Abstract
Context
Spatially heterogeneous oceanographic properties such as currents, waves, and biogeochemical gradients control the movement of gametes and larvae of marine species. However, it is poorly understood how such spatial dynamics may shape the genetic connectivity, diversity, and structure of marine populations.
Objectives
We applied a seascape genetics framework to evaluate the relationships between marine environmental factors and gene flow among populations of the endangered Mediterranean pillow coral (Cladocora caespitosa).
Methods
We modelled gene flow among locations in the Adriatic and northern Ionian Seas as a function of sea surface temperature, salinity, currents and geographic distance. Isolation by distance and isolation by resistance hypotheses were then compared using model optimization in a generalized linear mixed effects modelling framework.
Results
Overall genetic differentiation among locations was relatively low (FST = 0.028). We identified two genetic groups, with the northernmost location segregating from the rest of the locations, although some admixture was evident. Almost 25% of the individuals analysed were identified as putative migrants and a potential barrier to gene flow was identified between the northern and central-southern basins. The best gene flow models predicted that genetic connectivity in this species is primarily driven by the movement along the coastlines and sea surface currents.
Conclusions
A high percentage of self-recruitment and relatively low migration rates has been detected in the studied populations of C. caespitosa. Its fragmented distribution along the coast can be predicted by stepping-stone oceanographic transport by coastal currents among suitable habitat patches.
Similar content being viewed by others
References
Ahrens CW, Rymer PD, Stow A, Bragg J, Dillon S, Umbers KDL, Dudaniec RY (2018) The search for loci under selection: trends, biases and progress. Mol Ecol 27:1342–1356. https://doi.org/10.1111/mec.14549
Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Proceedings 2nd international symposium on information theory, Budapest, pp 267–281
Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst—outlier method. BMC Bioinformatics 9:323. https://doi.org/10.1186/1471-2105-9-323
Ayre DJ, Hughes TP (2000) Genotypic diversity and gene flow in brooding and spawning corals along the great barrier reef, Australia. Evolution 54:1590–1605
Balkenhol N, Cushman SA, Storfer AT, Waits LP (2015) Introduction to landscape genetics—concepts, methods, applications. In: Balkenhol N, Cushman SA, Storfer AT, Waits LP (eds) Landscape genetics: concepts, methods, applications. Wiley, UK, pp 1–7
Balkenhol N, Waits LP, Dezzani RJ (2009) Statistical approaches in landscape genetics: an evaluation of methods for linking landscape and genetic data. Ecography 32:818–830. https://doi.org/10.1111/j.1600-0587.2009.05807.x
Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome Populations Interactions CNRS UMR5 117: 5000
Bellan-Santini D, Bellan G, Bitar G, Harmelin J-G, Pergent G (2002) Handbook for interpreting types of marine habitat for the selection of sites to be included in the national inventories of natural sites of conservation interest. UNEP-MAP RAC/SPA, Tunis, p 168
Boero F, Foglini F, Fraschetti S, Goriup P, Macpherson E, Planes S et al (2016) CoCoNet: towards coast to coast networks of marine protected areas (from the shore to the high and deep sea), coupled with sea-based wind energy potential. Scires It 6:1–95. https://doi.org/10.2423/i22394303v6Sp1
Bothwell HM, Cushman SA, Woolbright SA (2017) Conserving threatened riparian ecosystems in the American West: precipitation gradients and river networks drive genetic connectivity and diversity in a foundation riparian tree (Populus angustifolia). Mol Ecol 26:5114–5132. https://doi.org/10.1111/mec.14281
