Adaptive vs. neutral genetic diversity: implications for landscape genetics Research Article Received: 23 February 2005 Accepted: 05 November 2005 DOI:
Cite this article as: Holderegger, R., Kamm, U. & Gugerli, F. Landscape Ecol (2006) 21: 797. doi:10.1007/s10980-005-5245-9 Abstract
Genetic diversity is important for the maintenance of the viability and the evolutionary or adaptive potential of populations and species. However, there are two principal types of genetic diversity: adaptive and neutral – a fact widely neglected by non-specialists. We introduce these two types of genetic diversity and critically point to their potential uses and misuses in population or landscape genetic studies. First, most molecular-genetic laboratory techniques analyse neutral genetic variation. This means that the gene variants detected do not have any direct effect on fitness. This type of genetic variation is thus selectively neutral and tells us nothing about the adaptive or evolutionary potential of a population or a species. Nevertheless, neutral genetic markers have great potential for investigating processes such as gene flow, migration or dispersal. Hence, they allow us to empirically test the functional relevance of spatial indices such as connectivity used in landscape ecology. Second, adaptive genetic variation, i.e. genetic variation under natural selection, is analysed in quantitative genetic experiments under controlled and uniform environmental conditions. Unfortunately, the genetic variation (i.e. heritability) and population differentiation at quantitative, adaptive traits is not directly linked with neutral genetic diversity or differentiation. Thus, neutral genetic data cannot serve as a surrogate of adaptive genetic data. In summary, neutral genetic diversity is well suited for the study of processes within landscapes such as gene flow, while the evolutionary or adaptive potential of populations or species has to be assessed in quantitative genetic experiments. Landscape ecologists have to mind these differences between neutral and adaptive genetic variation when interpreting the results of landscape genetic studies.
Keywords Adaptive genetic variation Heritability Landscape genetics Neutral genetic variation Population differentiation Quantitative genetics References
Antolin M.F., Savage L.T. and Eisen R.J. 2006. Landscape features influence genetic structure of Black-Tailed Prairie Dogs (
). Landsc. Ecol. 21: 867–875.
Google Scholar Conner, J.K., Hartl, D.L. 2004A Primer to Ecological Genetics Sinauer Sunderland, Massachusetts, USA Google Scholar Darwin, C. 1859The Origin of Species by Means of Natural Selection John Murray London, UK Google Scholar Falconer, D.S., MacKay, T.F.C. 1996Introduction to Quantitative Genetics Longman Harlow, UK Google Scholar Frankham, R., Ballou, J.D., Briscoe, D.A. 2004A Primer to Conservation Genetics Cambridge University Press Cambridge, UK Google Scholar Futuyma, D.J. 2005Evolution Sinauer Sunderland, Massachusetts, USA Google Scholar Godoy, J.A., Jordano, P. 2001 Seed dispersal by animals: exact identification of source trees with endocarp DNA microsatellites Mol. Ecol. 10 2275 2283 PubMed CrossRef Google Scholar Hartl, D.L., Clark, A.G. 1997Principles of Population Genetics Sinauer Sunderland, Massachusetts, USA Google Scholar Holderegger, R., Gugerli, F., Scheidegger, C., Taberlet, P. In press Integrating genetics with landscape ecology to infer spatio-temporal processes Kienast, F. Gosh, R. Wildi, O. eds. A Changing World: Challenges for Landscape Research Springer Dordrecht, NL Google Scholar Jackson, R.B., Linder, C.R., Lynch, M., Puruganen, M., Sommerville, S., Thayer, S.S. 2002 Linking molecular insight and ecological research Trends Ecol. Evol. 17 409 414 CrossRef Google Scholar Kimura, M. 1983The Neutral Theory of Molecular Evolution Cambridge University Press Cambridge, UK Google Scholar Kremer, A., Kleinschmit, J., Cottrell, J., et al. 2002 Is there a correlation between chloroplastic and nuclear divergenceor what are the roles of history and selection on genetic diversity in European oaks For. Ecol. Manage. 156 75 87 CrossRef Google Scholar Latta, R.G. 2003 Gene flow, adaptive population divergence and comparative population structure across loci New Phytol. 161 51 58 CrossRef Google Scholar Latta, R.G. 2006 Using comparisons among different classes of genetic markers to infer spatial processes Landscape Ecol. 21 809 820 Google Scholar Li, W.-H., Graur, D. 1991Fundamentals of Molecular Evolution Sinauer Sunderland, Massachusetts, USA Google Scholar Li, H., Wu, J. 2004 Use and misuse of landscape indices Landscape Ecol. 19 389 399 CrossRef Google Scholar Lowe, A., Harris, S., Ashton, P. 2004Ecological Genetics. Design, Analysis and Application Blackwell Oxford, UK Google Scholar Manel, S., Schwartz, M.K., Luikart, G., Taberlet, P. 2003 Landscape genetics: combining landscape ecology and population genetics Trends Ecol. Evol. 18 189 197 CrossRef Google Scholar McKay, J.K., Latta, R.G. 2002 Adaptive population divergence: markers, QTL and traits Trends Ecol. Evol. 17 285 291 CrossRef Google Scholar Merilä, J., Crnokrak, P. 2001 Comparison of genetic differentiation at marker loci and quantitative traits J. Evol. Biol. 14 892 903 CrossRef Google Scholar O’Meally, D., Colgan, D.J. 2005 Genetic ranking for biological conservation using information from multiple species Biol. Conserv. 122 395 407 CrossRef Google Scholar
Pannell J.R. and Dorken M.E. 2006. Colonisation as a common denominator in plant metapopulations and range expansions: effects on genetic diversity and sexual systems. Landscape Ecol. 21: 837–847.
