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Genomics and gene flow barriers in hybrid Populus - COMPLETED 2010

Barriers to gene flow between divergent populations or species result from selection on divergent phenotypes and from negative genomic interactions in hybrids. The recent sequencing of the Populus genome has created the opportunity to address the genetics of barriers to gene flow in a tree genus of immense ecological and economic importance.

Gene locus with lower than expected introgression across hybrid zone, showing a negative departure from neutrality

We (1) carried out population genomic scans of three replicate natural hybrid zones of two widespread, ecologically important forest trees (Populus alba and P. tremula) to identify loci involved in reproductive isolation and adaptive introgression, (2) extended this work to candidate genes involved in ecological divergence, and (3) carried out an admixture mapping genome scan for leaf morphology, a suite of traits with great interspecific differentiation and potential correlation with biomass accumulation. Admixture between genetically divergent populations facilitates genomic studies of the mechanisms involved in adaptation, reproductive isolation and speciation, including mapping of the loci involved in these phenomena. Little is known about how pre- and postzygotic barriers will affect the prospects of ‘admixture mapping’ in wild species. We studied 93 mapped genetic markers (microsatellites, indels and sequence polymorphisms, > 63000 data points) to address this topic in P. alba/P. tremula hybrid zones. Using genotype and linkage information and recently developed analytical tools we showed that (1) reproductive isolation between these species is much stronger than previously assumed but this cannot prevent the introgression of neutral or advantageous alleles, (2) unexpected genotypic gaps exist between recombinant hybrids and their parental taxa, (3) these conspicuous genotypic patterns are due to assortative mating and strong postzygotic barriers, rather than recent population history. These findings allowed us to discuss possible evolutionary trajectories of hybrid lineages between these species and outline strategies for admixture mapping in hybrid zones between highly divergent populations. Admixture facilitates adaptation from standing variation in P. tremula. Whether admixture constrains or facilitates adaptation from standing variation is largely unknown, especially in ecological keystone or foundation species. We examined patterns of neutral and adaptive population divergence in P. tremula, a widespread forest tree, using mapped molecular genetic markers. We detected the genetic signature of postglacial admixture between a western and an eastern lineage of P. tremula in Scandinavia, a suspected zone of postglacial contact for many species. Stringent divergence based neutrality tests provided clear indications for locally varying selection at the European scale. Six out of 12 polymorphisms under selection were located < 1000 bases away from the nearest gene predicted by the P. trichocarpa genome sequence. Few of these exhibited a signature of ‘selective sweeps’ in diversity based tests, which is to be expected if adaptation occurs primarily from standing variation. In Scandinavia, admixture explained genomic patterns of ancestry and the nature of clinal variation and strength of selection for bud set, a phenological trait of adaptive significance in temperate trees, measured in a common garden trial. Our data provide a hitherto missing direct link between past range shifts due to climatic oscillations and levels of standing variation currently available for selection and adaptation.


 Lexer,C., Joseph, J.A., van Loo, M., Barbará, T., Heinze, B., Bartha, D., Castiglione, S., Fay, M.F., Buerkle, C.A. (2010) Genomic admixture analysis in European Populus spp. reveals unexpected patterns of reproductive isolation and mating. Genetics 186: 699–712.
 

de Carvalho D, Ingvarsson PK, Joseph J, Suter L, Sedivy C, Macaya-Sanz D, Cottrell J, Heinze B, Schanzer S, Lexer C (2010) Admixture facilitates adaptation from standing variation in the European aspen (P. tremula L.), a widespread forest tree. Molecular Ecology 19: 1638-1650.
 

Buerkle, C.A. & Lexer, C. (2008) Admixture as the basis for genetic mapping. Trends in Ecology and Evolution 23: 686-694.
 

 Lexer, C., Joseph, J., van Loo, M., Prenner, G., Heinze, B., Chase, M.W. & Kirkup, D. (2009) The use of digital image-based morphometrics to study the phenotypic mosaic in taxa with porous genomes. Taxon 58: 349-364.
 

Macaya-Sanz, Suter, L., Joseph, J., Barbará, T., Alba, N., Gonzalez-Martinez, S.C., Widmer, A., Lexer, C. (2011) Genetic analysis of post-mating reproductive barriers in hybridizing European Populus species. Heredity doi:10.1038/hdy.2011.35
 

Project partners and collaborators

Austria

Berthold Heinze, Marcela van Loo

Brazil

Dulcineia de Carvalho

Italy

Stefano Castiglione

Spain

David Macaya- Sanz

Switzerland

Alex Widmer

UK

Joan Cottrell

USA

Alex Buerkle

Project team

Jodrell Laboratory

Mike Fay, Christian Lexer,Thelma Barbará, Jeff Joseph,

HLAA Directorate

Don Kirkup

Science Teams: 
Project Leader: