Skip to main content

Advertisement

SpringerLink
Log in

The importance of sampling design: spatial patterns and clonality in estimating the genetic diversity of coral reefs

  • Feature Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The interpretation of genetic variation on and among corals on reefs has rarely been contextualized in an explicitly spatial framework where each individual has both genetic and spatial parameters. Here, we explore interactions between sampling effort, sampling design, and the presence of spatial genetic structure (SGS) on the ability to effectively characterize genetic diversity on a coral reef. To do this, we take our dataset of 2352 genotypes (78 unique multi-locus genotypes) of the coral, Pocillopora damicornis, collected from June 2007 to October 2009, a dataset of near-exhaustive sampling of a single patch reef in Kāne‘ohe Bay, Hawai‘i (21°27.462N, 157°48.405W), and subsample from it using three different strategies: (1) random sampling from throughout the reef; (2) saturation sampling all corals from within a pre-defined area of the reef, avoiding the reef’s edge; and (3) sampling all nearest neighbors of a randomly chosen coral while allowing for the inclusion of the reef’s edge. Our results demonstrate appreciable variation (e.g., 0.35–0.46) in estimates of observed heterozygosity (H O) using a typical sample size of 50 and that in the presence of SGS, non-random sampling schemes can give biased estimates of genetic diversity. Furthermore, our results indicate that over 1000 samples (i.e., ~40 % of the total number of colonies) are required to reveal the true pattern of spatial genetic structure at our site. We also demonstrate by rarefaction analysis that the bias in estimating clonal richness (i.e., the proportion of unique genotypes in a given sampling area relative to the total number of samples surveyed) for small sample numbers is due to the predominance of clones (i.e., high level of clonality) and not skew in genet frequency distribution. Overall, we argue that: (1) consideration of sampling design is important in population genetic studies, particularly since non-random sampling in the presence of SGS can give biased estimates of genetic diversity and (2) intense to near-exhaustive sampling schemes may be important for characterizing genetic diversity in highly clonal populations.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Alberto F, Gouveia L, Arnaud-Haond S, Pérez-Lloréns JL, Duarte CM, Serrão EA (2005) Within-population spatial genetic structure, neighbourhood size and clonal subrange in the seagrass Cymodocea nodosa. Mol Ecol 14:2669–2681

    Article  CAS  Google Scholar 

  • Arnaud-Haond S, Duarte CM, Alberto F, Serrão EA (2007) Standardizing methods to address clonality in population studies. Mol Ecol 16:5115–5139

    Article  CAS  Google Scholar 

  • Arnaud-Haond S, Vonau V, Rouxel C, Bonhomme F, Prou J, Goyard E, Boudry P (2008) Genetic structure at different spatial scales in the pearl oyster (Pinctada margaritifera cumingii) in French Polynesian lagoons: beware of sampling strategy and genetic patchiness. Mar Biol 155:147–157

    Article  Google Scholar 

  • Baltanás A (1992) On the use of some methods for the estimation of species richness. Oikos 65:484–492

    Article  Google Scholar 

  • Baums IB, Miller MW, Hellberg ME (2006) Geographic variation in clonal structure in a reef-building Caribbean coral, Acropora palmate. Ecol Mono 76:503–519

    Article  Google Scholar 

  • Becheler R, Diekmann O, Hily C, Moalic Y, Arnaud-Haond S (2010) The concept of population in clonal organisms: mosaics of temporally colonized patches are forming highly diverse meadows of Zostera marina in Brittany. Mol Ecol 19:2394–2407

    CAS  Google Scholar 

  • Becheler R, Benkara E, Moalic Y, Arnaud-Haond S (2013) Scaling of processes shaping the clonal dynamics and genetic mosaics of seagrasses through temporal genetic monitoring. Hered 112:114–121

    Article  Google Scholar 

  • Billingham MR, Simões T, Reusch TBH, Serrão EA (2007) Genetic sub-structure and intermediate optimal outcrossing distance in the marine angiosperm Zostera marina. Mar Biol 152:793–801

    Article  Google Scholar 

  • Björklund M, Bergek S (2009) On the relationship between population differentiation and sampling effort: is more always better? Oikos 118:1127–1129

    Article  Google Scholar 

  • Blanquer A, Uriz M, Caujapé-Castells J (2009) Small-scale spatial genetic structure in Scopalina lophyropoda, an encrusting sponge with philopatric larval dispersal and frequent fission and fusion events. Mar Ecol Prog Ser 380:95–102

