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.
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References
Arnaud-Haond S, Duarte CM, Alberto F, Serrao EA (2007) Standardizing methods to address clonality in population studies. Mol Ecol 16:5115–5139
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 33:878–889
Avolio ML, Chang CC, Smith MD (2011) Assessing fine-scale genotypic structure of a dominant species in native grasslands. Am Midl Nat 165:211–224
Avolio ML, Beaulieu JM, Smith MD (in revision) Genetic diversity of a dominant C4 grass is altered with increased precipitation variability. Oecologia
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 364:1607–1616
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 15:1379–1391
Benson EJ, Hartnett DC (2006) The role of seed and vegetative reproduction in plant recruitment and demography in tallgrass prairie. Plant Ecol 187:163–177
Cadotte MW, Cardinale BJ, Oakley TH (2008) Evolutionary history and the effect of biodiversity on plant productivity. Proc Natl Acad Sci USA 105:17012–17017
Cadotte MW, Hamilton MA, Murray BR (2009) Phylogenetic relatedness and plant invader success across two spatial scales. Divers Distrib 15:481–488
Chang CC, Smith MD (2012) Invasion of an intact plant community: the role of population versus community level diversity. Oecologia 168:1091–1102
Cmokrak P, Merila J (2002) Genetic population divergence: markers and traits. Trends Ecol Evol 17:501
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 313:966–968
Crutsinger GM, Souza L, Sanders NJ (2008) Intraspecific diversity and dominant genotypes resist plant invasions. Ecol Lett 11:16–23
Dubcovsky J, Dvorak J (2007) Genome plasticity a key factor in the success of polyploid wheat under domestication. Science 318:393
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
Ellstrand NC, Roose ML (1987) Patterns of genotypic diversity in clonal plant-species. Am J Bot 74:123–131
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10
Felsenstein J (1985) Confidence-limits on phylogenies—an approach using the bootstrap. Evolution 39:783–791
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 160:429–441
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 118–138
Hughes AR, Stachowicz JJ (2004) Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc Natl Acad Sci USA 101:8998–9002
Hughes AR, Stachowicz JJ (2009) Ecological impacts of genotypic diversity in the clonal seagrass Zostera marina. Ecology 90:1412–1419
Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623
Huston MA (1997) Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 110:449–460
Johnson MTJ, Lajeunesse MJ, Agrawal AA (2006) Additive and interactive effects of plant genotypic diversity on arthropod communities and plant fitness. Ecol Lett 9:24–34
Jousset A, Schmid B, Scheu S, Eisenhauer N (2011) Genotypic richness and dissimilarity opposingly affect ecosystem functioning. Ecol Lett 14:537–545
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 15:3469–3480
Keeler KH (2004) Impact of intraspecific polyploidy in Andropogon gerardii (Poaceae) populations. Am Midl Nat 152:63–74
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, Cambridge
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 100:253–260
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 14:415–424
Kotowska AM, Cahill JFJ, Keddie BA (2010) Plant genetic diversity yields increased plant productivity and herbivore performance. J Ecol 98:237–245
Lauenroth WK, Adler PB (2008) Demography of perennial grassland plants: survival, life expectancy and life span. J Ecol 96:1023–1032
Legendre P, Legendre L (1998) Numerical ecology, 2nd edn. Elvisier, Amsterdam
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 21:1–17
Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76
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 185–210
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
Merila J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. J Evol Biol 14:892–903
Meudt HM, Clarke AC (2007) Almost forgotten or latest practice? AFLP applications, analyses and advances. Trends Plant Sci 12:106–117
Munzbergova Z, Skalova H, Hadincova V (2009) Genetic diversity affects productivity in early but not late stages of stand development. Basic Appl Ecol 10:411–419
Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590
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 York
Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103
Reusch TBH, Bostrom C (2011) Widespread genetic mosaicism in the marine angiosperm Zostera marina is correlated with clonal reproduction. Evol Ecol 25:899–913
Reusch TBH, Ehlers A, Hammerli A, Worm B (2005) Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc Natl Acad Sci USA 102:2826–2831
Rogers JS (1972) Measures of genetic similarity and genetic distance. Studies in genetics VII. University of Texas, Dallas, pp 145–153
Schweitzer JA, Bailey JK, Hart SC, Whitham TG (2005) Nonadditive effects of mixing cottonwood genotypes on litter decomposition and nutrient dynamics. Ecology 86:2834–2840
Smith MD, Knapp AK (2003) Dominant species maintain ecosystem function with non-random species loss. Ecol Lett 6:509–517
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 92:7719–7723
Tilman D, Lehman CL, Thomson KT (1997) Plant diversity and ecosystem productivity: theoretical considerations. Proc Natl Acad Sci USA 94:1857–1861
Vekemans X (2002) AFLP-SURV, 1.0 edn. Laboratoire de Génétique et Ecologie Végétale, Université Libre de Bruxelles, Belgium
Vellend M (2005) Species diversity and genetic diversity: parallel processes and correlated patterns. Am Nat 166:199–215
Vellend M (2006) The consequences of genetic diversity in competitive communities. Ecology 87:304–311
Vellend M (2008) Effects of diversity on diversity: consequences of competition and facilitation. Oikos 117:1075–1085
Vellend M, Geber MA (2005) Connections between species diversity and genetic diversity. Ecol Lett 8:767–781
Vellend M, Drummond EBM, Tomimatsu H (2010) Effects of genotype identity and diversity on the invasiveness and invisibility of plant populations. Oecologia 162:371–381
Weaver JE (1954) North American Prairie. Johnson, Lincoln
Webb CO (2000) Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. Am Nat 156:145–155
Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505
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 103:505–518
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 29:245–263
Wimp GM, Young WP, Woolbright SA, Martinsen GD, Keim P, Whitham TG (2004) Conserving plant genetic diversity for dependent animal communities. Ecol Lett 7:776–780
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 171:875–886
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, Edmonton
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.
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Avolio, M.L., Beaulieu, J.M., Lo, E.Y.Y. et al. Measuring genetic diversity in ecological studies. Plant Ecol 213, 1105–1115 (2012). https://doi.org/10.1007/s11258-012-0069-6
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DOI: https://doi.org/10.1007/s11258-012-0069-6