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Genetic insights into recolonization processes of Mediterranean octocorals

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Abstract

Marine ecosystems are strongly impacted by the consequences of human activities, such as habitat destruction or artificialization and climate change. In the Mediterranean Sea, sessile benthic species, and particularly octocorals, have been affected by mass mortality events linked with positive thermal anomalies. The future survival of octocoral populations impacted by global change will depend on their recolonization abilities facing local extirpation or important modification of their habitat. We studied these processes in Mediterranean octocorals in two situations: the colonization of artificial substrates (wrecks) by the red gorgonian Paramuricea clavata, and the recolonization following mortality events in the yellow gorgonian Eunicella cavolini. With microsatellite markers (seven for P. clavata, five for E. cavolini), we analyzed the genetic diversity of populations on artificial substrates and their differentiation from other neighboring populations. For P. clavata the populations on artificial substrates were not or lowly differentiated from the closest populations (1.3–1.6 km) on natural substrates, and showed similar levels of genetic diversity. Artificial substrates can then be considered as an interesting substitute for natural substrates for this species. For E. cavolini we did not detect any variation in diversity or relatedness following recuperation after mortality events. In both cases, our results suggest the input from different populations in the recolonization process, which helps in maintaining the genetic diversity. These results are useful for the management of these species and of associated ecosystems.

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All genotypes have been deposited in the Zenodo database under reference: https://doi.org/10.5281/zenodo.3724056

References

  • Allendorf FW (1986) Genetic drift and the loss of alleles versus heterozygosity. Zoo Biol 5:181–190

    Article  Google Scholar 

  • Allendorf FW, Luikart GH, Atken SN (2017) Conservation and the genetics of populations, 2nd edn. John Wiley & Sons, Hoboken

    Google Scholar 

  • Arizmendi-Mejía R, Linares C, Garrabou J, Antunes A, Ballesteros E, Cebrian E, Díaz D, Ledoux J-B (2015) Combining genetic and demographic data for the conservation of a Mediterranean marine habitat-forming species. PLoS One 10:e0119585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Austerlitz F, Mariette S, Machon N, Gouyon P-H, Godelle B (2000) Effects of colonization processes on genetic diversity: differences between annual plants and tree species. Genetics 154:1309–1321

    CAS  PubMed  PubMed Central  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier, France

  • Bell G, Collins S (2008) Adaptation, extinction and global change. Evol Appl 1:3–16

    Article  PubMed  PubMed Central  Google Scholar 

  • Benestan L, Gosselin T, Perrier C, Sainte-Marie B, Rochette R, Bernatchez L (2015) RAD genotyping reveals fine-scale genetic structuring and provides powerful population assignment in a widely distributed marine species, the American lobster (Homarus americanus). Mol Ecol 24:3299–3315

    Article  PubMed  Google Scholar 

  • Boudouresque C-F, Blanfuné A, Fernandez C, Lejeusne C, Pérez T, Ruitton S, Thibault D, Thibaut T, Verlaque M (2017) Marine biodiversity-warming vs. biological invasions and overfishing in the Mediterranean Sea: take care, ‘One Train can hide another’. MOJ Ecol Environ Sci 2:1–13

    Google Scholar 

  • Cánovas-Molina A, Montefalcone M, Bavestrello G, Masmoudi MB, Haguenauer A, Hammami P, Chaoui L, Kara MH, Aurelle D (2018) From depth to regional spatial genetic differentiation of Eunicella cavolini in the NW Mediterranean. C R Biol 341:421–432

    Article  PubMed  Google Scholar 

  • Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    Article  CAS  PubMed  Google Scholar 

  • Cigliano M, Gambi MC (2007) The long hot summer: a further mortality event of Gorgonians along the Phlaegrean islands (Tyrrhenian Sea). Biol Mar Med 14:292–293