    Article  Google Scholar 

  • Brose U, Martinez ND, Williams RJ (2003) Estimating species richness: sensitivity to sample coverage and insensitivity to spatial patterns. Ecol 84:2364–2377

    Article  Google Scholar 

  • Calderón I, Ortega N, Duran S et al (2007) Finding the relevant scale: clonality and genetic structure in a marine invertebrate (Crambe crambe, Porifera). Mol Ecol 16:1799–1810

    Article  Google Scholar 

  • Cavers S, Degen B, Caron H, Lemes MR, Margis R, Salgueiro F, Lowe AJ (2005) Optimal sampling strategy for estimation of spatial genetic structure in tree populations. Hered 95:281–289

    Article  CAS  Google Scholar 

  • Chao A, Shen T-J (2003) Nonparametric estimation of Shannon’s index of diversity when there are unseen species in sample. Enviro Ecol Stat 10:429–443

    Article  Google Scholar 

  • Combosch DJ, Vollmer SV (2011) Population genetics of an ecosystem-defining reef coral Pocillopora damicornis in the tropical eastern Pacific. PLoS ONE 6:e21200

    Article  CAS  Google Scholar 

  • De Meeûs T, Lehmann L, Balloux F (2006) Molecular epidemiology of clonal diploids: a quick overview and a short DIY (do it yourself) notice. Infect Genet Evol 6:163–170

    Article  Google Scholar 

  • Ellstrand NC, Roose ML (1987) Patterns of genotypic diversity in clonal plant species. Am J Bot 74:123–131

    Article  Google Scholar 

  • Epperson BK (1993) Spatial and space-time correlations in systems of subpopulations with genetic drift and migration. Genetics 133:711–727

    CAS  Google Scholar 

  • Fager EW (1972) Diversity: a sampling study. Am Nat 106:293–310

    Article  Google Scholar 

  • Gorospe KD, Karl SA (2013) Genetic relatedness does not retain spatial pattern across multiple spatial scales: dispersal and colonization in the coral, Pocillopora damicornis. Mol Ecol 22:3721–3736

    Article  Google Scholar 

  • Halkett F, Simon J, Balloux F (2005) Tackling the population genetics of clonal and partially clonal organisms. TREE 20:194–201

    Google Scholar 

  • Hardy OJ, Vekemans X (1999) Isolation by distance in a continuous population: reconciliation between spatial autocorrelation analysis and population genetics models. Hered 83:145–154

    Article  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Not 2:618–620

    Article  Google Scholar 

  • Heywood JS (1991) Spatial analysis of genetic variation in plant populations. Ann Revi Ecol Syst 22:335–355

    Article  Google Scholar 

  • Hunter CL (1993) Genotypic variation and clonal structure in coral populations with different disturbance histories. Evol 47:1213–1228

    Article  Google Scholar 

  • Johnson MS, Black R (1982) Chaotic genetic patchiness in an intertidal limpet, Siphonaria sp. Mar Biol 70:157–164

    Article  Google Scholar 

  • Jost L (2008) G ST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    Article  Google Scholar 

  • Kalisz S, Nason JD, Hanzawa FM, Tonsor SJ (2001) Spatial population genetic structure in Trillium grandiflorum: the roles of dispersal, mating, history, and selection. Evol 55:1560–1568

    Article  CAS  Google Scholar 

  • Ledoux JB, Garrabou J, Bianchimani O, Drap P, Féral JP, Aurelle D (2010) Fine-scale genetic structure and inferences on population biology in the threatened Mediterranean red coral, Corallium rubrum. Mol Ecol 19:4204–4216

    Article  Google Scholar 

  • Legendre P, Dale MRT, Fortin M-J, Gurevitch J, Hohn M, Myers D (2002) The consequences of spatial structure for the design and analysis of ecological field surveys. Ecogr 25:601–615

    Article  Google Scholar 

  • McFadden CS (1997) Contributions of sexual and asexual reproduction to population structure in the clonal soft coral, Alcyonium rudyi. Evol 51:112–126

    Article  Google Scholar 

  • Meirmans PG (2012) The trouble with isolation by distance. Mol Ecol 21:2839–2846

    Article  Google Scholar 

  • Meirmans P, van Tienderen P (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Not 4:792–794

    Article  Google Scholar 

  • Miller KJ, Ayre DJ (2008) Population structure is not a simple function of reproductive mode and larval type: insights from tropical corals. J Anim Eco 77:713–724

