Abstract
Understanding the origin and distribution of genetic diversity across landscapes is critical for predicting the future of organisms in changing climates. This study investigated how adaptive and demographic forces have shaped diversity and population structure in Pinus densata, a keystone species on Qinghai-Tibetan Plateau (QTP). We examined the distribution of genomic diversity across the range of P.densata using exome capture sequencing. We applied spatially explicit tests to dissect the impacts of allele surfing, geographic isolation and environmental gradients on population differentiation and forecasted how this genetic legacy may limit the persistence of P.densata in future climates. We found that allele surfing from range expansion could explain the distribution of 39% of the c. 48000 genotyped single nucleotide polymorphisms (SNPs). Uncorrected, these allele frequency clines severely confounded inferences of selection. After controlling for demographic processes, isolation-by-environment explained 9.2-19.5% of the genetic structure, with c. 4.0% of loci being affected by selection. Allele surfing and genotype-environment associations resulted in genomic mismatch under projected climate scenarios. We illustrate that significant local adaptation, when coupled with reduced diversity as a result of demographic history, constrains potential evolutionary response to climate change. The strong signal of genomic vulnerability in P.densata may be representative for other QTP endemics.
Highlights
The ability of a species to sustain environmental change is primarily determined by its genetic reservoir, which is shaped over the course of history through demography and selection
Detecting adaptive sources of genetic differentiation is often confounded by dispersal-demographic factors including isolation by distance (IBD) and allele surfing, but natural populations are widely expected to experience isolation by environment (IBE; Orsini et al, 2013; Wang & Bradburd, 2014), in which gene flow among populations inhabiting different ecological habitats is limited by selection (Nosil et al, 2009; Feder et al, 2012a)
We evaluated the effect of IBD and IBE in shaping genomic variation among populations using redundancy analysis (RDA)
Summary
The ability of a species to sustain environmental change is primarily determined by its genetic reservoir, which is shaped over the course of history through demography and selection. The importance of density-dependent effects during range expansion in producing strong clines or even discrete genetic sectors has been illustrated by microbial experiments and simulation studies (Excoffier & Ray, 2008; Excoffier et al, 2009; Waters et al, 2013; Peischl et al, 2016). Detecting adaptive sources of genetic differentiation is often confounded by dispersal-demographic factors including IBD and allele surfing, but natural populations are widely expected to experience isolation by environment (IBE; Orsini et al, 2013; Wang & Bradburd, 2014), in which gene flow among populations inhabiting different ecological habitats is limited by selection (Nosil et al, 2009; Feder et al, 2012a). Methods exist to control for the ubiquitous autocorrelation of IBE and IBD, distinguishing selection from dispersal-demographic effects during range expansion remains a challenge
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