A landscape genetics approach reveals ecological‐based differentiation in populations of holm oak (Quercus ilex L.) at the northern limit of its range

The holm oak plays a relevant role in the functioning of Mediterranean forests. In the area north of Garda Lake, Italian Prealps, holm oak populations are at the northernmost edge of their distribution. Being peripheral, these populations are of particular interest for ecological, evolutionary and conservation studies. Through an explicit individual-based landscape genetics approach, we addressed the following questions: (1) are levels of genetic variation reduced in these marginal populations compared with central populations?; (2) despite the narrow geographical scale, do individual-based analyses have some power to detect genetic differentiation?; (3) do environmental and/or climatic factors exert a role in shaping patterns of genetic variation and differentiation? Through a Bayesian method, we identified three clusters whose genetic variability can be considered to be of the same order as that recorded in central Quercus ilex populations. Although being geographically very close (< 20 km), the differentiation was statistically significant (P < 0.05) with global F st and Φ Pt values of 0.019 and 0.038, respectively. Geography and phylogeography could not be invoked to explain this differentiation. A redundancy discriminant analysis revealed that relevant eco-pedological and climatic features, such as soil depth, aspect, elevation and humidity, were correlated with the observed pattern of differentiation. Toblino was ecologically separated from the other clusters, as it lies on deep soil with subhumid conditions. The differentiation of the Brione–Ranzo–Val Busa cluster appeared to be related to superficial soils and drier conditions, whereas the Nanzone–Padaro cluster was differentiated mainly according to its mid-elevation. Coupling spatial and genetic information on a local scale proved to be effective to investigate the evolutionary and demographic history of peripheral populations. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ••, ••–••.

[1]  Markus Metz,et al.  GRASS GIS: A multi-purpose open source GIS , 2012, Environ. Model. Softw..

[2]  L. Waits,et al.  Landscape genetics: where are we now? , 2010, Molecular ecology.

[3]  J. Goudet FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Updated from Goudet (1995) , 2001 .

[4]  R. Petit,et al.  Detection of hybrids in nature: application to oaks (Quercus suber and Q. ilex) , 2009, Heredity.

[5]  L. Gil,et al.  Nuclear microsatellite markers for the identification of Quercus ilex L. and Q. suber L. hybrids , 2003 .

[6]  Gilles Guillot,et al.  Inference of structure in subdivided populations at low levels of genetic differentiation - the correlated allele frequencies model revisited , 2008, Bioinform..

[7]  B. Gardiner,et al.  Linnean Society of London , 1956, Nature.

[8]  Arnaud Estoup,et al.  Analysing georeferenced population genetics data with Geneland: a new algorithm to deal with null alleles and a friendly graphical user interface , 2008, Bioinform..

[9]  Pierre Taberlet,et al.  Landscape genetics: combining landscape ecology and population genetics , 2003 .

[10]  E. Mayr Populations, Species, and Evolution, An Abridgment of Animal Species and Evolution , 1970 .

[11]  C. R. Rao,et al.  Linear Statistical Inference and its Applications , 1968 .

[12]  Helena Mitasova,et al.  Chapter 17 Geomorphometry in GRASS GIS , 2009 .

[13]  P. Smouse,et al.  genalex 6: genetic analysis in Excel. Population genetic software for teaching and research , 2006 .

[14]  O. Gaggiotti,et al.  INVITED REVIEW: What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity , 2006, Molecular ecology.

[15]  R. Lumaret,et al.  Effect of geographical discontinuity on genetic variation in Quercus ilex L. (holm oak). Evidence from enzyme polymorphism , 1995, Heredity.

[16]  A. Lowe,et al.  A case for incorporating phylogeography and landscape genetics into species distribution modelling approaches to improve climate adaptation and conservation planning , 2010 .

[17]  Calyampudi R. Rao,et al.  Linear statistical inference and its applications , 1965 .

[18]  Markus Neteler,et al.  Open Source GIS: A GRASS GIS Approach , 2007 .

[19]  Duccio Rocchini,et al.  Are landscapes as crisp as we may think , 2007 .

[20]  C. Parmesan Ecological and Evolutionary Responses to Recent Climate Change , 2006 .

[21]  R. Bonal,et al.  Genetic consequences of habitat fragmentation in long-lived tree species: the case of the mediterranean Holm Oak (Quercus ilex, L.). , 2010, The Journal of heredity.

[22]  R. Lumaret,et al.  Reproduction and gene flow in the genus Quercus L , 1993 .

[23]  M. Fortin,et al.  Perspectives on the use of landscape genetics to detect genetic adaptive variation in the field , 2010, Molecular ecology.

[24]  Dylan Keon,et al.  Equations for potential annual direct incident radiation and heat load , 2002 .

[25]  Peter Lesica,et al.  When Are Peripheral Populations Valuable for Conservation , 1995 .

[26]  A. Zuur,et al.  Analysing Ecological Data , 2007 .

[27]  Madhur Anand,et al.  Spatial complexity of ecological communities: Bridging the gap between probabilistic and non-probabilistic uncertainty measures , 2006 .

[28]  H. Howe,et al.  Characterization of highly variable (GA/CT)n microsatellites in the bur oak, Quercus macrocarpa , 1995, Theoretical and Applied Genetics.

[29]  L. Excoffier,et al.  Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. , 1992, Genetics.

[30]  V. Raynal,et al.  Phylogeographical variation of chloroplast DNA in holm oak (Quercus ilex L.) , 2002, Molecular ecology.

[31]  Arnaud Estoup,et al.  A Spatial Statistical Model for Landscape Genetics , 2005, Genetics.

[32]  R. Petit,et al.  Conserving biodiversity under climate change: the rear edge matters. , 2005, Ecology letters.

[33]  A. Iezzoni,et al.  CHLOROPLAST DNA VARIATION IN SOUR CHERRY , 1996 .

[34]  M. Migliaccio,et al.  Sicily represents the Italian reservoir of chloroplast DNA diversity of Quercus ilex L. (Fagaceae) , 2005 .

[35]  H. Carson,et al.  Genetic conditions which promote or retard the formation of species. , 1959, Cold Spring Harbor symposia on quantitative biology.

[36]  J. Pausas,et al.  Rodent acorn selection in a Mediterranean oak landscape , 2007, Ecological Research.

[37]  L. Gil,et al.  Differences in fine-scale genetic structure and dispersal in Quercus ilex L. and Q. suber L.: consequences for regeneration of mediterranean open woods , 2007, Heredity.

[38]  H. Steinkellner,et al.  Identification and characterization of (GA/CT)n- microsatellite loci from Quercus petraea , 1997, Plant Molecular Biology.

[39]  J. Beek,et al.  Developments in Soil Science , 2019, Global Change and Forest Soils.

[40]  R. Lumaret,et al.  Distribution spatiale des génotypes dans une population de chêne vert (Quercus ilex L.), flux génique et régime de reproduction , 1988, Génétique, sélection, évolution.

[41]  F. Vessella,et al.  Multiple genome relationships and a complex biogeographic history in the eastern range of Quercus suber L. (Fagaceae) implied by nuclear and chloroplast DNA variation , 2009 .

[42]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[43]  Marie-Josée Fortin,et al.  Applications of landscape genetics in conservation biology: concepts and challenges , 2010, Conservation Genetics.

[44]  Variation in the genetic structure and reproductive biology of holm oak populations , 1992, Vegetatio.

[45]  A. Estoup,et al.  Microsatellite null alleles and estimation of population differentiation. , 2007, Molecular biology and evolution.