Evolutionary Biology

Separate the wheat from the chaff: genomic scan for local adaptation in the red coral Corallium rubrum

10.24072/pcjournal.12 - Peer Community Journal, Volume 1 (2021), article no. e31.

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Genomic data allow an in-depth and renewed study of local adaptation. The red coral (Corallium rubrum, Cnidaria) is a highly genetically structured species and a promising model for the study of adaptive processes along an environmental gradient. Here, we used RAD-Sequencing in order to study the vertical genetic structure of this species and to search for signals of local adaptation to depth and thermal regime in the red coral. Previous studies have shown different thermotolerance levels according to depth in this species which could correspond to genetic or environmental differences. We designed a sampling scheme with six pairs of shallow vs deep populations distributed in three geographical regions as replicates. Our results showed significant differentiation among locations and among sites separated by around 20 m depth. The tests of association between genetics and environment allowed the identification of candidate loci under selection but with a potentially high rate of false positive. We discuss the methodological obstacles and biases encountered for the detection of selected loci in such a strongly genetically structured species. On this basis, we also discuss the significance of the candidate loci for local adaptation detected in each geographical region and the evolution of red coral populations along environmental gradients.

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DOI: 10.24072/pcjournal.12
Pratlong, M. 1, 2; Haguenauer, A. 1, 3; Brener, K. 4; Mitta, G. 4; Toulza, E. 4; Garrabou, J. 5, 6; Bensoussan, N. 7; Pontarotti, P. 2, 8; Aurelle, D. 1, 5, 9

1 Aix Marseille Univ, Avignon Université, CNRS, IRD, IMBE, Marseille, France
2 Aix Marseille Univ, CNRS, Centrale Marseille, I2M, Equipe Evolution Biologique et Modélisation, Marseille, France
3 CRIOBE - Perpignan, USR3278 CRIOBE EPHE-CNRS-UPVD, France
4 IHPE, Univ Montpellier, CNRS, IFREMER, Univ Perpignan Via Domitia, Perpignan, France
5 Aix Marseille Univ., Université de Toulon, CNRS, IRD, MIO UM 110, 13288, Marseille, France
6 Institute of Marine Sciences (ICM-CSIC), Barcelona, 08003, Spain
7 IPSO FACTO, SCOPArl, Pole Océanologie, Marseille, 13001, France
8 Aix Marseille Univ, IRD, APHM, Microbe, Evolution, Phylogénie, Infection, IHU Méditerranée Infection, Marseille, France
9 Institut de Systématique, Evolution, Biodiversité (ISYEB), Muséum national d'Histoire naturelle, CNRS, Sorbonne Université, EPHE, 57 rue Cuvier, 75005 Paris, France
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Pratlong, M.; Haguenauer, A.; Brener, K.; Mitta, G.; Toulza, E.; Garrabou, J.; Bensoussan, N.; Pontarotti, P.; Aurelle, D. Separate the wheat from the chaff: genomic scan for local adaptation in the red coral Corallium rubrum. Peer Community Journal, Volume 1 (2021), article  no. e31. doi : 10.24072/pcjournal.12. https://peercommunityjournal.org/articles/10.24072/pcjournal.12/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100061

[1] Alleaume-Benharira, M.; Pen, I. R.; Ronce, O. Geographical patterns of adaptation within a species' range: interactions between drift and gene flow, Journal of Evolutionary Biology, Volume 19 (2006) no. 1, pp. 203-215 | Article

[2] Altschul, S. F.; Gish, W.; Miller, W.; Myers, E. W.; Lipman, D. J. Basic local alignment search tool, Journal of Molecular Biology, Volume 215 (1990) no. 3, pp. 403-410 | Article

[3] Araneda, C.; Larraín, M. A.; Hecht, B.; Narum, S. Adaptive genetic variation distinguishes Chilean blue mussels ( Mytilus chilensis ) from different marine environments, Ecology and Evolution, Volume 6 (2016) no. 11, pp. 3632-3644 | Article

[4] Ayre, D. J. Localized Adaptation of Sea Anemone Clones: Evidence from Transplantation Over Two Spatial Scales, The Journal of Animal Ecology, Volume 64 (1995) no. 2 | Article

