Skip to main content
SpringerLink
Log in

Fine-scale patterns of genetic variation in a widespread clonal seagrass species

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Seagrasses are ecosystem engineers that offer important habitat for a large number of species and provide a range of ecosystem services. Many seagrass ecosystems are dominated by a single species, with research showing that genotypic diversity at fine spatial scales plays an important role in maintaining a range of ecosystem functions. However, for most seagrass species, information on fine-scale patterns of genetic variation in natural populations is lacking. In this study, we use a hierarchical sampling design to determine the levels of genetic and genotypic diversity at different spatial scales (centimeters, meters, kilometers) in the Australian seagrass Zostera muelleri. Our analysis shows that at fine spatial scales (<1 m), levels of genotypic diversity are relatively low (R (Plots) = 0.37 ± 0.06 SE), although there is some intermingling of genotypes. At the site (10’s m) and meadow location (km) scale, we found higher levels of genotypic diversity (R (sites) = 0.79 ± 0.04 SE; R (Locations) = 0.78 ± 0.04 SE). We found some sharing of genotypes between sites within meadows, but no sharing of genotypes between meadow locations. We also detected a high level of genetic structuring between meadow locations (F ST = 0.278). Taken together, our results indicate that both sexual and asexual reproductions are important in maintaining meadows of Z. muelleri. The dominant mechanism of asexual reproduction appears to occur via localized rhizome extension, although the sharing of a limited number of genotypes over the scale of 10’s of meters could also result from the localized dispersal and recruitment of fragments. The large number of unique genotypes at the meadow scale indicates that sexual reproduction is important in maintaining these populations, while the high level of genetic structuring suggests little gene flow and connectivity between our study sites. These results imply that recovery from disturbances will occur through both sexual and asexual regeneration, but the limited connectivity at the landscape scale implies that recovery at meadow-scale losses is likely to be limited.

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

Similar content being viewed by others

References

  • Alberto F, Gouveia L, Arnaud-Haond S, Perez-Llorens JL, Duarte CM, Serrao 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, 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 

  • Arnaud-Haond S, Marba N, Diaz-Almela E, Serrao EA, Duarte CM (2010) comparative analysis of stability-genetic diversity in seagrass (Posidonia oceanica) meadows yields unexpected results. Estuaries Coasts 33:878–889

    Article  Google Scholar 

  • 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

    Article  CAS  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, Hily C, Arnaud-Haond S (2014) Scaling of processes shaping the clonal dynamics and genetic mosaic of seagrasses through temporal genetic monitoring. Heredity 112:114–121

    Article  CAS  Google Scholar 

  • Campbell ML (2003) Recruitment and colonisation of vegetative fragments of Posidonia australis and Posidonia coriacea. Aquat Bot 76:175–184

    Article  Google Scholar 

  • Di Carlo G, Badalamenti F, Jensen AC, Koch EW, Riggio S (2005) Colonisation process of vegetative fragments of Posidonia oceanica (L.) Delile on rubble mounds. Mar Biol 147:1261–1270

    Article  Google Scholar 

  • Dorken ME, Eckert CG (2001) Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). J Ecol 89:339–350

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ehlers A, Worm B, Reusch TBH (2008) Importance of genetic diversity in eelgrass Zostera marina for its resilience to global warming. Mar Ecol Prog Ser 355:1–7

    Article  Google Scholar 

  • Eriksson O (1989) Seedling dynamics and life histories in clonal plants. Oikos 55:231–238

    Article  Google Scholar 

  • Eriksson O (1993) Dynamics of genets in clonal plants. Trends Ecol Evol 8:313–316

    Article  CAS  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 14:2611–2620

    Article  CAS  Google Scholar 

  • Evans SM, Sinclair EA, Poore AGB, Steinberg PD, Kendrick GA, Vergés A (2014) Genetic diversity in threatened Posidonia australis seagrass meadows. Conserv Genet 15:717–728

    Article  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  Google Scholar 

  • Franssen SU, Gu J, Winters G, Huylmans A-K, Wienpahl I, Sparwel M, Coyer JA, Olsen JL, Reusch TBH, Bornberg-Bauer E (2014) Genome-wide transcriptomic responses of the seagrasses Zostera marina and Nanozostera noltii under a simulated heatwave confirm functional types. Mar Genom 15:65–73

    Article  Google Scholar 

  • Goudet J (2002) FSTAT, a program to estimate and test gene diversities and fixation indices. Institute of Ecology, University of Lausanne, Switzerland. http://www.unil.ch/izea/softwares/fstat.html

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

    Article  Google Scholar 

  • Hall L, Hanisak MD, RW V (2006) Fragments of the seagrasses Halodule wrightii and Halophila johnsonii as potential recruits in Indian River Lagoon, Florida. Mar Ecol Prog Ser 310:109–117

    Article  Google Scholar 

  • Hämmerli A, Reusch TBH (2002) Local adaptation and transplant dominance in genets of the marine clonal plant Zostera marina. Mar Ecol Prog Ser 242:111–118

