Genomic diversity, population structure, and migration following rapid range expansion in the Balsam Poplar,Populus balsamifera

Abstract

Rapid range expansions can cause pervasive changes in the genetic diversity and structure of populations. The postglacial history of the Balsam Poplar, Populus balsamifera, involved the colonization of most of northern North America, an area largely covered by continental ice sheets during the last glacial maximum. To characterize how this expansion shaped genomic diversity within and among populations, we developed 412 SNP markers that we assayed for a range-wide sample of 474 individuals sampled from 34 populations. We complemented the SNP data set with DNA sequence data from 11 nuclear loci from 94 individuals, and used coalescent analyses to estimate historical population size, demographic growth, and patterns of migration. Bayesian clustering identified three geographically separated demes found in the Northern, Central, and Eastern portions of the species' range. These demes varied significantly in nucleotide diversity, the abundance of private polymorphisms, and population substructure. Most measures supported the Central deme as descended from the primary refuge of diversity. Both SNPs and sequence data suggested recent population growth, and coalescent analyses of historical migration suggested a massive expansion from the Centre to the North and East. Collectively, these data demonstrate the strong influence that range expansions exert on genomic diversity, both within local populations and across the range. Our results suggest that an in-depth knowledge of nucleotide diversity following expansion requires sampling within multiple populations, and highlight the utility of combining insights from different data types in population genomic studies.

Local Selection Across a Latitudinal Gradient Shapes Nucleotide Diversity in Balsam Poplar, Populus balsamifera L

“…Assuming a 15-year generation time (Ingvarsson 2008), this corresponds to 10,000 years ago, when a large proportion of the glaciated area of P. balsamifera's current range started to become ice free and available for colonization. For three reasons our demographic model should produce conservative estimates of differentiation for testing local adaptation: there was no migration between subpopulations (allowing that migration narrowed the confidence intervals on p T-S ; results not shown), unaccounted-for population substructure will elevate p S , thereby lowering the empirical estimates of p T-S , and finally the northern subgroup we used for our empirical data contained individuals from all three regional genetic clusters (Keller et al 2010), which should increase empirical estimates of p S and lower p T-S over expectations from a simple north-south demographic split. We simulated 50,000 replicates of the coalescent with Hudson's MS, conditioned on the total number of segregating sites for each phenology gene, and compared the observed p T-S to the 95% confidence interval under neutrality.…”

“…We refrained from testing more complicated models that include population subdivision and migration among regional groups (e.g., Keller et al 2010) because our initial simple models captured the major features of diversity found in the range-wide sample of 15 individuals (see Results). In other words, these ABC models should not be viewed as accurate descriptors of the demographic history as much as simplified models that capture the patterns of nucleotide diversity found in the reference loci from a widespread sample of a limited number of individuals.…”

“…We then tested if the empirical differentiation between subgroups was greater than expected in the absence of selection, using an index of absolute nucleotide differentiation, p T-S = p T 2 p S , in which p T is the total nucleotide diversity across the pooled sample and p S is the average nucleotide diversity within each of the two latitudinal groups (Charlesworth 1998). Because we lacked the sampling to explicitly model a demographic scenario of latitudinal divergence among three regional clusters (Keller et al 2010), we simulated the expected distribution of p T-S under a neutral model that captured the major biological features of balsam poplar's northward expansion from a southern refugial population. Our coalescent model consisted of a single ancestral population of N 0 = 20,000 that split into two equal sized subpopulations (N 1 = N 2 = 10,000) 650 generations before present.…”

“…On the basis of SNP data from 412 loci assayed from 474 trees sampled from across the species range, this expansion appears to have involved the spread of populations from a southwestern refugial population into the northwest and northeast (Keller et al 2010). This spread is reflected in the current diversity forming three broadly distributed genetic clusters, currently situated in the northern, central, and eastern parts of the range.…”

Geographical barriers and climate influence demographic history in narrowleaf cottonwoods

“…Furthermore, repeated Quaternary glacial cycles have had a pronounced effect, seen in both the past and current distribution of species, even in areas that were free of ice during the last glacial maximum (LGM, ca 18 000 years ago; Frenzel et al, 1992;Jackson and Weng, 1999;Hu et al, 2009). These climatic shifts impacted population size, subdivision and migration, leaving genetic signatures in genome-wide patterns of polymorphism and influencing patterns of natural selection (Ingvarsson, 2008;Keller et al, 2010Keller et al, , 2011Ma et al, 2010;Levsen et al, 2012;Cushman et al, 2014;Evans et al, 2014;Zhou et al, 2014).…”