[5] Barrett, R. D. H.; Hoekstra, H. E. Molecular spandrels: tests of adaptation at the genetic level, Nature Reviews Genetics, Volume 12 (2011) no. 11, pp. 767-780 | Article

[6] Barshis, D. J.; Ladner, J. T.; Oliver, T. A.; Seneca, F. O.; Traylor-Knowles, N.; Palumbi, S. R. Genomic basis for coral resilience to climate change, Proceedings of the National Academy of Sciences, Volume 110 (2013) no. 4, pp. 1387-1392 | Article

[7] BARSHIS, D. J.; STILLMAN, J. H.; GATES, R. D.; TOONEN, R. J.; SMITH, L. W.; BIRKELAND, C. Protein expression and genetic structure of the coralPorites lobatain an environmentally extreme Samoan back reef: does host genotype limit phenotypic plasticity?, Molecular Ecology, Volume 19 (2010) no. 8, pp. 1705-1720 | Article

[8] Bay, R. A.; Palumbi, S. R. Multilocus Adaptation Associated with Heat Resistance in Reef-Building Corals, Current Biology, Volume 24 (2014) no. 24, pp. 2952-2956 | Article

[9] Benestan, L.; Quinn, B. K.; Maaroufi, H.; Laporte, M.; Clark, F. K.; Greenwood, S. J.; Rochette, R.; Bernatchez, L. Seascape genomics provides evidence for thermal adaptation and current-mediated population structure in American lobster (Homarus americanus), Molecular Ecology, Volume 25 (2016) no. 20, pp. 5073-5092 | Article

[10] Benjamini, Y.; Hochberg, Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing, Journal of the Royal Statistical Society: Series B (Methodological), Volume 57 (1995) no. 1, pp. 289-300 | Article

[11] Bernardi, G.; Azzurro, E.; Golani, D.; Miller, M. R. Genomic signatures of rapid adaptive evolution in the bluespotted cornetfish, a Mediterranean Lessepsian invader, Molecular Ecology, Volume 25 (2016) no. 14, pp. 3384-3396 | Article

[12] Bierne, N.; Roze, D.; Welch, J. J. Pervasive selection or is it…? why areFSToutliers sometimes so frequent?, Molecular Ecology, Volume 22 (2013) no. 8, pp. 2061-2064 | Article

[13] Bierne, N.; Welch, J.; Loire, E.; Bonhomme, F.; David, P. The coupling hypothesis: why genome scans may fail to map local adaptation genes, Molecular Ecology, Volume 20 (2011) no. 10, pp. 2044-2072 | Article

[14] Boavida, J.; Paulo, D.; Aurelle, D.; Arnaud-Haond, S.; Marschal, C.; Reed, J.; Gonçalves, J. M. S.; Serrão, E. A. A Well-Kept Treasure at Depth: Precious Red Coral Rediscovered in Atlantic Deep Coral Gardens (SW Portugal) after 300 Years, PLOS ONE, Volume 11 (2016) no. 1 | Article

[15] Bongaerts, P.; Riginos, C.; Brunner, R.; Englebert, N.; Smith, S. R.; Hoegh-Guldberg, O. Deep reefs are not universal refuges: Reseeding potential varies among coral species, Science Advances, Volume 3 (2017) no. 2 | Article

[16] Bongaerts, P.; Riginos, C.; Hay, K. B.; van Oppen, M. J.; Hoegh-Guldberg, O.; Dove, S. Adaptive divergence in a scleractinian coral: physiological adaptation of Seriatopora hystrix to shallow and deep reef habitats, BMC Evolutionary Biology, Volume 11 (2011) no. 1 | Article

[17] Bradbury, I. R.; Hubert, S.; Higgins, B.; Borza, T.; Bowman, S.; Paterson, I. G.; Snelgrove, P. V. R.; Morris, C. J.; Gregory, R. S.; Hardie, D. C.; Hutchings, J. A.; Ruzzante, D. E.; Taggart, C. T.; Bentzen, P. Parallel adaptive evolution of Atlantic cod on both sides of the Atlantic Ocean in response to temperature, Proceedings of the Royal Society B: Biological Sciences, Volume 277 (2010) no. 1701, pp. 3725-3734 | Article