    Google Scholar 

  • Coll M, Piroddi C, Steenbeek J, Kaschner K, Lasram FBR, Aguzzi J, Ballesteros E, Bianchi CN, Corbera J, Dailianis T (2010) The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS One 5:e11842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coll M, Piroddi C, Albouy C, Ben Rais Lasram F, Cheung WW, Christensen V, Karpouzi VS, Guilhaumon F, Mouillot D, Paleczny M (2012) The Mediterranean Sea under siege: spatial overlap between marine biodiversity, cumulative threats and marine reserves. Glob Ecol Biogeogr 21:465–480

    Article  Google Scholar 

  • Colson I, Hughes RN (2004) Rapid recovery of genetic diversity of dogwhelk (Nucella lapillus L.) populations after local extinction and recolonization contradicts predictions from life history characteristics. Mol Ecol 13:2223–2233

    Article  CAS  PubMed  Google Scholar 

  • Coma R, Ribesl RM, Zabala M, Gilil J-M (1995) Reproduction and cycle of gonadal development in the Mediterranean gorgonian Paramuriceaclavata. Mar Ecol Prog Ser 117:173–183

    Article  Google Scholar 

  • Costantini F, Fauvelot C, Abbiati M (2007) Fine-scale genetic structuring in Corallium rubrum: evidence of inbreeding and limited effective larval dispersal. Mar Ecol Prog Ser 340:109–119

    Article  CAS  Google Scholar 

  • Cramer W, Guiot J, Fader M, Garrabou J, Gattuso J-P, Iglesias A, Lange MA, Lionello P, Llasat MC, Paz S (2018) Climate change and interconnected risks to sustainable development in the Mediterranean. Nat Clim Change 8(11):972–980

    Article  Google Scholar 

  • Cupido R, Cocito S, Manno V, Ferrando S, Peirano A, Iannelli M, Bramanti L, Santangelo G (2012) Sexual structure of a highly reproductive, recovering gorgonian population: quantifying reproductive output. Mar Ecol Prog Ser 469:25–36

    Article  Google Scholar 

  • D’Aloia CC, Bogdanowicz SM, Francis RK, Majoris JE, Harrison RG, Buston PM (2015) Patterns, causes, and consequences of marine larval dispersal. Proc Natl Acad Sci USA 112:13940–13945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dafforn KA, Glasby TM, Airoldi L, Rivero NK, Mayer-Pinto M, Johnston EL (2015) Marine urbanization: an ecological framework for designing multifunctional artificial structures. Front Ecol Environ 13:82–90

    Article  Google Scholar 

  • Fauvelot C, Bertozzi F, Costantini F, Airoldi L, Abbiati M (2009) Lower genetic diversity in the limpet Patella caerulea on urban coastal structures compared to natural rocky habitats. Mar Biol 156:2313–2323

    Article  Google Scholar 

  • Foll M, Gaggiotti O (2006) Identifying the environmental factors that determine the genetic structure of populations. Genetics 174:875–891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Francis RM (2017) pophelper: an R package and web app to analyse and visualize population structure. Mol Ecol Res 17:27–32

    Article  CAS  Google Scholar 

  • Gaggiotti OE, Foll M (2010) Quantifying population structure using the F-model. Mol Ecol Res 10:821–830

    Article  Google Scholar 

  • Gambi M (2014) L’isola d’Ischia: un osservatorio speciale per lo studio del cambiamento climatico globale a mare. In: Greco P (ed) Ischia Patrimonio dell’Umanità Natura e cultura. Doppiavoce Editore, Napoli, pp 71–97

    Google Scholar 

  • Gambi M, Barbieri F (2012) Population structure of the gorgonian Eunicella cavolinii in the “Grotta Azzurra” cave off Palinuro, after the mass mortality event in 2008. Biol Mar Mediterr 19:174

    Google Scholar 

  • Gambi M, Cigliano M, Iacono B (2006) Segnalazione di un evento di mortalità di gorgonacei lungo le coste delle isole di Ischia e Procida (Golfo di Napoli, Mar Tirreno). Biol Mar Mediterr 13:583–587

    Google Scholar 

  • Gambi M, Barbieri F, Signorelli S, Saggiomo V (2010) Mortality events along the Campania coast (Tyrrhenian Sea) in summers 2008 and 2009 and relation to thermal conditions. Biol Mar Mediterr 17:126