Brownstein MJ (1996) Modulation of non-templated nucleotide addition by Taq DNA polymerase: primer modifications that facilitate genotyping. Biotechniques 20:1004–1010. https://doi.org/10.2144/96206st01
Buonomo R, Assis J, Fernandes F, Engelen AH, Airoldi L, Serrão EA (2016) Habitat continuity and stepping stone oceanographic distances explain population genetic connectivity of the brown alga Cystoseira amentacea. Mol Ecol 26:766–780. https://doi.org/10.1111/mec.13960
Burnham KP, Anderson DR (2002) Model selection and inference: a practical information-theoretic approach, 2nd edn. Springer, New York. https://doi.org/10.1007/b97636
Carlson DF, Griffa A, Zambianchi E, Suaria G, Corgnati L, Magaldi MG, Poulain P-M, Russso A, Bellomo L, Mantovani C, Celentano P, Molcard A, Borghini M (2016) Observed and modeled surface Lagrangian transport between coastal regions in the Adriatic Sea with implications for marine protected areas. Cont Shelf Res 118:23–48. https://doi.org/10.1016/j.csr.2016.02.012
Casado-Amezúa P, García-Jiménez R, Kersting DK, Templado J, Coffroth MA, Merino P, Acevedo I, Machordom A (2011) Development of microsatellite markers as a molecular tool for conservation studies of the Mediterranean reef builder coral Cladocora caespitosa (Anthozoa, Scleractinia). J Hered 102:622–626. https://doi.org/10.1093/jhered/esr070
Casado-Amezúa P, Goffredo S, Templado J, Machordom A (2012) Genetic assessment of population structure and connectivity in the threatened Mediterranean coral Astroides calycularis (Scleractinia, Dendrophylliidae) at different spatial scales. Mol Ecol 21:3671–3685. https://doi.org/10.1111/j.1365-294X.2012.05655.x
Casado-Amezúa P, Kersting DK, Linares C, Bo M, Caroselli E, Garrabou J, Cerrano C, Ozalp B, Terrón-Sigler A, Betti F (2015) Cladocora caespitosa. The IUCN Red List of Threatened Species. e.T133142A75872554. http://dx.doi.org/10.2305/IUCN.UK.2015-2.RLTS.T133142A75872554.en
Casado-Amezúa P, Kersting DK, Templado J, Machordom A (2014) Regional genetic differentiation among populations of Cladocora caespitosa in the Western Mediterranean. Coral Reefs 33:1031–1040. https://doi.org/10.1007/s00338-014-1195-5
Castillo JA, Epps CW, Davis AR, Cushman SA (2014) Landscape effects on gene flow for a climate-sensitive montane species, the American pika. Mol Ecol 23:843–856. https://doi.org/10.1111/mec.12650
Chefaoui RM, Casado-Amezúa P, Templado J (2017) Environmental drivers of distribution and reef development of the Mediterranean coral Cladocora caespitosa. Coral Reefs 36:1195–1209. https://doi.org/10.1007/s00338-017-1611-8
Clynick BG, Chapman MG, Underwood AJ (2008) Fish assemblages associated with urban structures and natural reefs in Sydney, Australia. Austral Ecol 33:140–150. https://doi.org/10.1111/j.1442-9993.2007.01802.x
Coscia I, Robins PE, Porter JS, Malham SK, Ironside JE (2012) Modelled larval dispersal and measured gene flow: seascape genetics of the common cockle Cerastoderma edule in the southern Irish Sea. Conserv Genet 14:451. https://doi.org/10.1007/s10592-012-0404-4
Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Ann Rev Mar Sci 1:443–466. https://doi.org/10.1146/annurev.marine.010908.163757
Cushman SA, Elliot NB, Macdonald DW, Loveridge AJ (2016) A multi-scale assessment of population connectivity in African lions (Panthera leo). Landscape Ecol 31:1337–1353. https://doi.org/10.1007/s10980-015-0292-3
Cushman SA, McKelvey KS, Hayden J, Schwartz MK (2006) Gene flow in complex landscapes: testing multiple hypotheses with causal modelling. Am Nat 168:486–499. https://doi.org/10.1086/506976
Cushman SA, Shirk AJ, Howe GT, Murphy MA, Dyer RJ, Joost S (2018) The least cost path from landscape genetics to landscape genomics: challenges and opportunities to explore NGS data in a spatially explicit context. Front Genet 9:215. https://doi.org/10.3389/fgene.2018.00215