    Article  Google Scholar 

  • Hämmerli A, Reusch TBH (2003) Genetic neighbourhood of clone structures in eelgrass meadows quantified by spatial autocorrelation of microsatellite markers. Heredity 91:448–455

    Article  Google Scholar 

  • Heck KL, Valentine JF (2006) Plant–herbivore interactions in seagrass meadows. J Exp Mar Biol Ecol 330:420–436

    Article  Google Scholar 

  • Hellberg ME (2009) Gene flow and isolation among populations of marine animals. Annu Rev Ecol Syst 40:291–310

    Article  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332

    Article  Google Scholar 

  • Hughes AR, Stachowicz JJ (2004) Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc Natl Acad Sci USA 101:8998–9002

    Article  CAS  Google Scholar 

  • Hughes AR, Stachowicz JJ (2011) Seagrass genotypic diversity increases disturbance response via complementarity and dominance. J Ecol 99:445–453

    Google Scholar 

  • Hughes AR, Best RJ, Stachowicz JJ (2010) Genotypic diversity and grazer identity interactively influence seagrass and grazer biomass. Mar Ecol Prog Ser 403:43–51

    Article  Google Scholar 

  • Jenkins GP, May HMA, Wheatley MJ, Holloway MG (1997) Comparison of fish assemblages associated with seagrass and adjacent unvegetated habitats of Port Phillip Bay and Corner Inlet, Victoria, Australia, with emphasis on commercial species. Estuar Coast Shelf S 44:569–588

    Article  Google Scholar 

  • Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance. http://ibdws.sdsu.edu/

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

    Article  Google Scholar 

  • Jones TC, Gemmill CEC, Pilditch CA (2008) Genetic variability of New Zealand seagrass (Zostera muelleri) assessed at multiple spatial scales. Aquat Bot 88:39–46

    Article  Google Scholar 

  • Kamel SJ, Hughes AR, Grosberg RK, Stachowicz JJ (2012) Fine-scale genetic structure and relatedness in the eelgrass Zostera marina. Mar Ecol Prog Ser 447:127–137

    Article  Google Scholar 

  • Larkum AWD, Orth RJ, Duarte AC (2006) Seagrasses: biology, ecology and conservation. Springer, Dordrecht, The Netherlands

  • Macreadie PI, York PH, Sherman CDH (2014) Resilience of Zostera muelleri seagrass to small-scale disturbances: the relative importance of asexual versus sexual recovery. Ecol Evol 4:450–461

    Article  Google Scholar 

  • Massa SI, Paulino CM, Serrao EA, Duarte CM, Arnaud-Haond S (2013) Entangled effects of allelic and clonal (genotypic) richness in the resistance and resilience of experimental populations of the seagrass Zostera noltii to diatom invasion. BMC Ecol 13:39. doi:10.1186/1472-6785-1113-1139

    Article  Google Scholar 

  • Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794

    Article  Google Scholar 

  • Nei M (1972) Genetic distance between populations. Am Nat 106:283–292

    Article  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  Google Scholar 

  • Oetjen K, Reusch TBH (2007) Genome scans detect consistent divergent selection among subtidal vs. intertidal populations of the marine angiosperm Zostera marina. Mol Ecol 16:5156–5157

    Article  Google Scholar 

  • Olsen JL, Stam WT, Coyer JA, Reusch TBH, Billingham M, Bostrom C, Calvert E, Christie H, Granger S, La Lumiere R, Milchakova N, Oudot-Le Secq MP, Procaccini G, Sanjabi B, Serrao E, Veldsink J, Widdicombe S, Wyllie-Echeverria S (2004) North Atlantic phylogeography and large-scale population differentiation of the seagrass Zostera marina L. Mol Ecol 13:1923–1941

    Article  CAS  Google Scholar 

  • Ort BS, Cohen CS, Boyer KE, Wyllie-Echeverria S (2012) Population structure and genetic diversity among eelgrass (Zostera marina) beds and depths in San Francisco Bay. J Hered 103:533–546

    Article  Google Scholar 

  • Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL, Hughes AR, Kendrick GA, Kenworthy WJ, Olyarnik S, Short FT, Waycott M, Williams SL (2006) A global crisis for seagrass ecosystems. Bioscience 56:987–996

    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  Google Scholar 

  • Pan J, Price J (2001) Fitness and evolution in clonal plants: the impact of clonal growth. Evol Ecol 15:583–600

    Article  Google Scholar 

  • Peakall R, Smouse P (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    Article  CAS  Google Scholar 

  • Peterson BJ, Bricker E, Brisbin SJ, Furman BT, Stubler AD, Carroll JM, Berry DL, Gobler CJ, Calladine A, Waycott M (2013) Genetic diversity and gene flow in Zostera marina populations surrounding Long Island, New York, USA: no evidence of inbreeding, genetic degradation or population isolation. Aquat Bot 110:61–66