[18] Cannas, R.; Sacco, F.; Cau, A.; Cuccu, D.; Follesa, M. C.; Cau, A. Genetic monitoring of deep-water exploited banks of the precious Sardinia coralCorallium rubrum(L., 1758): useful data for a sustainable management, Aquatic Conservation: Marine and Freshwater Ecosystems, Volume 26 (2016) no. 2, pp. 236-250 | Article

[19] Catchen, J. M.; Amores, A.; Hohenlohe, P.; Cresko, W.; Postlethwait, J. H. Stacks: Building and Genotyping Loci De Novo From Short-Read Sequences, G3 Genes|Genomes|Genetics, Volume 1 (2011) no. 3, pp. 171-182 | Article

[20] Catchen, J.; Hohenlohe, P. A.; Bassham, S.; Amores, A.; Cresko, W. A. Stacks: an analysis tool set for population genomics, Molecular Ecology, Volume 22 (2013) no. 11, pp. 3124-3140 | Article

[21] Catchen, J. M.; Hohenlohe, P. A.; Bernatchez, L.; Funk, W. C.; Andrews, K. R.; Allendorf, F. W. Unbroken: RADseq remains a powerful tool for understanding the genetics of adaptation in natural populations, Molecular Ecology Resources, Volume 17 (2017) no. 3, pp. 362-365 | Article

[22] Chu, N. D.; Kaluziak, S. T.; Trussell, G. C.; Vollmer, S. V. Phylogenomic analyses reveal latitudinal population structure and polymorphisms in heat stress genes in the North Atlantic snailNucella lapillus, Molecular Ecology, Volume 23 (2014) no. 7, pp. 1863-1873 | Article

[23] Conesa, A.; Gotz, S.; Garcia-Gomez, J. M.; Terol, J.; Talon, M.; Robles, M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research, Bioinformatics, Volume 21 (2005) no. 18, pp. 3674-3676 | Article

[24] Coop, G.; Witonsky, D.; Di Rienzo, A.; Pritchard, J. K. Using Environmental Correlations to Identify Loci Underlying Local Adaptation, Genetics, Volume 185 (2010) no. 4, pp. 1411-1423 | Article

[25] Costantini, F.; Fauvelot, C.; Abbiati, M. Genetic structuring of the temperate gorgonian coral (Corallium rubrum) across the western Mediterranean Sea revealed by microsatellites and nuclear sequences, Molecular Ecology, Volume 16 (2007) no. 24, pp. 5168-5182 | Article

[26] Costantini, F.; Rossi, S.; Pintus, E.; Cerrano, C.; Gili, J.-M.; Abbiati, M. Low connectivity and declining genetic variability along a depth gradient in Corallium rubrum populations, Coral Reefs, Volume 30 (2011) no. 4, pp. 991-1003 | Article

[27] Danecek, P.; Auton, A.; Abecasis, G.; Albers, C. A.; Banks, E.; DePristo, M. A.; Handsaker, R. E.; Lunter, G.; Marth, G. T.; Sherry, S. T.; McVean, G.; Durbin, R. The variant call format and VCFtools, Bioinformatics, Volume 27 (2011) no. 15, pp. 2156-2158 | Article

[28] Daub, J. T.; Hofer, T.; Cutivet, E.; Dupanloup, I.; Quintana-Murci, L.; Robinson-Rechavi, M.; Excoffier, L. Evidence for Polygenic Adaptation to Pathogens in the Human Genome, Molecular Biology and Evolution, Volume 30 (2013) no. 7, pp. 1544-1558 | Article

[29] DeWitt, T. J.; Sih, A.; Wilson, D. S. Costs and limits of phenotypic plasticity, Trends in Ecology & Evolution, Volume 13 (1998) no. 2, pp. 77-81 | Article