    Google Scholar 

  • Garrabou J, Coma R, Bensoussan N, Bally M, Chevaldonné P, Cigliano M, Diaz D, Harmelin JG, Gambi MC, Kersting DK, Ledoux J-B, Lejeusne C, Linares C, Marschal C, Pérez T, Ribes M, Romano JC, Serrano E, Teixido N, Torrents O, Zabala M, Zuberer F, Cerrano C (2009) Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob Change Biol 15:1090–1103

    Article  Google Scholar 

  • Gattuso J-P, Magnan AK, Bopp L, Cheung WW, Duarte CM, Hinkel J, Mcleod E, Micheli F, Oschlies A, Williamson P (2018) Ocean solutions to address climate change and its effects on marine ecosystems. Front Mar Sci 5:337

    Article  Google Scholar 

  • Glover KA, Hansen MM, Lien S, Als TD, Høyheim B, Skaala Ø (2010) A comparison of SNP and STR loci for delineating population structure and performing individual genetic assignment. BMC Genet 11:2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haguenauer A, Zuberer F, Ledoux J-B, Aurelle D (2013) Adaptive abilities of the Mediterranean red coral Corallium rubrum in a heterogeneous and changing environment: from population to functional genetics. J Exp Mar Bio Ecol 449:349–357

    Article  Google Scholar 

  • Hughes TP, Kerry JT, Baird AH, Connolly SR, Chase TJ, Dietzel A, Hill T, Hoey AS, Hoogenboom MO, Jacobson M (2019) Global warming impairs stock–recruitment dynamics of corals. Nature 568:387

    Article  CAS  PubMed  Google Scholar 

  • Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    Article  CAS  PubMed  Google Scholar 

  • Kamvar ZN, Tabima JF, Grünwald NJ (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281

    Article  PubMed  PubMed Central  Google Scholar 

  • Kamvar ZN, Brooks JC, Grünwald NJ (2015) Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Front Genet 6:208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ledoux J, 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 19:4204–4216

    Article  PubMed  Google Scholar 

  • 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 19:675–690

    Article  CAS  PubMed  Google Scholar 

  • 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 5:1178–1192

    Article  PubMed  PubMed Central  Google Scholar 

  • Ledoux J, Frleta-Valić M, Kipson S, Antunes A, Cebrian E, Linares C, Sánchez P, Leblois R, Garrabou J (2018) Postglacial range expansion shaped the spatial genetic structure in a marine habitat-forming species: implications for conservation plans in the Eastern Adriatic Sea. J Biogeogr 45:2645–2657

    Article  Google Scholar 

  • Linares C, Doak DF, Coma R, Diaz D, Zabala M (2007) Life history and viability of a long-lived marine invertebrate: the octocoral Paramuricea clavata. Ecology 88:918–928

    Article  PubMed  Google Scholar 

  • Linares C, Coma R, Mariani S, Díaz D, Hereu B, Zabala M (2008) Early life history of the Mediterranean gorgonian Paramuricea clavata: implications for population dynamics. Invertebr Biol 127:1–11

    Article  Google Scholar 

  • Lippé C, Dumont P, Bernatchez L (2006) High genetic diversity and no inbreeding in the endangered copper redhorse, Moxostoma hubbsi (Catostomidae, Pisces): the positive sides of a long generation time. Mol Ecol 15:1769–1780

    Article  CAS  PubMed  Google Scholar 

  • Manel S, Perrier C, Pratlong M, Abi-Rached L, Paganini J, Pontarotti P, Aurelle D (2016) Genomic resources and their influence on the detection of the signal of positive selection in genome scans. Mol Ecol 25:170–184

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Quintana A, Bramanti L, Viladrich N, Rossi S, Guizien K (2015) Quantification of larval traits driving connectivity: the case of Corallium rubrum (L. 1758). Mar Biol 162:309–318

