Causes and consequences of large clonal assemblies in a poplar hybrid zone

Asexual reproduction is a common and fundamental mode of reproduction in plants. Although persistence in adverse conditions underlies most known cases of clonal dominance, proximal genetic drivers remain unclear, in particular for populations dominated by a few large clones. In this study, we studied a clonal population of the riparian tree Populus alba in the Douro river basin (northwestern Iberian Peninsula) where it hybridizes with Populus tremula, a species that grows in highly contrasted ecological conditions. We used 73 nuclear microsatellites to test whether genomic background (species ancestry) is a relevant cause of clonal success, and to assess the evolutionary consequences of clonal dominance by a few genets. Additional genotyping‐by‐sequencing data were produced to estimate the age of the largest clones. We found that a few ancient (over a few thousand years old) and widespread genets dominate the population, both in terms of clone size and number of sexual offspring produced. Interestingly, large clones possessed two genomic regions introgressed from P. tremula, which may have favoured their spread under stressful environmental conditions. At the population level, the spread of large genets was accompanied by an overall ancient (>0.1 Myr) but soft decline of effective population size. Despite this decrease, and the high clonality and dominance of sexual reproduction by large clones, the Douro hybrid zone still displays considerable genetic diversity and low inbreeding. This suggests that even in extreme cases as in the Douro, asexual and sexual dominance of a few large, geographically extended individuals does not threaten population survival.

[1]  F. Malrieu,et al.  Rare sex or out of reach equilibrium? The dynamics of FIS in partially clonal organisms , 2016, BMC Genetics.

[2]  Daniel Wegmann,et al.  Selection against recombinant hybrids maintains reproductive isolation in hybridizing Populus species despite F1 fertility and recurrent gene flow , 2016, Molecular ecology.

[3]  G. Luikart,et al.  Harnessing the power of RADseq for ecological and evolutionary genomics , 2016, Nature Reviews Genetics.

[4]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[5]  Angel Amores,et al.  Stacks: an analysis tool set for population genomics , 2013, Molecular ecology.

[6]  S. González-Martínez,et al.  Extensive Clonal Assemblies in Populus alba and Populus x canescens from the Iberian Peninsula , 2013, Tree Genetics & Genomes.

[7]  S. Castiglione,et al.  Genomic scan for single nucleotide polymorphisms reveals patterns of divergence and gene flow between ecologically divergent species , 2013, Molecular ecology.

[8]  P. Hedrick What is the evidence for heterozygote advantage selection? , 2012, Trends in ecology & evolution.

[9]  B. Heinze,et al.  Recombinant hybrids retain heterozygosity at many loci: new insights into the genomics of reproductive isolation in Populus , 2012, Molecular ecology.

[10]  D. Macaya-Sanz,et al.  The Atlantic–Mediterranean watershed, river basins and glacial history shape the genetic structure of Iberian poplars , 2012, Molecular ecology.

[11]  Faye D. Schilkey,et al.  Genome‐wide association genetics of an adaptive trait in lodgepole pine , 2012, Molecular ecology.

[12]  N. Marbà,et al.  Implications of Extreme Life Span in Clonal Organisms: Millenary Clones in Meadows of the Threatened Seagrass Posidonia oceanica , 2012, PloS one.

[13]  M. Martins-Loução,et al.  Fitness in Narcissus hybrids: low fertility is overcome by early hybrid vigour, absence of exogenous selection and high bulb propagation , 2011 .

[14]  A. Amores,et al.  Stacks: Building and Genotyping Loci De Novo From Short-Read Sequences , 2011, G3: Genes | Genomes | Genetics.

[15]  D. Macaya-Sanz,et al.  Genetic analysis of post-mating reproductive barriers in hybridizing European Populus species , 2011, Heredity.

[16]  R. Vitalis,et al.  Inferring Population Decline and Expansion From Microsatellite Data: A Simulation-Based Evaluation of the Msvar Method , 2011, Genetics.

[17]  M. Vallejo‐Marín,et al.  The Ecological and Evolutionary Consequences of Clonality for Plant Mating , 2010 .

[18]  M. Fay,et al.  Genomic Admixture Analysis in European Populus spp. Reveals Unexpected Patterns of Reproductive Isolation and Mating , 2010, Genetics.