[30] Doney, S. C.; Ruckelshaus, M.; Emmett Duffy, J.; Barry, J. P.; Chan, F.; English, C. A.; Galindo, H. M.; Grebmeier, J. M.; Hollowed, A. B.; Knowlton, N.; Polovina, J.; Rabalais, N. N.; Sydeman, W. J.; Talley, L. D. Climate Change Impacts on Marine Ecosystems, Annual Review of Marine Science, Volume 4 (2011) no. 1, pp. 11-37 | Article

[31] Etter, P. D.; Bassham, S.; Hohenlohe, P. A.; Johnson, E. A.; Cresko, W. A. SNP Discovery and Genotyping for Evolutionary Genetics Using RAD Sequencing, Methods in Molecular Biology, Humana Press, Totowa, NJ, 2011, pp. 157-178 | Article

[32] Evanno, G.; Regnaut, S.; Goudet, J. Detecting the number of clusters of individuals using the software structure: a simulation study, Molecular Ecology, Volume 14 (2005) no. 8, pp. 2611-2620 | Article

[33] Excoffier, L.; Lischer, H. E. L. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows, Molecular Ecology Resources, Volume 10 (2010) no. 3, pp. 564-567 | Article

[34] Falush, D.; Stephens, M.; Pritchard, J. K. Inference of Population Structure Using Multilocus Genotype Data: Linked Loci and Correlated Allele Frequencies, Genetics, Volume 164 (2003) no. 4, pp. 1567-1587 | Article

[35] Falush, D.; Stephens, M.; Pritchard, J. K. Inference of population structure using multilocus genotype data: dominant markers and null alleles, Molecular Ecology Notes, Volume 7 (2007) no. 4, pp. 574-578 | Article

[36] Felsenstein, J. Genetic drift in clines which are maintained by migration and natural selection, Genetics, Volume 81 (1975) no. 1, pp. 191-207 | Article

[37] Gagnaire, P.-A.; Gaggiotti, O. E. Detecting polygenic selection in marine populations by combining population genomics and quantitative genetics approaches, Current Zoology, Volume 62 (2016) no. 6, pp. 603-616 | Article

[38] Ganot, P.; Fritz, M.; Rausch, T.; Aurelle, D.; Haguenauer, A.; Romans, P.; et al. , , 13th International Coral Reef Symposium, Honolulu, Hawaï, 2016

[39] Garrabou, J.; Perez, T.; Sartoretto, S.; Harmelin, J. Mass mortality event in red coral Corallium rubrum populations in the Provence region (France, NW Mediterranean), Marine Ecology Progress Series, Volume 217 (2001), pp. 263-272 | Article

[40] Guo, B.; Li, Z.; Merilä, J. Population genomic evidence for adaptive differentiation in the Baltic Sea herring, Molecular Ecology, Volume 25 (2016) no. 12, pp. 2833-2852 | Article

[41] Haguenauer, A.; Zuberer, F.; Ledoux, J.-B.; Aurelle, D. Adaptive abilities of the Mediterranean red coral Corallium rubrum in a heterogeneous and changing environment: from population to functional genetics, Journal of Experimental Marine Biology and Ecology, Volume 449 (2013), pp. 349-357 | Article

[42] Hastings, A.; Rohlf, F. J. Gene Flow: Effect in Stochastic Models of Differentiation, The American Naturalist, Volume 108 (1974) no. 963, pp. 701-705 | Article

[43] Hoban, S.; Kelley, J. L.; Lotterhos, K. E.; Antolin, M. F.; Bradburd, G.; Lowry, D. B.; Poss, M. L.; Reed, L. K.; Storfer, A.; Whitlock, M. C. Finding the Genomic Basis of Local Adaptation: Pitfalls, Practical Solutions, and Future Directions, The American Naturalist, Volume 188 (2016) no. 4, pp. 379-397 | Article

[44] Hofer, T.; Ray, N.; Wegmann, D.; Excoffier, L. Large Allele Frequency Differences between Human Continental Groups are more Likely to have Occurred by Drift During range Expansions than by Selection, Annals of Human Genetics, Volume 73 (2009) no. 1, pp. 95-108 | Article

