Spatial autocorrelation of the environment influences the patterns and genetics of local adaptation

Abstract

Environmental heterogeneity can lead to spatially varying selection, which can, in turn, lead to local adaptation. Population genetic models have shown that the pattern of environmental variation in space can strongly influence the evolution of local adaptation. In particular, when environmental variation is highly autocorrelated in space local adaptation will more readily evolve. Despite this long-held prediction, the evolutionary genetic consequences of different patterns of environmental variation have not been thoroughly explored. In this study, simulations are used to model local adaptation to different patterns of environmental variation. The simulations confirm that local adaptation is expected to increase with the degree of spatial autocorrelation in the selective environment, but also show that highly heterogeneous environments are more likely to exhibit high variation in local adaptation, a result not previously described. Spatial autocorrelation in the environment also influences the evolution and genetic architecture of local adaptation, with different combinations of allele frequency and effect size arising under different patterns of environmental variation. These differences influence the ability to characterise the genetic basis of local adaptation in different environments. Finally, I analyse a large-scale provenance trial conducted on lodgepole pine and find suggestive evidence that spatially autocorrelated environmental variation leads to stronger local adaptation in natural populations of lodgepole pine. Overall, this work emphasizes the profound importance that the spatial pattern of selection can have on the evolution of local adaptation and how spatial autocorrelation should be considered when formulating hypotheses in ecological and genetic studies. Lay SummaryMany species exhibit local adaptation to environmental variation across their ranges. Theoretical population genetics predicts that the evolution of local adaptation and patterns of genetic variation underlying it will be influenced by the spatial pattern of variation across a species range. However, this prediction has not been thoroughly explored for cases of complex heterogeneous landscapes. In this paper, I analyse simulations and empirical data to characterise the effects that the spatial pattern of environmental variation can have on the evolution of local adaptation and the genetics underlying it. From these analyses, I show that the pattern of environmental variation influences the average level of local adaptation, variation in local adaptation as well as the genetics underlying this important phenomenon.