[19]  Xueping Zhou,et al.  A tomato glutaredoxin gene SlGRX1 regulates plant responses to oxidative, drought and salt stresses , 2010, Planta.

[20]  P. Stadler,et al.  Reconstruction of pedigrees in clonal plant populations. , 2010, Theoretical population biology.

[21]  M. van Loo,et al.  Genetic structure and introgression in riparian populations of Populus alba L. , 2010 .

[22]  S. Otto,et al.  Aging in a Long-Lived Clonal Tree , 2010, PLoS biology.

[23]  S. Strauss,et al.  Population substructure in continuous and fragmented stands of Populus trichocarpa , 2010, Heredity.

[24]  O. Jones,et al.  COLONY: a program for parentage and sibship inference from multilocus genotype data , 2010, Molecular ecology resources.

[25]  N. Rouhier Plant glutaredoxins: pivotal players in redox biology and iron-sulphur centre assembly. , 2010, The New phytologist.

[26]  R. Ceulemans,et al.  Genomic regions involved in productivity of two interspecific poplar families in Europe. 2. Biomass production and its relationships with tree architecture and phenology , 2010, Tree Genetics & Genomes.

[27]  E. Muller,et al.  Recent Changes in the Riparian Forest of a Large Regulated Mediterranean River: Implications for Management , 2010, Environmental management.

[28]  H. Bruelheide,et al.  Clonal structure and genetic diversity of three desert phreatophytes. , 2010, American journal of botany.

[29]  E. Muller,et al.  Seed dispersal, germination and early seedling establishment of Populus alba L. under simulated water table declines in different substrates , 2010, Trees.

[30]  N. Ellstrand,et al.  A Pleistocene Clone of Palmer's Oak Persisting in Southern California , 2009, PloS one.

[31]  J. Lundeberg,et al.  Genome-wide profiling of Populus small RNAs , 2009, BMC Genomics.

[32]  D. Charlesworth,et al.  The genetics of inbreeding depression , 2009, Nature Reviews Genetics.

[33]  Peter F. Stadler,et al.  FRANz: reconstruction of wild multi-generation pedigrees , 2009, Bioinform..

[34]  R. Ceulemans,et al.  Genomic regions involved in productivity of two interspecific poplar families in Europe. 1. Stem height, circumference and volume , 2009, Tree Genetics & Genomes.

[35]  S. Castiglione,et al.  The origin of clonal diversity and structure of Populus alba in Sardinia: evidence from nuclear and plastid microsatellite markers. , 2008, Annals of botany.

[36]  K. Ritland,et al.  Can clone size serve as a proxy for clone age?An exploration using microsatellite divergence in Populus tremuloides , 2008, Molecular ecology.

[37]  M. Hooten,et al.  Clonal dynamics in western North American aspen (Populus tremuloides) , 2008, Molecular ecology.

[38]  T. Kawecki Adaptation to Marginal Habitats , 2008 .

[39]  Pär K Ingvarsson,et al.  Multilocus Patterns of Nucleotide Polymorphism and the Demographic History of Populus tremula , 2008, Genetics.

[40]  B. Meyers,et al.  Genome-wide identification of NBS resistance genes in Populus trichocarpa , 2008, Plant Molecular Biology.

[41]  J. Silvertown The Evolutionary Maintenance of Sexual Reproduction: Evidence from the Ecological Distribution of Asexual Reproduction in Clonal Plants , 2008, International Journal of Plant Sciences.

[42]  C. Duarte,et al.  Standardizing methods to address clonality in population studies , 2007, Molecular ecology.

[43]  M. Fay,et al.  Clonality and spatial genetic structure in Populus x canescens and its sympatric backcross parent P. alba in a Central European hybrid zone. , 2007, The New phytologist.

[44]  M. Stephens,et al.  Inference of population structure using multilocus genotype data: dominant markers and null alleles , 2007, Molecular ecology notes.

[45]  M. Plummer,et al.  CODA: convergence diagnosis and output analysis for MCMC , 2006 .