[45] Hohenlohe, P. A.; Bassham, S.; Etter, P. D.; Stiffler, N.; Johnson, E. A.; Cresko, W. A. Population Genomics of Parallel Adaptation in Threespine Stickleback using Sequenced RAD Tags, PLoS Genetics, Volume 6 (2010) no. 2 | Article

[46] Hubisz, M. J.; Falush, D.; Stephens, M.; Pritchard, J. K. Inferring weak population structure with the assistance of sample group information, Molecular Ecology Resources, Volume 9 (2009) no. 5, pp. 1322-1332 | Article

[47] Jin, Y. K.; Lundgren, P.; Lutz, A.; Raina, J.-B.; Howells, E. J.; Paley, A. S.; Willis, B. L.; van Oppen, M. J. H. Genetic markers for antioxidant capacity in a reef-building coral, Science Advances, Volume 2 (2016) no. 5 | Article

[48] Jombart, T. adegenet: a R package for the multivariate analysis of genetic markers, Bioinformatics, Volume 24 (2008) no. 11, pp. 1403-1405 | Article

[49] Jones, F. C.; Grabherr, M. G.; Chan, Y. F.; Russell, P.; Mauceli, E.; Johnson, J.; Swofford, R.; Pirun, M.; Zody, M. C.; White, S.; Birney, E.; Searle, S.; Schmutz, J.; Grimwood, J.; Dickson, M. C.; Myers, R. M.; Miller, C. T.; Summers, B. R.; Knecht, A. K.; Brady, S. D.; Zhang, H.; Pollen, A. A.; Howes, T.; Amemiya, C.; Lander, E. S.; Di Palma, F.; Lindblad-Toh, K.; Kingsley, D. M. The genomic basis of adaptive evolution in threespine sticklebacks, Nature, Volume 484 (2012) no. 7392, pp. 55-61 | Article

[50] Kawecki, T. J.; Ebert, D. Conceptual issues in local adaptation, Ecology Letters, Volume 7 (2004) no. 12, pp. 1225-1241 | Article

[51] Kersting, D. K.; Bensoussan, N.; Linares, C. Long-Term Responses of the Endemic Reef-Builder Cladocora caespitosa to Mediterranean Warming, PLoS ONE, Volume 8 (2013) no. 8 | Article

[52] Knittweis, L.; Aguilar, R.; Alvarez, H.; Borg, J. A.; Evans, J.; Garcia, S.; Schembri, P. J., Rapport du Congrès de la Commission Internationale pour l'Exploration Scientifique de la Mer Méditerranée, 41. https://www.um.edu.mt/library/oar/handle/123456789/18340, 2016

[53] Kopelman, N. M.; Mayzel, J.; Jakobsson, M.; Rosenberg, N. A.; Mayrose, I. Clumpak : a program for identifying clustering modes and packaging population structure inferences across K, Molecular Ecology Resources, Volume 15 (2015) no. 5, pp. 1179-1191 | Article

[54] Kulmuni, J.; Westram, A. M. Intrinsic incompatibilities evolving as a by-product of divergent ecological selection: Considering them in empirical studies on divergence with gene flow, Molecular Ecology, Volume 26 (2017) no. 12, pp. 3093-3103 | Article

[55] Ledoux, J.-B.; Aurelle, D.; Bensoussan, N.; Marschal, C.; Féral, J.-P.; Garrabou, J. Potential for adaptive evolution at species range margins: contrasting interactions between red coral populations and their environment in a changing ocean, Ecology and Evolution, Volume 5 (2014) no. 6, pp. 1178-1192 | Article

[56] Ledoux, J.-B.; Aurelle, D.; Féral, J.-P.; Garrabou, J. Molecular forensics in the precious Mediterranean red coral, Corallium rubrum: testing DNA extraction and microsatellite genotyping using dried colonies, Conservation Genetics Resources, Volume 5 (2013) no. 2, pp. 327-330 | Article

[57] Ledoux, J.-B.; Garrabou, J.; Bianchimani, O.; Drap, P.; Féral, J.-P.; Aurelle, D. Fine-scale genetic structure and inferences on population biology in the threatened Mediterranean red coral, Corallium rubrum, Molecular Ecology, Volume 19 (2010) no. 19, pp. 4204-4216 | Article