    Article  Google Scholar 

  • Moran PAP (1950) Notes on continuous stochastic phenomena. Biometrika 37:17–23

    Article  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Apps 13:S146–S158

    Article  Google Scholar 

  • Pauls SU, Nowak C, Bálint M, Pfenninger M (2013) The impact of global climate change on genetic diversity within populations and species. Mol Ecol 22:925–946

    Article  Google Scholar 

  • Pinheiro JC, Bates DM, DebRoy S, Sarkar D, The R Development Core Team (2013) NLME: linear and nonlinear mixed effects models. R package version 3.1-111

  • Polato N, Concepcion GT, Toonen RJ, Baums IB (2010) Isolation by distance across the Hawaiian Archipelago in the reef-building coral Porites lobata. Mol Ecol 19:4661–4677

    Article  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Riginos C, Douglas KE, Jin Y, Shanahan DF, Treml EA (2011) Effects of geography and life history traits on genetic differentiation in benthic marine fishes. Ecog 34:566–575

    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 

  • Ruzzante D (1998) A comparison of several measures of genetic distance and population structure with microsatellite data: bias and sampling variance. Can J Fish Aquat Sci 55:1–14

    Article  Google Scholar 

  • Schwartz MK, McKelvey KS (2008) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Con Gen 10:441–452

    Article  Google Scholar 

  • Selkoe KA, Watson JR, White C, Horin B, Iacchei M, Mitarai S, Siegel DA, Gaines SD, Toonen RJ (2010) Taking the chaos out of genetic patchiness: seascape genetics reveals ecological and oceanographic drivers of genetic patterns in three temperate reef species. Mol Ecol 19:3708–3726

    Article  Google Scholar 

  • Slatkin M, Arter HE (1991) Spatial autocorrelation methods in population genetics. Am Nat 138:499–517

    Article  Google Scholar 

  • Sokal RR, Oden NL, Thomson BA (1997) A simulation study of microevolutionary inferences by spatial autocorrelation analysis. Biol J Lin Soc 60:73–93

    Article  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  Google Scholar 

  • van Oppen MJH, Gates RD (2006) Conservation genetics and the resilience of reef- building corals. Mol Ecol 15:3863–3883

    Article  Google Scholar 

  • Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935

    Article  CAS  Google Scholar 

  • Weersing K, Toonen R (2009) Population genetics, larval dispersal, and connectivity in marine systems. Mar Ecol Prog Ser 393:1–12

    Article  Google Scholar 

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

    Article  Google Scholar 

Download references

Acknowledgments

We acknowledge K. Withy-Allen, P. Bool, T. Burgess, M. Castrence, S. Churchill, M. Coloma, C. Demyan, M. DeLisle, K. Duncan, L. Furuto, M. Gaither, M. Hagedorn, R. Haverkort, M. Hayatdavoodi, L. Hedouin, H. Hilmer, M. Iacchei, D. Jayewardene, R. Lambrix, D. Lin, R. Lindemann, M. Lurie, B. Noedl, M. Noedl, A. Pan, C. Pequignet, H. Putnam, C. Rivera, T. Sauvage, J. Schultz, D. Smith, M. Takahashi, K. Tice, C. Tran, N. Umphress, and S. Webb for help with field work. Special thanks to D. Carlon, M. Donahue, M. McGranaghan, and R. Toonen for support and advice. We also thank the HIMB NSF-EPSCoR Core Genetics Lab Facility (EPS-0903833) for DNA fragment analysis support. Funding was provided to SAK by the National Science Foundation Grant OCE 06-27299 and Arcadia Wildlife, Inc. and to KDG by the National Science Foundation Graduate Research Fellowship Program and the University of Hawai‘i Edmondson Research Grant. The comments of S. Arnaud-Haond and two anonymous reviewers greatly improved the manuscript. This is Hawai‘i Institute of Marine Biology contribution #1617 and SOEST #9282.

Author information

Authors and Affiliations

  1. Hawai‘i Institute of Marine Biology, University of Hawai‘i at Mānoa, P.O. Box 1346, Kāne‘ohe, HI, 96744, USA

    Kelvin D. Gorospe, Megan J. Donahue & Stephen A. Karl

Authors
  1. Kelvin D. Gorospe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Megan J. Donahue
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stephen A. Karl
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stephen A. Karl.

Additional information

Communicated by C. Riginos.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 106 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gorospe, K.D., Donahue, M.J. & Karl, S.A. The importance of sampling design: spatial patterns and clonality in estimating the genetic diversity of coral reefs. Mar Biol 162, 917–928 (2015). https://doi.org/10.1007/s00227-015-2634-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-015-2634-8

Keywords

Search

Navigation