[46]  P. Pulkkinen,et al.  The effect of soil temperature and light on sprouting and rooting of root cuttings of hybrid aspen clones , 2005 .

[47]  F. Balloux,et al.  Tackling the population genetics of clonal and partially clonal organisms. , 2005, Trends in ecology & evolution.

[48]  S. Kalinowski hp-rare 1.0: a computer program for performing rarefaction on measures of allelic richness , 2005 .

[49]  M. Fay,et al.  Barrier to gene flow between two ecologically divergent Populus species, P. alba (white poplar) and P. tremula (European aspen): the role of ecology and life history in gene introgression , 2005, Molecular ecology.

[50]  O. Honnay,et al.  Prolonged clonal growth: escape route or route to extinction? , 2005 .

[51]  A. P. Alberti,et al.  Pleistocene glaciation in Spain , 2004 .

[52]  E. Muller,et al.  Variations in levels of clonality among Populus nigra L. stands of different ages , 2004, Evolutionary Ecology.

[53]  L. Rieseberg,et al.  Candidate gene polymorphisms associated with salt tolerance in wild sunflower hybrids: implications for the origin of Helianthus paradoxus, a diploid hybrid species. , 2003, The New phytologist.

[54]  L. Lehmann,et al.  The population genetics of clonal and partially clonal diploids. , 2003, Genetics.

[55]  M. Stephens,et al.  Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. , 2003, Genetics.

[56]  O. Hardy,et al.  spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels , 2002 .

[57]  Nathaniel Valière gimlet: a computer program for analysing genetic individual identification data , 2002 .

[58]  T. Whitham,et al.  Cottonwood hybrids gain fitness traits of both parents: a mechanism for theirlong-term persistence? , 2002, American journal of botany.

[59]  S. Otto,et al.  Evolution of sex: Resolving the paradox of sex and recombination , 2002, Nature Reviews Genetics.

[60]  W. Rice Evolution of sex: Experimental tests of the adaptive significance of sexual recombination , 2002, Nature Reviews Genetics.

[61]  Mark A. Beaumont,et al.  TESTING FOR GENETIC EVIDENCE OF POPULATION EXPANSION AND CONTRACTION: AN EMPIRICAL ANALYSIS OF MICROSATELLITE DNA VARIATION USING A HIERARCHICAL BAYESIAN MODEL , 2002, Evolution; international journal of organic evolution.

[62]  C. Eckert The loss of sex in clonal plants , 2001, Evolutionary Ecology.

[63]  N. Barsoum Relative contributions of sexual and asexual regeneration strategies in Populus nigra and Salix alba during the first years of establishment on a braided gravel bed river , 2001, Evolutionary Ecology.

[64]  T. Sachs Developmental processes and the evolution of plant clonality , 2001, Evolutionary Ecology.

[65]  Qibin Yu,et al.  Rooting of Hybrid Clones of Populus tremula L. × P. tremuloides Michx. by Stem Cuttings Derived from Micropropagated Plants , 2001 .

[66]  M W Feldman,et al.  Recent common ancestry of human Y chromosomes: evidence from DNA sequence data. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[67]  M. Beaumont Detecting population expansion and decline using microsatellites. , 1999, Genetics.

[68]  L. Rieseberg,et al.  Plant hybridization. , 1998, The New phytologist.

[69]  Jitka Klimešová,et al.  Clonal plant architecture A comparative analysis of form and function , 1997 .

[70]  D. Rubin,et al.  Inference from Iterative Simulation Using Multiple Sequences , 1992 .

[71]  M. Lynch THE GENETIC INTERPRETATION OF INBREEDING DEPRESSION AND OUTBREEDING DEPRESSION , 1991, Evolution; international journal of organic evolution.

[72]  F. C. Vasek CREOSOTE BUSH: LONG‐LIVED CLONES IN THE MOJAVE DESERT , 1980 .

[73]  G. Slavov,et al.  Salient Biological Features, Systematics, and Genetic Variation of Populus , 2010 .

[74]  R. Vaillancourt,et al.  Genetic Evidence that Lomatia tasmanica (Proteaceae) Is an Ancient Clone , 1998 .

[75]  L. Rieseberg,et al.  Tansley review No. 102 plant hybridization , 1998 .