[58] Ledoux, J.-B.; Mokhtar-Jamaï, K.; Roby, C.; Féral, J.-P.; Garrabou, J.; Aurelle, D. 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, Molecular Ecology, Volume 19 (2010) no. 4, pp. 675-690 | Article

[59] Lenormand, T. Gene flow and the limits to natural selection, Trends in Ecology & Evolution, Volume 17 (2002) no. 4, pp. 183-189 | Article

[60] Li, H.; Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform, Bioinformatics, Volume 25 (2009) no. 14, pp. 1754-1760 | Article

[61] Limborg, M. T.; Helyar, S. J.; De Bruyn, M.; Taylor, M. I.; Nielsen, E. E.; Ogden, R.; Carvalho, G. R.; Bekkevold, D. Environmental selection on transcriptome-derived SNPs in a high gene flow marine fish, the Atlantic herring (Clupea harengus), Molecular Ecology, Volume 21 (2012) no. 15, pp. 3686-3703 | Article

[62] Lõhelaid, H.; Teder, T.; Samel, N. Lipoxygenase-allene oxide synthase pathway in octocoral thermal stress response, Coral Reefs, Volume 34 (2015) no. 1, pp. 143-154 | Article

[63] Lowry, D. B.; Hoban, S.; Kelley, J. L.; Lotterhos, K. E.; Reed, L. K.; Antolin, M. F.; Storfer, A. Breaking RAD: an evaluation of the utility of restriction site‐associated DNA sequencing for genome scans of adaptation, Molecular Ecology Resources, Volume 17 (2017) no. 2, pp. 142-152 | Article

[64] Lundgren, P.; Vera, J. C.; Peplow, L.; Manel, S.; van Oppen, M. J. Genotype – environment correlations in corals from the Great Barrier Reef, BMC Genetics, Volume 14 (2013) no. 1 | Article

[65] Luu, K.; Bazin, E.; Blum, M. G. B. pcadapt: anRpackage to perform genome scans for selection based on principal component analysis, Molecular Ecology Resources, Volume 17 (2017) no. 1, pp. 67-77 | Article

[66] Manel, S.; Perrier, C.; Pratlong, M.; Abi-Rached, L.; Paganini, J.; Pontarotti, P.; Aurelle, D. Genomic resources and their influence on the detection of the signal of positive selection in genome scans, Molecular Ecology, Volume 25 (2016) no. 1, pp. 170-184 | Article

[67] Marschal, C.; Garrabou, J.; Harmelin, J. G.; Pichon, M. A new method for measuring growth and age in the precious red coral Corallium rubrum (L.), Coral Reefs, Volume 23 (2004) no. 3, pp. 423-432 | Article

[68] Martínez-Quintana, A.; Bramanti, L.; Viladrich, N.; Rossi, S.; Guizien, K. Quantification of larval traits driving connectivity: the case of Corallium rubrum (L. 1758), Marine Biology, Volume 162 (2015) no. 2, pp. 309-318 | Article

[69] McKinney, G. J.; Larson, W. A.; Seeb, L. W.; Seeb, J. E. RADseq provides unprecedented insights into molecular ecology and evolutionary genetics: comment on Breaking RAD by Lowry et al . (2016), Molecular Ecology Resources, Volume 17 (2017) no. 3, pp. 356-361 | Article

[70] Milano, I.; Babbucci, M.; Cariani, A.; Atanassova, M.; Bekkevold, D.; Carvalho, G. R.; Espiñeira, M.; Fiorentino, F.; Garofalo, G.; Geffen, A. J.; Hansen, J. H.; Helyar, S. J.; Nielsen, E. E.; Ogden, R.; Patarnello, T.; Stagioni, M.; Tinti, F.; Bargelloni, L. Outlier SNP markers reveal fine-scale genetic structuring across European hake populations (Merluccius merluccius), Molecular Ecology, Volume 23 (2014) no. 1, pp. 118-135 | Article