    Article  Google Scholar 

  • Masmoudi MB, Chaoui L, Topçu NE, Hammami P, Kara MH, Aurelle D (2016) Contrasted levels of genetic diversity in a benthic Mediterranean octocoral: consequences of different demographic histories? Ecol Evol 6:8665–8678

    Article  PubMed  PubMed Central  Google Scholar 

  • Mokhtar-Jamai K, Pascual M, Ledoux J-B, Coma R, Féral J-P, Garrabou J, Aurelle D (2011) From global to local genetic structuring in the red gorgonian Paramuricea clavata: the interplay between oceanographic conditions and limited larval dispersal. Mol Ecol 20:3291–3305

    Article  CAS  PubMed  Google Scholar 

  • Molecular Ecology Resources Primer Development Consortium, Aurelle D, Baker AJ, Bottin L, Brouat C, Caccone A, Chaix A, Dhakal P, Ding Y, Duplantier JM, Fiedler W, Fietz J, Fong Y, Forcioli D, Freitas TRO, Gunnarson GH, Haddrath O, Hadziabdic D, Hauksdottir S, Havill NP, Heinrich M, Heinz T, Hjorleifsdottir S, Hong Y, Hreggvidsson GO, Huchette S, Hurst J, Kane M, Kane NC, Kawakamit T, Ke W, Keith RA, Klauke N, Klein JL, Kun JFJ, Li C, Li G-Q, Li J-J, Loiseau A, Lu L-Z, Lucas M, Martins-Ferreira C, Mokhtar-Jamaï K, Olafsson K, Pampoulie C, Pan L, Pooler MR, Ren J-D, Rinehart TA, Roussel V, Santos MO, Schaefer HM, Scheffler BE, Schmidt A, Segelbacher G, Shen J-D, Skirnisdottir S, Sommer S, Tao Z-R, Taubert R, Tian Y, Tomiuk J, Trigiano RN, Ungerer MC, Van Wormhoudt A, Wadl PA, Wang D-Q, Weis-Dootz T, Xia Q, Yuan Q-Y (2010) Permanent genetic resources added to the molecular ecology resources database 1 February 2010–31 March 2010. Mol Ecol Res 10:751–754

    Article  Google Scholar 

  • Ordóñez V, Pascual M, Rius M, Turon X (2013) Mixed but not admixed: a spatial analysis of genetic variation of an invasive ascidian on natural and artificial substrates. Mar Biol 160:1645–1660

    Article  Google Scholar 

  • Orsini L, Vanoverbeke J, Swillen I, Mergeay J, Meester L (2013) Drivers of population genetic differentiation in the wild: isolation by dispersal limitation, isolation by adaptation and isolation by colonization. Mol Ecol 22:5983–5999

    Article  PubMed  Google Scholar 

  • Otto SP (2018) Adaptation, speciation and extinction in the Anthropocene. Proc R Soc Lond B Biol Sci 285:20182047

    Article  Google Scholar 

  • Padrón M, Costantini F, Bramanti L, Guizien K, Abbiati M (2018) Genetic connectivity supports recovery of gorgonian populations affected by climate change. Aquat Conserv 28:776–787

    Article  Google Scholar 

  • Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Portela R, Cerro-Gálvez E, Taboada S, Tidu C, Campillo-Campbell C, Mora J, Riesgo A (2016) Lonely populations in the deep: genetic structure of red gorgonians at the heads of submarine canyons in the north-western Mediterranean Sea. Coral Reefs 35:1013–1026

    Article  Google Scholar 

  • Pilczynska J, Cocito S, Boavida J, Serrão E, Queiroga H (2016) Genetic diversity and local connectivity in the Mediterranean red gorgonian coral after mass mortality events. PLoS One 11:e0150590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pilczynska J, Cocito S, Boavida J, Serrão EA, Assis J, Fragkopoulou E, Queiroga H (2019) Genetic diversity increases with depth in red gorgonian populations of the Mediterranean Sea and the Atlantic Ocean. PeerJ 7:e6794

    Article  PubMed  PubMed Central  Google Scholar 

  • Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    Article  CAS  PubMed  Google Scholar 

