Skip to main content

Advertisement

SpringerLink
Log in

Interplay between isolation by distance and genetic clusters in the red coral Corallium rubrum: insights from simulated and empirical data

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

The analysis of genetic structure is an important tool for the management of harvested and threatened species. Individual clustering methods and tests of Isolation by Distance (IBD) are currently used in this context. They have been applied to the red coral Corallium rubrum but some questions remained due to contrasted results among studies and limits in their interpretations. In this study, we used simulated and empirical data for a better understanding of the genetic structure in this species. We tested the impact of IBD between demes, sampling scheme and of clustering methods (BAPS, STRUCTURE or DAPC) on the inferred structure. By matching simulated scenarios to the empirical data, we first confirm that the genetic structure of the red coral is characterized by a combination between IBD and weak genetic breaks. Then, we demonstrate how the sampling scheme influences the results of the clustering methods. We also reveal the contrasted efficiencies of these methods to recover real demes or groups of demes in a context of IBD. Overall, our study underline the interest of comparing the results of different clustering methods and of using simulated data for interpreting empirical genetical data.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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 139:855–869

    Article  PubMed  CAS  Google Scholar 

  • Barnosky AD, Hadly EA, Bascompte J et al (2012) Approaching a state shift in earth’s biosphere. Nature 486:52–58

    Article  PubMed  CAS  Google Scholar 

  • Beaumont MA, Balding DJ (2004) Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol 13:969–980

    Article  PubMed  CAS  Google Scholar 

  • Blair C, Weigel DE, Balazik M, Keeley ATH, Walker FM, Landguth E, Cushman S, Murphy M, Waits L, Balkenhol N (2012) A simulation-based evaluation of methods for inferring linear barriers to gene flow. Mol Ecol Res 12:822–833

    Article  Google Scholar 

  • Bruckner AW (2009) Rate and extent of decline in Corallium (pink and red coral) populations: existing data meet the requirements for a CITES Appendix II listing. Mar Ecol Prog Ser 397:319–332

    Google Scholar 

  • Castric V, Bernatchez L (2003) The rise and fall of isolation by distance in the anadromous brook charr (Salvelinus fontinalis Mitchill). Genetics 163(3):983–996

    PubMed  Google Scholar 

  • Chen C, Durand E, Forbes F (2007) Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Mol Ecol Notes 7:747–756

    Article  Google Scholar 

  • Corander J, Marttinen P (2006) Bayesian identification of admixture events using multilocus molecular markers. Mol Ecol 15:2833–2843

    Article  PubMed  Google Scholar 

  • Corander J, Waldmann P, Sillanpää MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163(1):367–374

    PubMed  CAS  Google Scholar 

  • Corander J, Marttinen P, Siren J, Tang J (2008a) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinform 9(1):539

    Article  Google Scholar 

  • Corander J, Sirén J, Arjas E (2008b) Bayesian spatial modelling of genetic population structure. Comput Stat 23:111–129

    Article  Google Scholar 

  • Costantini F, Fauvelot C, Abbiati M (2007a) 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 

  • Costantini F, Fauvelot C, Abbiati M (2007b) Genetic structuring of the temperate gorgonian coral (Corallium rubrum) across the western Mediterranean sea revealed by microsatellites and nuclear sequences. Mol Ecol 16:5168–5182

    Article  PubMed  CAS  Google Scholar 

  • 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 31:261–269

    Google Scholar 

  • Dawson KJ, Belkhir K (2001) A Bayesian approach to the identification of panmictic populations and the assignment of individuals. Genet Res Camb 78:59–77

    Article  CAS  Google Scholar 

  • Dawson KJ, Belkhir K (2009) An agglomerative hierarchical approach to visualization in Bayesian clustering problems. Heredity 103:32–45