[71] Mumby, P. J.; Elliott, I. A.; Eakin, C. M.; Skirving, W.; Paris, C. B.; Edwards, H. J.; Enríquez, S.; Iglesias-Prieto, R.; Cherubin, L. M.; Stevens, J. R. Reserve design for uncertain responses of coral reefs to climate change, Ecology Letters, Volume 14 (2011) no. 2, pp. 132-140 | Article

[72] Nagylaki, T. Random genetic drift in a cline, Proceedings of the National Academy of Sciences, Volume 75 (1978) no. 1, pp. 423-426 | Article

[73] Orsini, L.; Vanoverbeke, J.; Swillen, I.; Mergeay, J.; De Meester, L. Drivers of population genetic differentiation in the wild: isolation by dispersal limitation, isolation by adaptation and isolation by colonization, Molecular Ecology, Volume 22 (2013) no. 24, pp. 5983-5999 | Article

[74] Palumbi, S. R.; Barshis, D. J.; Traylor-Knowles, N.; Bay, R. A. Mechanisms of reef coral resistance to future climate change, Science, Volume 344 (2014) no. 6186, pp. 895-898 | Article

[75] Pante, E.; Puillandre, N.; Viricel, A.; Arnaud-Haond, S.; Aurelle, D.; Castelin, M.; Chenuil, A.; Destombe, C.; Forcioli, D.; Valero, M.; Viard, F.; Samadi, S. Species are hypotheses: avoid connectivity assessments based on pillars of sand, Molecular Ecology, Volume 24 (2015) no. 3, pp. 525-544 | Article

[76] Pigliucci, M. Phenotypic plasticity: beyond nature and nurture, JHU Press, 2001

[77] Pivotto, I. D.; Nerini, D.; Masmoudi, M.; Kara, H.; Chaoui, L.; Aurelle, D. Highly contrasted responses of Mediterranean octocorals to climate change along a depth gradient, Royal Society Open Science, Volume 2 (2015) no. 5 | Article

[78] Plough, L. V.; Shin, G.; Hedgecock, D. Genetic inviability is a major driver of type III survivorship in experimental families of a highly fecund marine bivalve, Molecular Ecology, Volume 25 (2016) no. 4, pp. 895-910 | Article

[79] Plummer, M.; Best, N.; Cowles, K.; Vines, K. CODA: Convergence diagnosis and output analysis for MCMC, R news, Volume 6 (2006) | Article

[80] Prada, C.; Schizas, N. V.; Yoshioka, P. M. Phenotypic plasticity or speciation? A case from a clonal marine organism, BMC Evolutionary Biology, Volume 8 (2008) no. 1 | Article

[81] Pratlong, M.; Haguenauer, A.; Chabrol, O.; Klopp, C.; Pontarotti, P.; Aurelle, D. The red coral (Corallium rubrum) transcriptome: a new resource for population genetics and local adaptation studies, Molecular Ecology Resources, Volume 15 (2015) no. 5, pp. 1205-1215 | Article

[82] Pratlong, M.; Haguenauer, A.; Chenesseau, S.; Brener, K.; Mitta, G.; Toulza, E.; Bonabaud, M.; Rialle, S.; Aurelle, D.; Pontarotti, P. Evidence for a genetic sex determination in Cnidaria, the Mediterranean red coral ( Corallium rubrum ), Royal Society Open Science, Volume 4 (2017) no. 3 | Article

[83] Pritchard, J. K.; Di Rienzo, A. Adaptation – not by sweeps alone, Nature Reviews Genetics, Volume 11 (2010) no. 10, pp. 665-667 | Article

[84] Pritchard, J. K.; Stephens, M.; Donnelly, P. Inference of Population Structure Using Multilocus Genotype Data, Genetics, Volume 155 (2000) no. 2, pp. 945-959 | Article

[85] Putnam, H. M.; Gates, R. D. Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions, Journal of Experimental Biology, Volume 218 (2015) no. 15, pp. 2365-2372 | Article

[86] R Core Team, R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria., 2015

[87] Rossi, S.; Tsounis, G.; Orejas, C.; Padrón, T.; Gili, J.-M.; Bramanti, L.; Teixidó, N.; Gutt, J. Survey of deep-dwelling red coral (Corallium rubrum) populations at Cap de Creus (NW Mediterranean), Marine Biology, Volume 154 (2008) no. 3, pp. 533-545 | Article