  • Pivotto I, Nerini D, Masmoudi M, Kara H, Chaoui L, Aurelle D (2015) Highly contrasted responses of Mediterranean octocorals to climate change along a depth gradient. R Soc Open Sci 2:140493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pratlong M, Haguenauer A, Brener K, Mitta G, Toulza E, Garrabou J, Bensoussan N, Pontarotti P, Aurelle D (2018) Separate the wheat from the chaff: genomic analysis of local adaptation in the red coral Corallium rubrum. bioRxiv, 306456, ver. 3 peer-reviewed and recommended by PCI Evol Biol

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 64:9197–9201

    Article  Google Scholar 

  • Ribout C, Carpentieri C (2013) Automated genomic DNA purification of marine organisms on the epMotion® 5075 VAC from Eppendorf. Eppendorf Appl Note 281:1–6

    Google Scholar 

  • Ronce O (2007) How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annu Rev Ecol Evol Syst 38:231–253

    Article  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Res 8:103–106

    Article  Google Scholar 

  • Shorthouse DP (2010) SimpleMappr, an online tool to produce publication-quality point maps. https://www.simplemappr.net. Accessed 06 Apr 2020

  • Starger C, Barber P, Baker A (2010) The recovery of coral genetic diversity in the Sunda Strait following the 1883 eruption of Krakatau. Coral Reefs 29:547–565

    Article  Google Scholar 

  • Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24:2498–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Underwood JN, Smith LD, Van Oppen MJH, Gilmour JP (2007) Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching. Mol Ecol 16:771–784

    Article  CAS  PubMed  Google Scholar 

  • Verdura J, Linares C, Ballesteros E, Coma R, Uriz MJ, Bensoussan N, Cebrian E (2019) Biodiversity loss in a Mediterranean ecosystem due to an extreme warming event unveils the role of an engineering gorgonian species. Sci Rep 9:5911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J (2002) An estimator for pairwise relatedness using molecular markers. Genetics 160:1203–1215

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J (2011) COANCESTRY: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol Ecol Res 11:141–145

    Article  Google Scholar 

  • Weinberg S (1979) The light-dependent behaviour of planula larvae of Eunicella singularis and Corallium rubrum and its implication for octocorallian ecology. Bijdragen tot de Dierkunde 49:16–30

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    CAS  PubMed  Google Scholar 

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Acknowledgements

The E. cavolini samples have been obtained thanks to an ASSEMBLE TA project granted to D. Aurelle (grant agreement n° 227799), for an access to the Stazione Zoologica Anton Dohrn in Naples. We thank Mr Fabio Barbieri, at the “Gambieri Marine Field Station”, and the staff of the Palinuro Sub Diving Center (Palinuro), the Ischia Diving Agency and the ANS diving (Ischia), and the Alta Marea diving Center (Ustica) for support in collection of E. cavolini samples at Palinuro, Ischia and Ustica, respectively; Mr Marco Cannavacciuolo and the staff of the MEDA Unit (RIMAR Dept Stazione Zoologica of Naples) for sampling colonies at the Nisida island (Naples). The work of M. Masmoudi in France was supported by the Algerian—French collaboration program Tassili n° 12MDU853. This study has been funded by the French National Research Agency (ANR) program Adacni (ANR n° ANR‐12‐ADAP‐0016; https://adacni.imbe.fr). The project leading to this publication has received funding from European FEDER Fund under project 1166-–39417. J.-B. Ledoux is funded by an assistant researcher contract framework of the RD Unit—UID/Multi/04423/2019—Interdisciplinary Centre of Marine and Environmental Research—financed by the European Regional Development Fund (ERDF) through COMPETE2020—Operational Program for Competitiveness and Internationalisation (POCI) and national funds through FCT/MCTES (PIDDAC). We thank Oscar Puebla and two anonymous reviewers who helped us improve this article.

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Aurelle, D., Tariel, J., Zuberer, F. et al. Genetic insights into recolonization processes of Mediterranean octocorals. Mar Biol 167, 73 (2020). https://doi.org/10.1007/s00227-020-03684-z

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