Bavestrello G, Canese S, Giusti M, Angiolillo M, Cerrano C, Salvati E, Greco S (2011) Coral assemblage off the Calabrian Coast (South Italy) with new observations on living colonies of Antipathes dichotoma. Ital J Zool 78:231–242CrossRefGoogle Scholar
  19. Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010a) Assessing the “deep reef refugia” hypothesis: focus on Caribbean reefs. Coral Reefs 29:309–327CrossRefGoogle Scholar
  20. Bongaerts P, Riginos C, Ridgway T, Sampayo EM, van Oppen MJH, Englebert N, Vermeulen F, Hoegh-Guldberg O (2010b) Genetic divergence across habitats in the widespread coral Seriatopora hystrix and its associated Symbiodinium. PLoS ONE 5:e10871PubMedCentralCrossRefPubMedGoogle Scholar
  21. Brazeau DA, Lesser MP, Slattery M (2013) Genetic structure in the coral, Montastraea cavernosa: assessing genetic differentiation among and within mesophotic reefs. PLoS One 8:e65845PubMedCentralCrossRefPubMedGoogle Scholar
  22. Bruckner A (2014) Advances in management of precious corals in the family Corallidae: are new measures adequate? Curr Opin Environ Sustain 7:1–8CrossRefGoogle Scholar
  23. Cannas R, Sacco F, Cau A, Cuccu D, Follesa MC, Cau A (2014) Genetic monitoring of deep-water exploited banks of the precious Sardinia coral Corallium rubrum (L., 1758): useful data for a sustainable management. Aquat Conserv Mar Freshw Ecosyst. doi: 10.1002/aqc.2522 Google Scholar
  24. Chapuis M, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631CrossRefPubMedGoogle Scholar
  25. Clark MR, Rowden AA, Schlacher T, Williams A, Consalvey M, Stocks KI, Hall-Spencer JM (2010) The ecology of seamounts: structure, function, and human impacts. Ann Rev Mar Sci 2:253–278CrossRefPubMedGoogle Scholar
  26. Corander J, Marttinen P (2006) Bayesian identification of admixture events using multilocus molecular markers. Mol Ecol 15:2833–2843CrossRefPubMedGoogle Scholar
  27. Corander J, Marttinen P, Sirén J, Tang J (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9:539PubMedCentralCrossRefPubMedGoogle Scholar
  28. Costantini F, Abbiati M (2006) Development of microsatellite markers for the Mediterranean gorgonian coral Corallium rubrum. Mol Ecol Notes 6:521–523CrossRefGoogle Scholar
  29. Costantini F, Fauvelot C, Abbiati M (2007a) Genetic structuring of the temperate gorgonian coral (Corallium rubrum) across the western Mediterranean Sea revealed by microsatellites and nuclear sequences. Mol Ecol 16:5168–5182CrossRefPubMedGoogle Scholar
  30. Costantini F, Fauvelot C, Abbiati M (2007b) Fine-scale genetic structuring in Corallium rubrum: evidence of inbreeding and limited effective larval dispersal. Mar Ecol Prog Ser 340:109–119CrossRefGoogle Scholar
  31. Costantini F, Carlesi L, Abbiati M (2013) Quantifying spatial genetic structuring in mesophotic populations of the precious coral Corallium rubrum. PLoS ONE 8:e61546PubMedCentralCrossRefPubMedGoogle Scholar
  32. Costantini F, Aurelle D, Ledoux J-B, Abbiati M (in press) Population genetic structure of Corallium rubrum in the Mediterranean Sea: diversity, phylogeography, and bathymetric patterns. In: Goffredo S, Dubinsky Z (eds) The Cnidaria, past, present and future. The world of Medusa and her sisters. Springer International Publishing, ChamGoogle Scholar
  33. Costantini F, Rossi S, Pintus E, Cerrano C, Gili J-M, Abbiati M (2011) Low connectivity and declining genetic variability along a depth gradient in Corallium rubrum populations. Coral Reefs 30:991–1003CrossRefGoogle Scholar
  34. Costantini F, Taviani M, Remia A, Pintus E, Schembri PJ, Abbiati M (2010) Deep-water Corallium rubrum (L., 1758) from the Mediterranean Sea: preliminary genetic characterisation. Mar Ecol 31:261–269CrossRefGoogle Scholar
