Admixture in European Populus hybrid zones makes feasible the mapping of loci that contribute to reproductive isolation and trait differences

Abstract

The use of admixed human populations to scan the genome for chromosomal segments affecting complex phenotypic traits has proved a powerful analytical tool. However, its potential in other organisms has not yet been evaluated. Here, we use DNA microsatellites to assess the feasibility of this approach in hybrid zones between two members of the 'model tree' genus Populus: Populus alba (white poplar) and Populus tremula (European aspen). We analyzed samples of both species and a Central European hybrid zone (N ¼ 544 chromosomes) for a genome-wide set of 19 polymorphic DNA microsatellites. Our results indicate that allele frequency differentials between the two species are substantial (mean d ¼ 0.61970.067). Background linkage disequilibrium (LD) in samples of the parental gene pools is moderate and should respond to sampling schemes that minimize drift and account for rare alleles. LD in hybrids decays with increasing number of backcross generations as expected from theory and approaches background levels of the parental gene pools in advanced generation backcrosses. Introgression from P. tremula into P. alba varies strongly across marker loci. For several markers, alleles from P. tremula are slightly over-represented relative to neutral expectations, whereas a single locus exhibits evidence of selection against P. tremula genotypes. We interpret our results in terms of the potential for admixture mapping in these two ecologically divergent Populus species, and we validate a modified approach of studying genotypic clines in 'mosaic' hybrid zones. Keywords: hybrid zone; admixture; introgression; linkage disequilibrium; rare alleles; Populus Introduction 'Admixture mapping' as suggested by Chakraborty and Weiss (1988) and Briscoe et al. (1994) utilizes linkage disequilibrium (LD) induced by the mixing of genes from two divergent gene pools. In an outcrossing species and in the absence of confounding population structure, LD will decay with increasing genetic map or chromosomal distance (Lynch and Walsh, 1998), because the chance that stretches of DNA are broken up by recombination becomes greater the further two loci are apart. Admixture will effectively widen the region of a genome that is affected by LD, because recombination will take several/many generations to break up the chromosome blocks derived from each parental population (Briscoe et al., 1994;Chapman and Thompson, 2002). Hence, admixture potentially facilitates molecular marker-based 'genome-scans' to narrow in on genomic regions conferring trait differences between two divergent source gene pools (Chakraborty and Weiss, 1988;Briscoe et al., 1994;McKeigue et al., 2000;Pfaff et al., 2001). This prediction has been verified recently by successful admixture genome-scans for two complex traits in humans -hypertension and susceptibility for multiple sclerosis (Reich et al., 2005;Zhu et al., 2005).The requirements for genome-scans through admixture in humans have been carefully evaluated by geneticists for years (e.g., McKeigue et al., 2000;Pfaff et al., 2001;H...

Admixture as the basis for genetic mapping

“…For mapping loci that affect isolation between taxa, the over-and underrepresentation of certain genotypes in different genomic backgrounds (quantified by excess admixture) are of interest, without direct reference to traits that might be subject to selection [3][4][5]. In this application, loci and genotypes are identified that might be subject to positive or negative selection at a barrier to gene flow between divergent species or ecotypes (e.g.…”

“…Measures of excess admixture form the basis for mapping phenotypic variation and loci that contribute to isolation between taxa [4,28], although different implementations of admixture mapping parameterize and utilize excess admixture in different ways. http://doc.rero.ch 2 mapping incorporates population structure through its measure of excess ancestry (Box 1).…”

“…Admixture mapping in natural populations can facilitate studies of genetic architecture of phenotypes and the detection of regions or loci under selection. This potentially allows evolutionary biologists to study the genetic architecture of adaptation and speciation in situ [1], including long-lived or otherwise intractable taxa for which crosses or pedigrees would be difficult to obtain [4,9,10]. Similarly, admixture mapping can also aid studies of the phenotypic effects of recombination in microorganisms of medical or other direct relevance to humans [22,23], and the interpretation of data from metagenomics or community genomics research on microbial populations in their natural environments [22,24].…”

“…Admixture mapping work also is under way in two ecologically divergent European members of the genus Populus (poplars, aspens, cottonwoods), P. alba and P. tremula (floodplain versus upland species) [4,43,44]. Natural admixed populations of these species contain a high proportion of recombinant, backcrossed genotypes and occur in multiple locations throughout Europe [4,43,45].…”

“…Natural admixed populations of these species contain a high proportion of recombinant, backcrossed genotypes and occur in multiple locations throughout Europe [4,43,45]. A first survey allowed the refinement of statistical approaches to detect locus-specific effects in genomic studies of hybrid zones [4].…”