Cushman SA, Wasserman TN, Landguth EL, Shirk AJ (2013) Re-evaluating causal modelling with Mantel tests in landscape genetics. Diversity 5:51–72. https://doi.org/10.3390/d5010051
Dalongeville A, Benestan L, Mouillot D, Lobreaux S, Manel S (2018) Combining six genome scan melthods to detect candidate genes to salinity in the Mediterrenaean striped red mullet (Mullus surmuletus). BMC Genomics 19:217. https://doi.org/10.1186/s12864-018-4579-z
Dunning JB, Danielson BJ, Pulliam HR (1992) Ecological processes that affect populations in complex landscapes. Oikos 65:169–175
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 42:359–361. https://doi.org/10.1007/s12686-011-9548-7
Elahi R, O’Connor MI, Byrnes JE, Dunic J, Eriksson BK, Hensel MJ, Kearns PJ (2015) Recent trends in local-scale marine biodiversity reflect community structure and human impacts. Curr Biol 25:1938–1943. https://doi.org/10.1016/j.cub.2015.05.030
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620. https://doi.org/10.1111/j.1365-294x.2005.02553.x
Evans RD, Ryan NM, Travers MJ, Feng M, Hitchen Y, Kennington WJ (2019) A seascape genetic analysis of a stress-tolerant coral species along the Western Australian coast. Coral Reefs 38:63–78. https://doi.org/10.1007/s00338-018-01751-y
Excoffier L, Laval G, Schneider S (2005) ARLEQUIN (version 3.0: an integrated software package for population genetics data analysis). Evol Bioinform 1:47–50
Ferentinos G, Kastanos N (1988) Water circulation patterns in the Otranto Straits, eastern Mediterranean. Cont Shelf Res 8:1025–1041. https://doi.org/10.1016/0278-4343(88)90037-4
Foll M (2012) BayeScan v2.1 User Manual. Ecology 20:1450–1462
Galindo HM, Olson DB, Palumbi SR (2006) Seascape genetics: a coupled oceanographic-genetic model predicts population structure of Caribbean corals. Curr Biol 16:1622–1626. https://doi.org/10.1016/j.cub.2006.06.052
Goffredo S, Di Ceglie S, Zaccanti F (2009) Genetic differentiation of the temperate-subtropical stony coral Leptopsammia pruvoti in the Mediterranean Sea. Isr J Ecol Evol 55:99–115. https://doi.org/10.1560/IJEE.55.2.99
Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19
Harley CDG, Randall Hughes A, Hultgren KM, Miner BG, Sorte CJB, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241. https://doi.org/10.1111/j.1461-0248.2005.00871.x
Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Ecosystems of the world, vol 25. Elsevier, New York, pp 133–207
Hedgecock D, Chow V, Waples RS (1992) Effective population numbers of shellfish broodstocks estimated from temporal variance in allelic frequencies. Aquaculture 108:215–232. https://doi.org/10.1016/0044-8486(92)901008-W
Heerhartz SM, Dethier MN, Toft JD, Cordell JR, Ogston AS (2014) Effects of shoreline armoring on beach wrack subsidies to the nearshore ecotone in an estuarine fjord. Estuaries Coasts 37:1256–1268. https://doi.org/10.1007/s12237-013-9754-5
Jahnke M, Casagrandi R, Melià P, Schiavina M, Shultz ST, Zane L, Procaccini G (2017) Potential and realized connectivity of the seagrass Posidonia oceanica and their implication for conservation. Divers Distrib 23:1423–1434. https://doi.org/10.1111/ddi.12633
Jeffreys’s H (1961) Theory of probability (Oxford classic texts in the physical sciences), 3rd edn. Oxford University Press, Oxford
Kersting DK, Bensoussan N, Linares C (2013a) Long-term responses of the endemic reef-builder Cladocora caespitosa to Mediterranean warming. PLoS ONE 8:e70820. https://doi.org/10.1371/journal.pone.0070820
Kersting DK, Casado C, López-Legentil S, Linares C (2013b) Unexpected patterns in the sexual reproduction of the Mediterranean scleractinian coral Cladocora caespitosa. Mar Ecol Prog Ser 486:165–171. https://doi.org/10.3354/meps10356