Google Scholar Pearman, P.B. 2001 Conservation value of independently evolving units: sacred cow or testable hypothesis? Conserv. Biol. 15 780 783 CrossRef Google Scholar Pearse, D.E., Crandall, K.A. 2004 Beyond F ST: analysis of population genetic data for conservation Conserv. Genet. 5 585 602 CrossRef Google Scholar Petit, R., Csaikl, U.M., Bordács, S., et al. 2002 Chloroplast DNA variation in European white oaks. Phylogeography and patterns of diversity based on data from over 2600 populations For. Ecol. Manage. 156 5 26 CrossRef Google Scholar Reed, D.H., Frankham, R. 2001 How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis Evolution 55 1095 1103 PubMed CrossRef Google Scholar Reed, D.H., Frankham, R. 2002 Correlation between fitness and genetic diversity Conserv. Biol. 17 230 237 CrossRef Google Scholar Savolainen, O., Bokma, F., García-Gil, R., Komulainen, P., Repo, T. 2004 Genetic variation in cessation of growth and frost hardiness and consequences for adaptation of Pinus sylvestris to climatic changes For. Ecol. Manage. 197 79 89 CrossRef Google Scholar Schwaegerle, K.E.K., Garbutt, K., Bazzaz, F.A. 1986 Differentiation among nine populations of Phlox. I. Electrophoretic and quantitative variation Evolution 40 506 517 CrossRef Google Scholar Slatkin, M. 2005 Seeing ghosts: the effect of unsampled populations on migration rates estimated for sampled populations Mol. Ecol. 14 67 73 PubMed CrossRef Google Scholar Smouse, P.E., Sork, V.L. 2004 Measuring pollen flow in forest trees: an exposition of alternative approaches For. Ecol. Manage. 197 21 38 CrossRef Google Scholar Sork, V.L., Smouse, P.E. 2006 Landscape gene flow in contemporary tree populations Landscape Ecol. 21 821 836 Google Scholar Turner, M.G., Gardner, R.H., O’Neill, R.V. 2001Landscape Ecology in Theory and Practice Springer New York, USA Google Scholar Vandewoestijne, S., Baquette, M. 2004 Demographic versus genetic dispersal measures Popul. Ecol. 46 281 285 CrossRef Google Scholar
Wagner H., Werth S., Kalwij J.M., Bolli J. and Scheidegger C. 2006. Modelling the persistence and genetic structure of an epiphytic lichen. Landscape Ecol. 21: 849–865.
Google Scholar Widmer, A., Lexer, C. 2001 Glacial refugia: sanctuaries for allelic richness, but not for gene diversity Trends Ecol. Evol. 16 267 269 PubMed CrossRef Google Scholar Wiens, J.A. 1989 Spatial scaling in ecology Funct. Ecol. 3 385 397 CrossRef Google Scholar Wright, S. 1951 The genetical structure of populations Ann. Eugen. 15 323 354 Google Scholar Wu, J., Hobbs, R. 2002 Key issues and research priorities in landscape ecology: an idiosyncratic synthesis Landscape Ecol. 17 355 365 CrossRef Google Scholar