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Nature GeNetics VOLUME 46 | NUMBER 10 | OCTOBER 2014 1089
A suite of forces and factors, including mutation, recombination, selection, population history and gene duplication influence patterns of intraspecific genetic variation. Distinguishing which factors have shaped sequence variation across a genome requires extensive whole- genome sequencing of multiple individuals, which has only recently become tractable1. Most large-scale whole-genome resequencing studies have focused on model and domesticated species1–5. However, extensive sequencing of natural populations holds great promise for advancing understanding of evolutionary biology, including identify- ing functional variation and the molecular bases of adaptation. Recent work in a number of species has identified genomic regions that show signatures of positive selection, suggesting that such regions contain loci that control adaptive traits4,6–8. Relatively few studies, however, have combined genome-wide scans with phenotypic data to determine whether computationally identified selected regions influence adap- tive phenotypic variation5,9–13. Genome-wide studies of large natural populations combined with phenotypic measurements are necessary to determine which factors shape patterns of genetic variation within species and, therefore, enhance understanding of adaptation.
With large geographic ranges spanning wide environmental gradi- ents and a long history of research showing local adaptation14, forest trees are ideal for examining the processes shaping genetic variation in natural populations. Forest trees cover approximately 30% of ter- restrial land area15, provide direct feedback to global climate15 and are often foundation species that organize entire biotic communities and biogeochemical systems16,17. Clearly, biotic and abiotic interac- tions have influenced population sizes and distributions of forest trees, leaving diagnostic signatures in the genomes of present-day populations14,18,19. A deeper understanding of the evolutionary and
ecological forces that shaped these patterns will offer insights and options for ecosystem management, applied tree improvement and accelerated domestication efforts20.
Black cottonwood, Populus trichocarpa Torr. & Gray, is a dominant riparian tree that has become a model for the advancement of genome- level insights in forest trees21. The sequencing of 16 P. trichocarpa genomes revealed widespread patterns of linkage disequilibrium (LD) and population structure22 and extensive genecological studies have revealed a high degree of adaptive phenotypic variation in growth, vegetative phenology and physiological traits such as water-use effi- ciency and photosynthesis23–25, suggesting that local adaptation is prevalent. To date, candidate gene–association analyses have revealed loci with significant effects on phenotypic traits26,27. However, thus far there have been no publications describing whole-genome asso- ciations for adaptive traits in P. trichocarpa, or their relationship to signatures of selection in any forest tree species.
One of the salient features of the P. trichocarpa genome is a remark- ably well-conserved whole-genome duplication that is shared by all members of the Salicaceae and near relatives: the Salicoid duplica- tion28,29. Despite the extensive occurrence of segments of collinear paralogous genes, more than two-thirds of the duplicated genes are lost after the duplication event, and there are substantial functional biases in the remaining gene pairs—in particular, there is an over- abundance of gene categories with large numbers of protein-protein interactions30,31. A major unexplored question is whether the funda- mental, diagnostic differences in diversity between retained duplicate pairs and genes lacking paralogs from the Salicoid duplication (sin- gletons) are connected to patterns of natural selection and adaptive phenotypic variation.
Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations Luke M Evans1, Gancho T Slavov2, Eli Rodgers-Melnick1, Joel Martin3, Priya Ranjan4, Wellington Muchero4, Amy M Brunner5, Wendy Schackwitz3, Lee Gunter4, Jin-Gui Chen4, Gerald A Tuskan3,4 & Stephen P DiFazio1
Forest trees are dominant components of terrestrial ecosystems that have global ecological and economic importance. Despite distributions that span wide environmental gradients, many tree populations are locally adapted, and mechanisms underlying this adaptation are poorly understood. Here we use a combination of whole-genome selection scans and association analyses of 544 Populus trichocarpa trees to reveal genomic bases of adaptive variation across a wide latitudinal range. Three hundred ninety-seven genomic regions showed evidence of recent positive and/or divergent selection and enrichment for associations with adaptive traits that also displayed patterns consistent with natural selection. These regions also provide unexpected insights into the evolutionary dynamics of duplicated genes and their roles in adaptive trait variation.
1Department of Biology, West Virginia University, Morgantown, West Virginia, USA. 2Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, UK. 3The Joint Genome Institute, Walnut Creek, California, USA. 4Plant Systems Biology Group, BioSciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA. 5Department of Forest Resources and Environmental Conservation, Virginia Tech, Blacksburg, Virginia, USA. Correspondence should be addressed to S.P.D. (spdifazio@mail.wvu.edu).
Received 22 May; accepted 30 July; published online 24 August 2014; doi:10.1038/ng.3075
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