Kersting DK, Linares C (2012) Cladocora caespitosa bioconstructions in the Columbretes Islands Marine Reserve (Spain), NW Mediterranean: distribution, size structure and growth. Mar Ecol 33:427–436. https://doi.org/10.1111/j.1439-0485.2011.00508.x
Kersting DK, Teixidó N, Linares C (2014) Recruitment and mortality of the temperate coral Cladocora caespitosa: implications for the recovery of endangered populations. Coral Reefs 33:403–407
Kopelman NM, Mayze J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191. https://doi.org/10.1111/1755-0998.12387
Kružić P, Benković L (2008) Bioconstructional features of the coral Cladocora caespitosa (Anthozoa, Scleractinia) in the Adriatic Sea (Croatia). Mar Ecol 29:125–139. https://doi.org/10.1111/j.1439-0485.20008.00220.x
Kružić P, Žuljević A, Nikolić V (2008) Spawning of the colonial coral Cladocora caespitosa (Anthozoa, Scleractinia) in the Southern Adriatic Sea. Coral Reefs 27:337–341. https://doi.org/10.1007/s00338-007-0334-7
Landguth EL, Hand BK, Glassy JM, Cushman SA, Sawaya M (2011) UNICOR: a species connectivity and corridor network simulator. Ecography 34:1–6. https://doi.org/10.1111/j.1600-0587.2011.07149.x
Landguth EL, Holden ZA, Mahalovich MF, Cushman SA (2017) Using landscape genetics simulations for planting blister rust resistant whitebark pine in the US Northern Rocky Mountains. Front Genet 8:9. https://doi.org/10.3389/fgene.2017.00009
Liggins L, Treml EA, Riginos C (2013) Taking the plunge: an introduction to undertaking seascape genetic studies and using biophysical models. Geogr Compass 7:173–196. https://doi.org/10.1111/gec3.12031
Linnaeus C (1767) Systema naturae per regna tria naturae: secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Ed. 12. 1., Regnum Animale. 1 2. Holmiae, Laurentii Salvii. Holmiae Stockholm, Laurentii Salvii. pp 1–532 [1766] pp 533–1327
López-Márquez V, Templado J, Buckley D, Marino I, Boscari E, Micu D, Zane L, Machordom A (2019) Connectivity among populations of the top shell Gibbula divaricata in the Adriatic Sea. Front Genet 10:177. https://doi.org/10.3389/fgene.2019.00177
Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197. https://doi.org/10.1016/S0169-5347(03)00008-9
Mann KH, Lazier JRN (2006) Dynamics of marine ecosystems: biological-physical interactions in the oceans. Blackwell Publishing, Malden, MA, p 496
Manni F, Guerar E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76:173–190. https://doi.org/10.1353/hub.2004.0034
Mantel N (1967) Detection of disease clustering and a generalized regression approach. Can Res 27:209–220
Melià P, Schiavina M, Rossetto M, Gatto M, Fraschetti S, Casagrandi R (2016) Looking for hotspots of marine metacommunity connectivity: a methodological framework. Sci Rep 6:23705. https://doi.org/10.1038/srep23705
Monmonier MS (1973) Maximum-difference barriers: an alternative numerical regionalization method. Geogr Anal 5:245–261. https://doi.org/10.1111/j.1538-4632.1973.tb01011.x
Montefalcone M, Parravicini V, Vacchi M, Albertelli G, Ferrari M, Morri C, Bianchi CN (2010) Human influence on seagrass habitat fragmentation in NW Mediterranean Sea. Estuar Coast Shelf Sci 86:292–298. https://doi.org/10.1016/j.ecss.2009.11.018
Nicholls R, Woodroffe C, Burkett V (2016) Coastline degradation as an indicator of global change. In: Letcher TM (ed) Climate change: observed impacts on Planet Earth. Elsevier, Amsterdam, pp 309–324
Paetkau D, Slade R, Burden M, Estoup A (2004) Direct, real-time estimation of migration rate using assignment methods: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65. https://doi.org/10.1046/j.1365-294X.2004.02008.x