    Article  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  Google Scholar 

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

    CAS  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201

    Article  CAS  Google Scholar 

  • Reusch TBH (2002) Microsatellites reveal high population connectivity in eelgrass (Zostera marina) in two contrasting coastal areas. Limnol Oceanogr 47:78–85

    Article  Google Scholar 

  • Reusch TBH, Hughes AR (2006) The emerging role of genetic diversity for ecosystem functioning: estuarine macrophytes as models. Estuaries Coasts 29:159–164

    Article  Google Scholar 

  • Reusch TBH, Ehlers A, Hämmerli A, Worm B (2005) Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc Natl Acad Sci USA 102:2826–2831

    Article  CAS  Google Scholar 

  • Reynolds LK, McGlathery KJ, Waycott M (2012) Genetic diversity enhances restoration success by augmenting ecosystem services. Plos One 7:e38397. doi:10.1371/journal.pone.0038397

    Article  CAS  Google Scholar 

  • Reynolds LK, Waycott M, McGlathery KJ (2013) Restoration recovers population structure and landscape genetic connectivity in a dispersal-limited ecosystem. J Ecol 101:1288–1297

    Article  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ruckelshaus MH (1998) Spatial scale of genetic structure and an indirect estimate of gene flow in eelgrass, Zostera marina. Evolution 52:330–343

    Article  Google Scholar 

  • Sherman CDH, Ayre DJ (2008) Fine-scale adaptation in a clonal sea anemone. Evolution 62:1373–1380

    Article  Google Scholar 

  • Sherman CDH, Hunt A, Ayre DJ (2008) Is life history a barrier to dispersal? Contrasting patterns of genetic differentiation along an oceanographically complex coast. Biol J Linn Soc 95:106–116

    Article  Google Scholar 

  • Sherman CDH, Stanley AM, Keough MJ, Gardner MG, Macreadie PI (2012) Development of twenty-three novel microsatellite markers for the seagrass, Zostera muelleri from Australia. Conserv Genet Resour 4:689–693

    Article  Google Scholar 

  • Short F, Carruthers T, Dennison W, Waycott M (2007) Global seagrass distribution and diversity: a bioregional model. J Exp Mar Biol Ecol 350:3–20

    Article  Google Scholar 

  • Sokal RR (1979) Testing statistical significance of geographic variation patterns. Syst Zool 28:227–231

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry: the principles and practice of statistics in biological research, 2nd edn. Freeman, San Francisco

  • Thomson AG, York P, Smith T, Sherman CDH, Booth D, Keough M, Ross DJ, Macreadie P (2015) Seagrass viviparous propagules as a potential long-distance dispersal mechanism. Estuar Coasts 38:927–940

    Article  Google Scholar 

  • Vallejo-Marín M, Dorken ME, Barrett SCH (2010) The ecological and evolutionary consequences of clonality for plant mating. Annu Rev Ecol Syst 41:193–213

    Article  Google Scholar 

  • Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256

    Article  CAS  Google Scholar 

  • Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Fourqurean JW, Heck KL, Hughes AR, Kendrick GA, Kenworthy WJ, Short FT, Williams SL (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc Natl Acad Sci USA 106:12377–12381

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • York PH, Gruber RK, Hill R, Ralph PJ, Booth DJ, Macreadie PI (2013) Physiological and morphological responses of the temperate seagrass Zostera muelleri to multiple stressors: investigating the interactive effects of light and temperature. PLoS ONE 8:e76377

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank D. Poulos and B. McCarthy for their assistance with data collection, and Anna Stanley for helping to process genetic samples. This study was financially supported by a UTS Early Career Researcher Grant, a Paddy Pallin Science Grant, an ARC DECRA Fellowship (DE130101084), and funding from the Centre for Integrative Ecology, Deakin University.

Author information

Authors and Affiliations

  1. Centre for Integrative Ecology (Waurn Ponds Campus), School of Life and Environmental Sciences, Deakin University, 75 Pigdons Road, Locked Bag 20000, Geelong, VIC, 3220, Australia

    Craig D. H. Sherman, Paul H. York, Timothy M. Smith & Peter I. Macreadie

  2. Centre for Tropical Water and Aquatic Ecosystem Research (TropWATER), James Cook University, PO Box 6811, Cairns, QLD, 4870, Australia

    Paul H. York

  3. Plant Functional Biology and Climate Change Cluster (C3), School of the Environment, University of Technology Sydney, Sydney, NSW, 2007, Australia

    Peter I. Macreadie

Authors
  1. Craig D. H. Sherman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paul H. York
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Timothy M. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Peter I. Macreadie
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Craig D. H. Sherman.

Additional information

Responsible Editor: T. Reusch.

Reviewed by Undisclosed experts.

Data archiving All data used in the analyses to create the figures and tables are available via the Pangaea Digital Repository: PDI-11779.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 186 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sherman, C.D.H., York, P.H., Smith, T.M. et al. Fine-scale patterns of genetic variation in a widespread clonal seagrass species. Mar Biol 163, 82 (2016). https://doi.org/10.1007/s00227-016-2861-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-016-2861-7

Keywords

Search

Navigation