Advertisement

Plant Ecology

, Volume 213, Issue 7, pp 1105–1115 | Cite as

Measuring genetic diversity in ecological studies

  • Meghan L. AvolioEmail author
  • Jeremy M. Beaulieu
  • Eugenia Y. Y. Lo
  • Melinda D. Smith
Article

Abstract

There is an increasing interest in how genetic diversity may correlate with and influence community and ecosystem properties. Genetic diversity can be defined in multiple ways, and currently lacking in ecology is a consensus on how to measure genetic diversity. Here, we examine two broad classes of genetic diversity: genotype-based and genome-based measures. Genotype-based measures, such as genotypic richness, are more commonly used in ecological studies, and often it is assumed that as genotypic diversity increases, genomic diversity (the number of genetic polymorphisms and/or genomic dissimilarity among individuals) also increases. However, this assumption is rarely assessed. We tested this assumption by investigating correlations between genotype- and genome-based measures of diversity using two plant population genetic datasets: one observational with data collected at Konza Prairie, KS, and the other based on simulated populations with five levels of genotypic richness, a typical design of genetic diversity experiments. We found conflicting results for both datasets; we found a mismatch between genotypic and genomic diversity measures for the field data, but not the simulated data. Last, we tested the consequences of this mismatch and found that correlations between genetic diversity and community/ecosystem properties depended on metric used. Ultimately, we argue that genome-based measures should be included in future studies alongside genotypic-based measures because they capture a greater spectrum of genetic differences among individuals.

Keywords

Community diversity Ecosystem function Genome diversity Phenotype SGDC 

Notes

Acknowledgments

This research was supported by the USDA CSREES Ecosystem Studies Program, and the US Department of Energy’s Program for Ecosystem Research (#DE-FG02-04ER63892) to MDS. We thank Erem Kazancıoğlu for his assistance with the simulations. We also want to thank M. Vellend, J. Oliver, D. Post, C. Chang, J. Weis, T. Hanley, two anonymous reviewers and members of D. Post’s and M. Smith’s laboratories for their insightful comments and discussion of the manuscript.

Supplementary material

11258_2012_69_MOESM1_ESM.doc (586 kb)
Supplementary material 1 (DOC 586 kb)