    Article  PubMed  CAS  Google Scholar 

  • Dellicour S, Frantz A, Colyn M, Bertouille S, Chaumont F, Flamand M-C (2011) Population structure and genetic diversity of red deer (Cervus elaphus) in forest fragments in north-western France. Cons Gen 12:1287–1297

    Article  Google Scholar 

  • Durand E, Jay F, Gaggiotti OE, François O (2009) Spatial inference of admixture proportions and secondary contact zones. Mol Biol Evol 26(9):1963–1973

    Article  PubMed  CAS  Google Scholar 

  • Earl D, vonHoldt B (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Cons Gen Res 4(2):359–361

    Article  Google Scholar 

  • Epperson BK, McRae BH, Scribner K, Cushman SA, Rosenberg MS, Fortin M-J, James PMA et al (2010) Utility of computer simulations in landscape genetics. Mol Ecol 19(17):3549–3564

    Article  PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620

    Article  PubMed  CAS  Google Scholar 

  • Excoffier, Laval LG, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164(4):1567–1587

    PubMed  CAS  Google Scholar 

  • François O, Durand E (2010) Spatially explicit Bayesian clustering models in population genetics. Mol Ecol Res 10:773–784

    Article  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2010) Introduction to conservation genetics, 2nd edn. Cambridge University Press, New York

    Book  Google Scholar 

  • Frantz AC, Cellina S, Krier A, Schley L, Burke T (2009) Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: clusters or isolation by distance? J Appl Ecol 46:493–505

    Article  Google Scholar 

  • Garrabou J, Coma R, Bensoussan N et al (2009) Mass mortality in northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob Change Biol 15(5):1090–1103

    Article  Google Scholar 

  • Gauffre B, Estoup A, Bretagnolle V, Cosson JF (2008) Spatial genetic structure of a small rodent in a heterogeneous landscape. Mol Ecol 17:4619–4629

    Article  PubMed  CAS  Google Scholar 

  • Giraudel JL, Aurelle D, Lek S, Berrebi P (2000) Application of the self-organizing mapping and fuzzy clustering to microsatellite data: how to detect genetic structure in brown trout (Salmo trutta) populations. In: Lek S, Guégan JF (eds) Artificial neuronal networks. Springer, Berlin, pp 187–202

    Chapter  Google Scholar 

  • Guillot G, Estoup A, Mortier F, Cosson JF (2005) A spatial statistical model for landscape genetics. Genetics 170(3):1261–1280

    Article  PubMed  CAS  Google Scholar 

  • Guillot G, Leblois R, Coulon A, Frantz AC (2009) Statistical methods in spatial genetics. Mol Ecol 18:4734–4756

    Article  PubMed  Google Scholar 

  • Heller R, Siegismund HR (2009) Relationship between three measures of genetic differentiation G ST, D EST and G’ ST : how wrong have we been? Mol Ecol 18:2080–2083

    Article  PubMed  CAS  Google Scholar 

  • Hoban S, Bertorelle G, Gaggiotti OE (2012) Computer simulations: tools for population and evolutionary genetics. Nat Rev Gen 13:110–122

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11(1):94

    Article  PubMed  Google Scholar 

  • Kalinowski ST (2011) The computer program STRUCTURE does not reliably identify the main genetic clusters within species: simulations and implications for human population structure. Heredity 106(4):625–632

    Article  PubMed  CAS  Google Scholar 

  • Kimura M, Weiss GH (1964) Stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49:561–576

    PubMed  CAS  Google Scholar 

  • Latch EK, Dharmarajan G, Glaubitz JC, Rhodes OEJ (2006) Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Cons Gen 7:295–302

    Article  Google Scholar 

  • Laval G, Excoffier L (2004) SIMCOAL 2.0: a program to simulate genomic diversity over large recombining regions in a subdivided population with a complex history. Bioinformatics 20(15):2485–2487