  35. Danovaro R, Corinaldesi C, D’Onghia G, Galil B, Gambi C, Gooday A, Lampadariou N, Luna G, Morigi C, Olu K, Polymenakou P (2010) Deep-sea biodiversity in the Mediterranean Sea: The known, the unknown, and the unknowable. PLoS ONE 5:e11832PubMedCentralCrossRefPubMedGoogle Scholar
  36. Davies AJ, Roberts JM, Hall-Spencer J (2007) Preserving deep-sea natural heritage: Emerging issues in offshore conservation and management. Biol Conserv 138:299–312CrossRefGoogle Scholar
  37. Dempster A, Laird N, Rubin D (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc Series B Stat Methodol 39:1–38Google Scholar
  38. Fabri MC, Pedel L, Beuck L, Galgani F, Hebbeln D, Freiwald A (2014) Megafauna of vulnerable marine ecosystems in French mediterranean submarine canyons: Spatial distribution and anthropogenic impacts. Deep Sea Res Part 2 Top Stud Oceanogr 104:184–207CrossRefGoogle Scholar
  39. Follesa MC, Cannas R, Cau A, Pedoni C, Pesci P, Cau A (2013) Deep-water red coral from the island of Sardinia (north-western Mediterranean): a local example of sustainable management. Mar Freshw Res 64:706–715CrossRefGoogle Scholar
  40. Freiwald A, Beuck L, Ruggeberg A, Taviani M, Hebbeln D, R/V Meteor Cruise M70–1 participants (2009) The white coral community in the Central Mediterranean Sea revealed by ROV surveys. Oceanography 22:58–74CrossRefGoogle Scholar
  41. Fu Y (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedCentralPubMedGoogle Scholar
  42. FAO, GFCM (2010) Report of the transversal workshop on red coral Alghero (Sardinia), Italy. General Fisheries Commission for the Mediterranean Scientific Advisory Committee, thirteenth Session Marseille, France, 7–11 February 2011Google Scholar
  43. FAO, GFCM (2014) Appendix I. Guidelines for the management of Mediterranean red coral populations. Report of the thirty-eighth session of the General Fisheries Commission for the Mediterranean, Rome, Italy, 19–24 May 2014Google Scholar
  44. Gori A, Rossi S, Linares C, Berganzo E, Orejas C, Dale MR, Gili J-M (2011) Size and spatial structure in deep versus shallow populations of the Mediterranean gorgonian Eunicella singularis (Cap de Creus, northwestern Mediterranean Sea). Mar Biol 158:1721–1732CrossRefGoogle Scholar
  45. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  46. Herrera S, Shank TM (2015) RAD sequencing enables unprecedented phylogenetic resolution and objective species delimitation in recalcitrant divergent taxa. bioRxiv 019745Google Scholar
  47. Herrera S, Shank TM, Sánchez JA (2012) Spatial and temporal patterns of genetic variation in the widespread antitropical deep-sea coral Paragorgia arborea. Mol Ecol 21:6053–6067CrossRefPubMedGoogle Scholar
  48. Kahng S, Copus J, Wagner D (2014) Recent advances in the ecology of mesophotic coral ecosystems (MCEs). Curr Opin Environ Sustain 7:72–81CrossRefGoogle Scholar
  49. Kalinowski ST (2005) hp-rare 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189CrossRefGoogle Scholar
  50. Kendall M, Stewart A (1977) The advanced theory of statistics, vol 1. Macmillan, New YorkGoogle Scholar
  51. Keough MJ, Downes BJ (1982) Recruitment of marine invertebrates : the role of active larval choices and early mortality. Oecologia 54:348–352CrossRefGoogle Scholar
  52. Ledoux J-B, Aurelle D, Bensoussan N, Marschal C, Féral J-P, Garrabou J (2015) Potential for adaptive evolution at species range margins: contrasting interactions between red coral populations and their environment in a changing ocean. Ecol Evol 5:1178–1192PubMedCentralCrossRefPubMedGoogle Scholar