References

  1. Arnaud-Haond S, Duarte CM, Alberto F, Serrao EA (2007) Standardizing methods to address clonality in population studies. Mol Ecol 16:5115–5139PubMedCrossRefGoogle Scholar
  2. 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. Estuar Coasts 33:878–889CrossRefGoogle Scholar
  3. Avolio ML, Chang CC, Smith MD (2011) Assessing fine-scale genotypic structure of a dominant species in native grasslands. Am Midl Nat 165:211–224CrossRefGoogle Scholar
  4. Avolio ML, Beaulieu JM, Smith MD (in revision) Genetic diversity of a dominant C4 grass is altered with increased precipitation variability. OecologiaGoogle Scholar
  5. Bailey JK, Schweitzer JA, Ubeda F, Koricheva J, LeRoy CJ, Madritch MD, Rehill BJ, Bangert RK, Fischer DG, Allan GJ, Whitham TG (2009) From genes to ecosystems: a synthesis of the effects of plant genetic factors across levels of organization. Philos Trans R Soc B 364:1607–1616CrossRefGoogle Scholar
  6. Bangert RK, Turek RJ, Rehill B, Wimp GM, Schweitzer JA, Allan GJ, Bailey JK, Martinsen GD, Keim P, Lindroth RL, Whitham TG (2006) A genetic similarity rule determines arthropod community structure. Mol Ecol 15:1379–1391PubMedCrossRefGoogle Scholar
  7. Benson EJ, Hartnett DC (2006) The role of seed and vegetative reproduction in plant recruitment and demography in tallgrass prairie. Plant Ecol 187:163–177CrossRefGoogle Scholar
  8. Cadotte MW, Cardinale BJ, Oakley TH (2008) Evolutionary history and the effect of biodiversity on plant productivity. Proc Natl Acad Sci USA 105:17012–17017PubMedCrossRefGoogle Scholar
  9. Cadotte MW, Hamilton MA, Murray BR (2009) Phylogenetic relatedness and plant invader success across two spatial scales. Divers Distrib 15:481–488CrossRefGoogle Scholar
  10. Chang CC, Smith MD (2012) Invasion of an intact plant community: the role of population versus community level diversity. Oecologia 168:1091–1102PubMedCrossRefGoogle Scholar
  11. Cmokrak P, Merila J (2002) Genetic population divergence: markers and traits. Trends Ecol Evol 17:501Google Scholar
  12. Crutsinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC, Sanders NJ (2006) Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313:966–968PubMedCrossRefGoogle Scholar
  13. Crutsinger GM, Souza L, Sanders NJ (2008) Intraspecific diversity and dominant genotypes resist plant invasions. Ecol Lett 11:16–23PubMedGoogle Scholar
  14. Dubcovsky J, Dvorak J (2007) Genome plasticity a key factor in the success of polyploid wheat under domestication. Science 318:393Google Scholar
  15. 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 355:1–7CrossRefGoogle Scholar
  16. Ellstrand NC, Roose ML (1987) Patterns of genotypic diversity in clonal plant-species. Am J Bot 74:123–131CrossRefGoogle Scholar
  17. Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10CrossRefGoogle Scholar
  18. Felsenstein J (1985) Confidence-limits on phylogenies—an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  19. Gonzalez-Perez MA, Lledo MD, Lexer C, Fay M, Marrero M, Banares-Baudet A, Carque E, Sosa PA (2009) Genetic diversity and differentiation in natural and reintroduced populations of Bencomia exstipulata and comparisons with B-caudata (Rosaceae) in the Canary Islands: an analysis using microsatellites. Bot J Linn Soc 160:429–441CrossRefGoogle Scholar
  20. Gornall RJ (1999) Population genetic structure in agamospermous plants. In: Hollingsworth PM, Bateman RM, Gornall RJ (eds) Molecular systematics and plant evolution. Taylor and Francis, London, pp 118–138CrossRefGoogle Scholar
  21. Hughes AR, Stachowicz JJ (2004) Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc Natl Acad Sci USA 101:8998–9002PubMedCrossRefGoogle Scholar
  22. Hughes AR, Stachowicz JJ (2009) Ecological impacts of genotypic diversity in the clonal seagrass Zostera marina. Ecology 90:1412–1419PubMedCrossRefGoogle Scholar
  23. Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623PubMedCrossRefGoogle Scholar
  24. Huston MA (1997) Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 110:449–460CrossRefGoogle Scholar
  25. Johnson MTJ, Lajeunesse MJ, Agrawal AA (2006) Additive and interactive effects of plant genotypic diversity on arthropod communities and plant fitness. Ecol Lett 9:24–34PubMedGoogle Scholar
  26. Jousset A, Schmid B, Scheu S, Eisenhauer N (2011) Genotypic richness and dissimilarity opposingly affect ecosystem functioning. Ecol Lett 14:537–545PubMedCrossRefGoogle Scholar
  27. Jump AS, Hunt JM, Martinez-Izquierdo JA, Penuelas J (2006) Natural selection and climate change: temperature-linked spatial and temporal trends in gene frequency in Fagus sylvatica. Mol Ecol 15:3469–3480PubMedCrossRefGoogle Scholar
  28. Keeler KH (2004) Impact of intraspecific polyploidy in Andropogon gerardii (Poaceae) populations. Am Midl Nat 152:63–74CrossRefGoogle Scholar
  29. Kembel S, Ackerly D, Blomberg S, Cowan P, Helmus M, Morlon H, Webb CO (2009) Picante: R tools for integrating phlogenies and ecology. R package version 05-3. Harvard University, CambridgeGoogle Scholar
  30. Kloda JM, Dean PDG, Maddren C, MacDonald DW, Mayes S (2008) Using principle component analysis to compare genetic diversity across polyploidy levels within plant complexes: an example from British Restharrows (Ononis spinosa and Ononis repens). Heredity 100:253–260PubMedCrossRefGoogle Scholar
  31. Kosman E, Leonard KJ (2005) Similarity coefficients for molecular markers in studies of genetic relationships between individuals for haploid, diploid, and polyploid species. Mol Ecol 14:415–424PubMedCrossRefGoogle Scholar