[88] Rousset, F. genepop’007: a complete re-implementation of the genepop software for Windows and Linux, Molecular Ecology Resources, Volume 8 (2008) no. 1, pp. 103-106 | Article

[89] Sambrook, J.; Fritsch, E.; Maniatis, T. Molecular cloning, Cold spring harbor laboratory press, New York, 1989

[90] Sanford, E.; Kelly, M. W. Local Adaptation in Marine Invertebrates, Annual Review of Marine Science, Volume 3 (2010) no. 1, pp. 509-535 | Article

[91] Santangelo, G.; Bramanti, L.; Rossi, S.; Tsounis, G.; Vielmini, I.; Lott, C.; Gili, J. Patterns of variation in recruitment and post-recruitment processes of the Mediterranean precious gorgonian coral Corallium rubrum, Journal of Experimental Marine Biology and Ecology, Volume 411 (2012), pp. 7-13 | Article

[92] Sherman, C. D. H.; Ayre, D. J. Fine-scale adaptation in a clonal sea anemone, Evolution, Volume 62 (2008) no. 6, pp. 1373-1380 | Article

[93] Slatkin, M.; Maruyama, T. Genetic drift in a cline, Genetics, Volume 81 (1975) no. 1, pp. 209-222 | Article

[94] Smith, L. W.; Barshis, D.; Birkeland, C. Phenotypic plasticity for skeletal growth, density and calcification of Porites lobata in response to habitat type, Coral Reefs, Volume 26 (2007) no. 3, pp. 559-567 | Article

[95] Szulkin, M.; Gagnaire, P.-A.; Bierne, N.; Charmantier, A. Population genomic footprints of fine-scale differentiation between habitats in Mediterranean blue tits, Molecular Ecology, Volume 25 (2016) no. 2, pp. 542-558 | Article

[96] Torrents, O.; Tambutté, E.; Caminiti, N.; Garrabou, J. Upper thermal thresholds of shallow vs. deep populations of the precious Mediterranean red coral Corallium rubrum (L.): Assessing the potential effects of warming in the NW Mediterranean, Journal of Experimental Marine Biology and Ecology, Volume 357 (2008) no. 1, pp. 7-19 | Article

[97] Ulstrup, K. E.; Van Oppen, M. J. H. Geographic and habitat partitioning of genetically distinct zooxanthellae ( Symbiodinium ) in Acropora corals on the Great Barrier Reef, Molecular Ecology, Volume 12 (2003) no. 12, pp. 3477-3484 | Article

[98] de Villemereuil, P.; Gaggiotti, O. E. A new F ST ‐based method to uncover local adaptation using environmental variables, Methods in Ecology and Evolution, Volume 6 (2015) no. 11, pp. 1248-1258 | Article

[99] Wang, L.; Liu, S.; Zhuang, Z.; Guo, L.; Meng, Z.; Lin, H. Population Genetic Studies Revealed Local Adaptation in a High Gene-Flow Marine Fish, the Small Yellow Croaker (Larimichthys polyactis), PLoS ONE, Volume 8 (2013) no. 12 | Article

[100] Weinberg, S. The Light-Dependent Behaviour of Planula Larvae of Eunicella Singularis and Corallium Rubrum and its Implication for Octocorallian Ecology, Bijdragen tot de Dierkunde, Volume 49 (1979) no. 1, pp. 16-30 | Article

[101] Wrange, A.-L.; André, C.; Lundh, T.; Lind, U.; Blomberg, A.; Jonsson, P. J.; Havenhand, J. N. Importance of plasticity and local adaptation for coping with changing salinity in coastal areas: a test case with barnacles in the Baltic Sea, BMC Evolutionary Biology, Volume 14 (2014) no. 1 | Article

[102] Ziegler, M.; Roder, C. M.; Büchel, C.; Voolstra, C. R. Limits to physiological plasticity of the coral Pocillopora verrucosa from the central Red Sea, Coral Reefs, Volume 33 (2014) no. 4, pp. 1115-1129 | Article

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