  53. Ledoux J-B, Garrabou J, Bianchimani O, Drap P, Féral J-P, Aurelle D (2010a) Fine-scale genetic structure and inferences on population biology in the threatened Mediterranean red coral, Corallium rubrum. Mol Ecol 19:4204–4216CrossRefPubMedGoogle Scholar
  54. Ledoux J-B, Mokhtar-Jamaï K, Roby C, Féral J-P, Garrabou J, Aurelle D (2010b) Genetic survey of shallow populations of the Mediterranean red coral [Corallium rubrum (Linnaeus, 1758)]: new insights into evolutionary processes shaping nuclear diversity and implications for conservation. Mol Ecol 19:675–690CrossRefPubMedGoogle Scholar
  55. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  56. Linares C, Coma R, Diaz D, Zabala M, Hereu B, Dantart L (2005) Immediate and delayed effects of a mass mortality event on gorgonian population dynamics and benthic community structure in the NW Mediterranean Sea. Mar Ecol Prog Ser 305:127–137CrossRefGoogle Scholar
  57. Lindsay SM, Wethey DS, Woodin SA (1997) Modeling interactions of browsing predation, infaunal activity, and recruitment in marine soft-sediment habitats. Am Nat 148:684–699CrossRefGoogle Scholar
  58. Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237CrossRefGoogle Scholar
  59. Marsili L (1725) Histoire physique de la mer. Aux depens de la comp, Amsterdam, NetherlandsGoogle Scholar
  60. Martínez-Quintana A, Bramanti L, Viladrich N, Rossi S, Guizien K (2014) Quantification of larval traits driving connectivity: the case of Corallium rubrum (L. 1758). Mar Biol 162:309–318CrossRefGoogle Scholar
  61. McFadden C, van Ofwegen L (2012) Stoloniferous octocorals (Anthozoa, Octocorallia) from South Africa, with descriptions of a new family of Alcyonacea, a new genus of Clavulariidae, and a new species of Cornularia (Cornulariidae). Invertebr Syst 26:331–356CrossRefGoogle Scholar
  62. Mercurio M, Cardone F (2012) Dati preliminari sul corallo rosso delle coste pugliesi. Biol Mar Mediterr 19:178–179Google Scholar
  63. Morato T, Watson R, Pitcher TJ, Pauly D (2006) Fishing down the deep. Fish Fish 7:24–34CrossRefGoogle Scholar
  64. Morrison CL, Ross SW, Nizinski MS, Brooke S, Järnegren J, Waller RG, Johnson RL, King TL (2011) Genetic discontinuity among regional populations of Lophelia pertusa in the North Atlantic Ocean. Conserv Genet 12:713–729CrossRefGoogle Scholar
  65. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  66. Pante E, Watling L (2011) Chrysogorgia from the New England and Corner Seamounts: Atlantic-Pacific connections. J Mar Biol Assoc U.K. 92:911–927CrossRefGoogle Scholar
  67. Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  68. Piry S, Luikart G, Cornuet J (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  69. Ponti M, Perlini RA, Ventra V, Grech D, Abbiati M, Cerrano C (2014) Ecological shifts in Mediterranean coralligenous assemblages related to gorgonian forest loss. PLoS ONE 9:e102782PubMedCentralCrossRefPubMedGoogle Scholar
  70. Priori C, Mastascusa V, Erra F, Angiolillo M, Canese S, Santangelo G (2013) Demography of deep-dwelling red coral populations: age and reproductive structure of a highly valued marine species. Estuar Coast Shelf Sci 118:43–49CrossRefGoogle Scholar
  71. Pyle R (2000) Assessing undiscovered fish biodiversity on deep coral reefs using advanced self-contained diving technology. Mar Technol Soc J 34:82–91CrossRefGoogle Scholar
  72. Quattrini AM, Georgian SE, Byrnes L, Stevens A, Falco R, Cordes EE (2013a) Niche divergence by deep-sea octocorals in the genus Callogorgia across the continental slope of the Gulf of Mexico. Mol Ecol 22:4123–4140CrossRefPubMedGoogle Scholar
