Genotyping-by-sequencing and ecological niche modeling illuminate phylogeography, admixture, and Pleistocene range dynamics in quaking aspen (Populus tremuloides).

Justin C Bagley,Karen E Mock,Upendra K Devisetty,Eliécer E Gutiérrez,Neander M Heming,Andrew J Eckert,Steven H Strauss

doi:10.1002/ece3.6214

Abstract

Populus tremuloides is the widest‐ranging tree species in North America and an ecologically important component of mesic forest ecosystems displaced by the Pleistocene glaciations. Using phylogeographic analyses of genome‐wide SNPs (34,796 SNPs, 183 individuals) and ecological niche modeling, we inferred population structure, ploidy levels, admixture, and Pleistocene range dynamics of P. tremuloides, and tested several historical biogeographical hypotheses. We found three genetic lineages located mainly in coastal–Cascades (cluster 1), east‐slope Cascades–Sierra Nevadas–Northern Rockies (cluster 2), and U.S. Rocky Mountains through southern Canadian (cluster 3) regions of the P. tremuloides range, with tree graph relationships of the form ((cluster 1, cluster 2), cluster 3). Populations consisted mainly of diploids (86%) but also small numbers of triploids (12%) and tetraploids (1%), and ploidy did not adversely affect our genetic inferences. The main vector of admixture was from cluster 3 into cluster 2, with the admixture zone trending northwest through the Rocky Mountains along a recognized phenotypic cline (Utah to Idaho). Clusters 1 and 2 provided strong support for the “stable‐edge hypothesis” that unglaciated southwestern populations persisted in situ since the last glaciation. By contrast, despite a lack of clinal genetic variation, cluster 3 exhibited “trailing‐edge” dynamics from niche suitability predictions signifying complete northward postglacial expansion. Results were also consistent with the “inland dispersal hypothesis” predicting postglacial assembly of Pacific Northwestern forest ecosystems, but rejected the hypothesis that Pacific‐coastal populations were colonized during outburst flooding from glacial Lake Missoula. Overall, congruent patterns between our phylogeographic and ecological niche modeling results and fossil pollen data demonstrate complex mixtures of stable‐edge, refugial locations, and postglacial expansion within P. tremuloides. These findings confirm and refine previous genetic studies, while strongly supporting a distinct Pacific‐coastal genetic lineage of quaking aspen.

Highlights

Many North American forest tree species are broadly distributed across large areas of the continent (Little, 1971; Prasad, Iverson, Matthews, & Peters, 2007)
Our specific goals were fourfold: (a) to infer broadscale patterns of population structuring and ploidy levels within P. tremuloides using genomic single nucleotide polymorphism (SNP) data; (b) to test the presence and directionality of admixture between intraspecific gene pools; (c) to infer Pleistocene range dynamics of the species and its genetic lineages using ecological niche modeling (ENM) and assess whether genetic differentiation is explained by connectivity or isolation of predicted suitable habitats over the last glacial cycle; and (d) to test several a priori historical biogeographical hypotheses for North American forest trees described below
We inferred the phylogeographic history of P. tremuloides by combining broadscale inferences of population structure, admixture, and ploidy based on genome-wide SNP data (Elshire et al, 2011) with spatially explicit predictions of the past to present geographical distributions of the species and its intraspecific lineages using ENM hindcasting (Peterson et al, 2011; Waltari et al, 2007)

Summary

| INTRODUCTION

Many North American forest tree species are broadly distributed across large areas of the continent (Little, 1971; Prasad, Iverson, Matthews, & Peters, 2007). Related populations and species frequently occur across major geographical barriers, including western Pacific mountain ranges (e.g., Cascades, Sierra Nevada), ranges of the greater continental divide (Rocky Mountains) and eastern divide (Appalachian Mountains), or xeric habitats of the Great Basin and major deserts Explaining such distributions requires historical biogeographical processes such as range fragmentation in a wide-ranging ancestral lineage spanning both sides of a barrier, or dispersal into areas on either side (e.g., Rosen, 1978). Our specific goals were fourfold: (a) to infer broadscale patterns of population structuring and ploidy levels within P. tremuloides using genomic SNP data; (b) to test the presence and directionality of admixture between intraspecific gene pools; (c) to infer Pleistocene range dynamics of the species and its genetic lineages using ENMs and assess whether genetic differentiation is explained by connectivity or isolation of predicted suitable habitats over the last glacial cycle; and (d) to test several a priori historical biogeographical hypotheses for North American forest trees described below

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| MATERIALS AND METHODS

Findings

| DISCUSSION