Paterno M, Schiavina M, Aglieri G, Ben Souissi J, Boscari E, Casagrandi R, Chassanite A, Chiantore M, Congiu L, Guarnieri G, Kruschel C, Macic V, Marino IAM, Papetti C, Patarnello T, Zane L, Melià P (2017) Population genomics meet Lagrangian simulations: oceanographic patterns and long larval duration ensure connectivity among Paracentrotus lividus populations in the Adriatic and Ionian seas. Ecol Evol 7:2463–2479. https://doi.org/10.1002/ece3.2844
Peakal R, Smouse PE (2006) GENEALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x
Peirano A, Abbate M, Cerrati G, Difesca V, Peroni C, Rodolfo-Metalpa R (2005) Monthly variations in calix growth, polyp tissue, and density banding of the Mediterranean scleractinian Cladocora caespitosa (L.). Coral Reefs 24:404–409. https://doi.org/10.1007/s00338-005-0020-6
Peirano A, Kružić P, Mastronuzzi G (2009) Growth of Mediterranean reef of Cladocora caespitosa (L.) in the late quaternary and climate inferences. Facies 55:325–333. https://doi.org/10.1007/s10347-008-0177-x
Perry CT, Larcombe P (2003) Marginal and non-reef-building coral environments. Coral Reefs 22:427–432. https://doi.org/10.1007/s00338-003-0330-5
Pineda J, Hare JA, Sponaugle S (2007) Larval transport and dispersal in the coastal ocean and consequences for population connectivity. Oceanography 20:22–39. https://doi.org/10.5670/oceanog.2007.27
Pinsky ML, Palumbi SR (2014) Meta-analysis reveals lower genetic diversity in overfished populations. Mol Ecol 23:29–39. https://doi.org/10.1111/mec.12509
Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539. https://doi.org/10.1093/jhered/esh074
Polato N, Concepcion GT, Toonen RJ, Baums I (2010) Isolation by distance across the Hawaiian Archipelago in the reef-building coral Porites lobata. Mol Ecol 19:4661–4677. https://doi.org/10.1111/j.1365-294X.2010.04836.x
Poulain PM, Hariri S (2013) Transit and residence times in the surface Adriatic Sea as derived from drifter data and Lagrangian numerical simulations. Ocean Sci 9:713–729. https://doi.org/10.5194/os-9-713-2013
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201. https://doi.org/10.1073/pnas.94.17.9197
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249. https://doi.org/10.1093/oxfordjournals.jhered.a111573
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Riginos C, Liggins L (2013) Seascape genetics: populations, individuals, and genes marooned and adrift. Geogr Compass 7:197–216. https://doi.org/10.1111/gec3.12032
Russo A, Artegiani A (1996) Adriatic sea hydrography. Sci Mar 60:33–43
Schubel JR (1994) Coastal pollution and waste management, chapter 9. In: Environmental science in the coastal zone: issues for further research. The National Academies Press, Washington, DC
Selkoe KA, D’Aloia CD, Crandall ED, Iacchei M, Liggins L, Puritz JB, von der Heyden S, Toonen RJ (2016) A decade of seascape genetics: contributions to basic and applied marine connectivity. Mar Ecol Prog Ser 554:1–19. https://doi.org/10.3354/meps11792
Selkoe KA, Henzler CM, Gaines SD (2008) Seascape genetics and the spatial ecology of marine populations. Fish Fish 9:363–377. https://doi.org/10.1111/j.1467-2979.2008.00300.x
Selkoe KA, Scribner KT, Galindo HM (2015) Waterscape genetics -applications of landscape genetics to rivers, lakes and seas. In: Balkenhol N, Cushman SA, Storfer AT, Waits LP (eds) Landscape genetics: concepts, methods, applications. Wiley, UK, pp 220–245
Selkoe KA, Toonen RJ (2011) Marine connectivity: a new look at pelagic larval duration and genetic metrics of dispersal. Mar Ecol Prog Ser 436:291–305. https://doi.org/10.3354/meps09238
Severance EG, Karl SA (2006) Contrasting population genetic structures of sympatric, mass-spawning Caribbean corals. Mar Biol 150:57–68. https://doi.org/10.1007/s00227-006-0332-2
Shirk AJ, Cushman SA, Waring KM, Wehenkel CA, Leal-Sáenz A, Toney C, Lopez-Sanchez CA (2018) Southwestern white pine (Pinus strobiformis) species distribution models project a large range shift and contraction due to regional climatic changes. Forest Ecol Manag 411:176–186. https://doi.org/10.1016/j.foreco.2018.01.025