    Article  PubMed  CAS  Google Scholar 

  • Leblois R, Estoup A, Rousset F (2003) Influence of mutational and sampling factors on the estimation of demographic parameters in a ‘‘Continuous’’ population under isolation by distance. Mol Biol Evol 20(4):491–502

    Article  PubMed  CAS  Google Scholar 

  • Leblois R, Estoup A, Rousset F (2009) IBD Sim: a computer program to simulate genotypic data under Isolation by Distance. Mol Ecol Res 9:107–109

    Article  Google Scholar 

  • 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(19):4204–4216

    Article  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(4):675–690

    Article  PubMed  CAS  Google Scholar 

  • Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18(4):189–197

    Article  Google Scholar 

  • Orozco-Ter Wengel P, Corander J, Schlötterer C (2011) Genealogical lineage sorting leads to significant but incorrect Bayesian multilocus inference of population structure. Mol Ecol 20:1108–1121

    Article  Google Scholar 

  • Palsbøll PJ, Bérubé M, Allendorf FW (2006) Identification of management units using population genetic data. Trends Ecol Evol 22(1):11–16

    Article  PubMed  Google Scholar 

  • Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13(sp1):146–158

    Article  Google Scholar 

  • Perrier C, Guyomard R, Baglinière J-L, Evanno G (2011) Determinants of hierarchical genetic structure in Atlantic salmon populations: environmental factors vs. anthropogenic influences. Mol Ecol 20(20):4231–4245

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959

    PubMed  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1283–1286

    Article  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145(4):1219–1228

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Rousset F, Leblois R (2012) Likelihood-based inferences under isolation by distance: two-dimensional habitats and confidence intervals. Mol Biol Evol 29(3):957–973

    Article  PubMed  CAS  Google Scholar 

  • Safner T, Miller MP, McRae BH, Fortin M-J, Manel S (2011) Comparison of Bayesian clustering and edge detection methods for inferring boundaries in landscape genetics. Int J Mol Sci 12:865–889

    Article  PubMed  CAS  Google Scholar 

  • Schwartz MK, McKelvey KS (2009) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Cons Genet 10(2):441–452

    Article  Google Scholar 

  • Viard F, Franck P, Dubois M-P, Estoup A, Jarne P (1998) Variation of microsatellite size homoplasy across electromorphs, loci, and populations in three invertebrate species. J Mol Evol 47:42–51

    Article  PubMed  CAS  Google Scholar 

  • Waples RS, Gaggiotti O (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15:1419–1439

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Zellmer AJ, Hanes MM, Hird SM, Carstens BC (2012) Deep phylogeographic structure and environmental differentiation in the carnivorous plant Sarracenia alata. Syst Biol 61(5):763–777

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Anne Chenuil-Maurel and Gwilherm Penant for helpful discussion on this topic. Two anonymous reviewers greatly helped improving a first version of this manuscript. J-B. Ledoux is supported by a post-doctoral grant SFRH/BPD/74400/2010 from Fundação para a Ciência e Tecnologia (FCT).

Author information

Authors and Affiliations

  1. Aix-Marseille Université, CNRS, IMBE UMR 7263, 13007, Marseille, France

    Didier Aurelle & Jean-Baptiste Ledoux

  2. Institut de Ciències del Mar CSIC, Passeig Maritim de la Barceloneta 37-49, 08003, Barcelona, Spain

    Jean-Baptiste Ledoux

  3. CIMAR/CIIMAR, Centro Interdisciplinar de Investigação Marinha e Ambiental, Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Porto, Portugal

    Jean-Baptiste Ledoux

Authors
  1. Didier Aurelle
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jean-Baptiste Ledoux
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Didier Aurelle.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 352 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aurelle, D., Ledoux, JB. Interplay between isolation by distance and genetic clusters in the red coral Corallium rubrum: insights from simulated and empirical data. Conserv Genet 14, 705–716 (2013). https://doi.org/10.1007/s10592-013-0464-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-013-0464-0

Keywords

Search

Navigation