  32. Kotowska AM, Cahill JFJ, Keddie BA (2010) Plant genetic diversity yields increased plant productivity and herbivore performance. J Ecol 98:237–245CrossRefGoogle Scholar
  33. Lauenroth WK, Adler PB (2008) Demography of perennial grassland plants: survival, life expectancy and life span. J Ecol 96:1023–1032CrossRefGoogle Scholar
  34. Legendre P, Legendre L (1998) Numerical ecology, 2nd edn. Elvisier, AmsterdamGoogle Scholar
  35. Leinonen T, O’Hara RB, Cano JM, Merila J (2007) Comparative studies of quantitative trait and neutral marker divergence: a meta-analysis. J Evol Biol 21:1–17PubMedGoogle Scholar
  36. Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76PubMedCrossRefGoogle Scholar
  37. McLellan AJDP, Kaltz O, Schmid B (1997) Structure and analysis of phenotypic and genetic variation in clonal plants. In: de Kroon H, Van Groenendael JM (eds) The ecology and evolution of clonal plants. Backhuys, Leiden, pp 185–210Google Scholar
  38. Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794CrossRefGoogle Scholar
  39. Merila J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. J Evol Biol 14:892–903CrossRefGoogle Scholar
  40. Meudt HM, Clarke AC (2007) Almost forgotten or latest practice? AFLP applications, analyses and advances. Trends Plant Sci 12:106–117PubMedCrossRefGoogle Scholar
  41. Munzbergova Z, Skalova H, Hadincova V (2009) Genetic diversity affects productivity in early but not late stages of stand development. Basic Appl Ecol 10:411–419CrossRefGoogle Scholar
  42. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedGoogle Scholar
  43. Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson GL, Stevens HH (2012) vegan: Community ecology package. R package version 111-4. Willey, New YorkGoogle Scholar
  44. Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103PubMedGoogle Scholar
  45. Reusch TBH, Bostrom C (2011) Widespread genetic mosaicism in the marine angiosperm Zostera marina is correlated with clonal reproduction. Evol Ecol 25:899–913CrossRefGoogle Scholar
  46. Reusch TBH, Ehlers A, Hammerli A, Worm B (2005) Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc Natl Acad Sci USA 102:2826–2831PubMedCrossRefGoogle Scholar
  47. Rogers JS (1972) Measures of genetic similarity and genetic distance. Studies in genetics VII. University of Texas, Dallas, pp 145–153Google Scholar
  48. Schweitzer JA, Bailey JK, Hart SC, Whitham TG (2005) Nonadditive effects of mixing cottonwood genotypes on litter decomposition and nutrient dynamics. Ecology 86:2834–2840CrossRefGoogle Scholar
  49. Smith MD, Knapp AK (2003) Dominant species maintain ecosystem function with non-random species loss. Ecol Lett 6:509–517CrossRefGoogle Scholar
  50. Song KM, Lu P, Tang KL, Osborn TC (1995) Rapid genome change in synthetic polyploids of brassica and its implications for polyploid evolution. Proc Natl Acad Sci USA 92:7719–7723PubMedCrossRefGoogle Scholar
  51. Tilman D, Lehman CL, Thomson KT (1997) Plant diversity and ecosystem productivity: theoretical considerations. Proc Natl Acad Sci USA 94:1857–1861PubMedCrossRefGoogle Scholar
  52. Vekemans X (2002) AFLP-SURV, 1.0 edn. Laboratoire de Génétique et Ecologie Végétale, Université Libre de Bruxelles, BelgiumGoogle Scholar
  53. Vellend M (2005) Species diversity and genetic diversity: parallel processes and correlated patterns. Am Nat 166:199–215PubMedCrossRefGoogle Scholar
  54. Vellend M (2006) The consequences of genetic diversity in competitive communities. Ecology 87:304–311PubMedCrossRefGoogle Scholar
  55. Vellend M (2008) Effects of diversity on diversity: consequences of competition and facilitation. Oikos 117:1075–1085CrossRefGoogle Scholar
  56. Vellend M, Geber MA (2005) Connections between species diversity and genetic diversity. Ecol Lett 8:767–781CrossRefGoogle Scholar
  57. Vellend M, Drummond EBM, Tomimatsu H (2010) Effects of genotype identity and diversity on the invasiveness and invisibility of plant populations. Oecologia 162:371–381PubMedCrossRefGoogle Scholar
  58. Weaver JE (1954) North American Prairie. Johnson, LincolnGoogle Scholar
  59. Webb CO (2000) Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. Am Nat 156:145–155PubMedCrossRefGoogle Scholar
  60. Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505CrossRefGoogle Scholar
  61. Weltzin JF, Muth NZ, Von Holle B, Cole PG (2003) Genetic diversity and invisibility: a test using a model system with a novel experimental design. Oikos 103:505–518CrossRefGoogle Scholar
  62. Widen B, Cronberg N, Widen M (1994) Genotypic diversity, molecular markers and spatial-distribution of genets in clonal plants, a literature survey. Folia Geobot Phytotaxon 29:245–263CrossRefGoogle Scholar
  63. Wimp GM, Young WP, Woolbright SA, Martinsen GD, Keim P, Whitham TG (2004) Conserving plant genetic diversity for dependent animal communities. Ecol Lett 7:776–780CrossRefGoogle Scholar
  64. Yang WH, Glover BJ, Rao GY, Yang J (2006) Molecular evidence for multiple polyploidization and lineage recombination in the Chrysanthemum indicum polyploid complex (Asteraceae). New Phytol 171:875–886PubMedCrossRefGoogle Scholar
  65. Yeh FC, Boyle TJB (1999) Popgene version 1.31. Microsoft window-based freeware for population analysis. University of Alberta and Centre for International Forestry Research, EdmontonGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Meghan L. Avolio
    • 1
    Email author
  • Jeremy M. Beaulieu
    • 1
  • Eugenia Y. Y. Lo
    • 1
  • Melinda D. Smith
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyYale UniversityNew HavenUSA

Personalised recommendations