Shirk AJ, Landguth EL, Cushman SA (2017) A comparision of regression methods for model selection in individual-based landscape genetic analysis. Mol Ecol Resour 18:55–67. https://doi.org/10.1111/1755-0998.12709
Shirk AJ, Wallin DO, Cushman SA, Rice CG, Warheit KI (2010) Inferring landscape effects on gene flow: a new model selection framework. Mol Ecol 19:3603–3619. https://doi.org/10.1111/j.1365-294X.2010.04745.x
Siegel DA, Kinlan BP, Gaylord B, Gaines SD (2003) Lagrangian descriptions of marine larval dispersion. Mar Ecol Prog Ser 260:83–96. https://doi.org/10.3354/meps260083
Sponaugle S, Cowen RK, Shanks A, Morgan SG, Leis JM, Pineda J, Boehlert GW, Kingsford MJ, Lindeman KC, Grimes C, Munro L (2002) Predicting self-recruitment in marine populations: biophysical correlates and mechanisms. Bull Mar Sci 70:341–375
Storfer A, Murphy MA, Evans S, Golberg CS, Robinson S, Spear SF, Dezzani R, Delmelle E, Vierling L, Waits LP (2007) Putting the “landscape” in landscape genetics. Heredity 98:128–142. https://doi.org/10.1038/sj.hdy.6800917
Storfer A, Murphy MA, Spear SF, Holderegger R, Waits LP (2010) Landscape genetics: where are we now? Mol Ecol 19:3496–3514. https://doi.org/10.1111/j.1365-294X.2010.04691.x
Strathmann RR, Hughes TP, Kuris AM, Lindeman KC, Morgan SG, Pandolfi JM, Warner RR (2002) Evolution of local recruitment and its consequences for marine populations. Bull Mar Sci 70:377–396
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICROCHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x
Venter O, Sanderson EW, Magrach A, Allan JR, Beher J, Jones KR, Possingham HF, Laurance WF, Wood P, Fekete BM, Levy MA, Watson JEM (2016) Global terrestrial human footprint maps for 1993-2009. Sci data 3:160067. https://doi.org/10.1038/sdata.2016.67
Waples RS (1990) Conservation genetics of Pacific Salmon. II. Effective population size and the rate of loss of genetic variability. J Hered 81:267–276
Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: Fst ≠ 1/(4Nm + 1). Heredity 82:117–125
Woodson CB, McManus MA (2007) Foraging behaviour can influence dispersal marine organisms. Limnol Oceanogr 52:2701–2709
Yang J, Cushman SA, Song X, Yang J, Zhang P (2015) Genetic diversity and drivers of genetic differentiation of Reaumuria soongorica of the Inner Mongolia plateau in China. Plant Ecol 216:925–937. https://doi.org/10.1007/s11258-015-0479-3
Yang J, Cushman SA, Yang J, Yang M, Bao T (2013) Effects of climatic gradients on genetic differentiation of Caragana on the Ordos Plateau, China. Landscape Ecol 28:1729–1741. https://doi.org/10.1007/s10980-013-9913-x
Zayasu Y, Satoh N, Shinzato C (2018) Genetic diversity of farmed and wild populations of the reef-building coral, Acropora tenuis. Restor Ecol 26:1195–1202. https://doi.org/10.1111/rec.12687
Acknowledgements
This research was funded by the European project CoCoNET “Towards COast to COast NETworks of marine protected areas (from the shore to the high and deep sea), coupled with sea-based wind energy potential” from the VII FP of the European Commission (Grant Agreement No. 287844) and the Spanish Ministry of Economy and Competitiveness (Grant reference: CTM2014-57949-R). We want to thank Antheus s.r.l and many people who helped collecting samples. Thanks to Computational Biogeography and photography laboratories of the MNCN and to Melinda Modrell for the revision of the language.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
López-Márquez, V., Cushman, S.A., Templado, J. et al. Seascape genetics and connectivity modelling for an endangered Mediterranean coral in the northern Ionian and Adriatic seas. Landscape Ecol 34, 2649–2668 (2019). https://doi.org/10.1007/s10980-019-00911-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10980-019-00911-x