  73. Quattrini AM, Etnoyer PJ, Doughty C, English L, Falco R, Remon N, Rittinghouse M, Cordes EE (2013b) A phylogenetic approach to octocoral community structure in the deep Gulf of Mexico. Deep Sea Res Part 2 Top Stud Oceanogr 99:92–102CrossRefGoogle Scholar
  74. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283CrossRefGoogle Scholar
  75. Rogers AD (2000) The role of the oceanic oxygen minima in generating biodiversity in the deep sea. Deep Res Part 2 Top Stud Oceanogr 47:119–148CrossRefGoogle Scholar
  76. Rogers A, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  77. Santangelo G, Abbiati M (2001) Red coral: conservation and management of an over-exploited Mediterranean species. Aquat Conserv 11:253–259CrossRefGoogle Scholar
  78. Slatkin M (1987) Gene flow and geographic structure of natural populations. Science 236:787–792CrossRefPubMedGoogle Scholar
  79. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralCrossRefPubMedGoogle Scholar
  80. Tang J, Hanage WP, Fraser C, Corander J (2009) Identifying currents in the gene pool for bacterial populations using an integrative approach. PLoS Comput Biol 5:e1000455PubMedCentralCrossRefPubMedGoogle Scholar
  81. Tescione G (1973) The Italians and their Coral Fishing. Fausto Fiorino, NaplesGoogle Scholar
  82. Thoma J, Pante E, Brugler M, France S (2009) Deep-sea octocorals and antipatharians show no evidence of seamount-scale endemism in the NW Atlantic. Mar Ecol Prog Ser 397:25–35CrossRefGoogle Scholar
  83. Torrents O, Garrabou J (2011) Fecundity of red coral Corallium rubrum (L.) populations inhabiting in contrasting environmental conditions in the NW Mediterranean. Mar Biol 158:1019–1028CrossRefGoogle Scholar
  84. Tsounis G, Rossi S, Grigg R, Santangelo G, Bramanti L, Gili J-M (2010) The exploitation and conservation of precious corals. Oceanogr Mar Biol Ann Rev 48:161–212Google Scholar
  85. van Oppen MJH, Bongaerts P, Underwood JN, Peplow LM, Cooper TF (2011) The role of deep reefs in shallow reef recovery: an assessment of vertical connectivity in a brooding coral from west and east Australia. Mol Ecol 20:1647–1660CrossRefPubMedGoogle Scholar
  86. Vellend M, Geber M (2005) Connections between species diversity and genetic diversity. Ecol Lett 8:767–781CrossRefGoogle Scholar
  87. Vetrano A, Napolitano E, Iacono R, Schroeder K, Gasparini GP (2010) Tyrrhenian Sea circulation and water mass fluxes in Spring 2004: observations and model results. J Geophys Res 115:C06023Google Scholar
  88. Villamor A, Costantini F, Abbiati M (2014) Genetic structuring across marine biogeographic boundaries in rocky shore invertebrates. PLoS ONE 9:e101135PubMedCentralCrossRefPubMedGoogle Scholar
  89. Virgilio M, Airoldi L, Abbiati M (2006) Spatial and temporal variations of assemblages in a Mediterranean coralligenous reef and relationships with surface orientation. Coral Reefs 25:265–272CrossRefGoogle Scholar
  90. Weir B, Cockerham C (1984) Estimating F-statistics for the analysis of population structure. Evolution (N Y) 38:1358–1370Google Scholar
  91. Winnepenninckx B, Backeljau T, De Wachter R (1993) Extraction of high molecular weight DNA from molluscs. Trends Genet 9:407CrossRefPubMedGoogle Scholar
  92. Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Dipartimento di Scienze Biologiche, Geologiche ed Ambientali and Centro Interdipartimentale di Ricerca per le Scienze AmbientaliUniversity of Bologna, ULR CoNISMaRavennaItaly
  2. 2.Consiglio Nazionale delle Ricerche, Istituto di Scienze MarineISMARBolognaItaly

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