Abstract
Accurately detecting signatures of local adaptation using genetic‐environment associations (GEAs) requires controlling for neutral patterns of population structure to reduce the risk of false positives. However, a high degree of collinearity between climatic gradients and neutral population structure can greatly reduce power, and the performance of GEA methods in such case is rarely evaluated in empirical studies. In this study, we attempted to disentangle the effects of local adaptation and isolation by environment (IBE) from those of isolation by distance (IBD) and isolation by colonization from glacial refugia (IBC) using range‐wide samples in two white pine species. For this, SNPs from 168 genes, including 52 candidate genes for growth and phenology, were genotyped in 133 and 61 populations of Pinus strobus and P. monticola, respectively. For P. strobus and using all 153 SNPs, climate (IBE) did not significantly explained among‐population variation when controlling for IBD and IBC in redundancy analyses (RDAs). However, 26 SNPs were significantly associated with climate in single‐locus GEA analyses (Bayenv2 and LFMM), suggesting that local adaptation took place in the presence of high gene flow. For P. monticola, we found no evidence of IBE using RDAs and weaker signatures of local adaptation using GEA and F ST outlier tests, consistent with adaptation via phenotypic plasticity. In both species, the majority of the explained among‐population variation (69 to 96%) could not be partitioned between the effects of IBE, IBD, and IBC. GEA methods can account differently for this confounded variation, and this could explain the small overlap of SNPs detected between Bayenv2 and LFMM. Our study illustrates the inherent difficulty of taking into account neutral structure in natural populations and the importance of sampling designs that maximize climatic variation, while minimizing collinearity between climatic gradients and neutral structure.
Highlights
Climate is a major factor affecting the distribution of genetic diversity among natural populations of plants
| 8651 addressed the following questions: (1) “Can we detect genes showing signatures of local adaptation to climate in each species and in both species?” and (2) “Did local adaptation to climate contribute to the observed population structure (IBE) in P. monticola and P. strobus, or was it mostly driven by neutral processes (i.e., isolation by distance (IBD) or isolation by colonization from glacial refugia (IBC))?”
P. strobus could be considered an ideal species in which to look for signatures of local adaptation since it shows moderate among-population genetic variation for adaptive traits, but weak neutral population structure
Summary
Climate is a major factor affecting the distribution of genetic diversity among natural populations of plants. Tree species generally exhibit moderate to high among-population genetic variation for adaptive traits along climatic gradients (Alberto et al, 2013; Savolainen, Pyhäjärvi, & Knürr, 2007) Despite such evidence of local adaptation from common-garden studies, patterns of population structure observed at nuclear loci are often considered to result from neutral processes affecting the whole genome, including genetic drift, gene flow, and past demographic events (e.g., recent range contractions and expansions). Because the selective climatic gradients, geography, and postglacial recolonization routes are often spatially correlated in natural populations, it is extremely difficult to separate the relative effects of IBE from those of IBD and IBC Disentangling these effects is important to accurately control for neutral population structure (e.g., IBD and IBC) when looking for signatures of local adaptation. | 8651 addressed the following questions: (1) “Can we detect genes showing signatures of local adaptation to climate in each species and in both species?” and (2) “Did local adaptation to climate contribute to the observed population structure (IBE) in P. monticola and P. strobus, or was it mostly driven by neutral processes (i.e., IBD or IBC)?”
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