Modularity of genes involved in local adaptation to climate despite physical linkage

Linkage among genes experiencing different selection pressures can make natural selection less efficient. Theory predicts that when local adaptation is driven by complex and non-covarying stresses, increased linkage is favored for alleles with similar pleiotropic effects, with increased recombination favored among alleles with contrasting pleiotropic effects. Here, we introduce a framework to test these predictions with a co-association network analysis, which clusters loci based on differing associations. We use this framework to study the genetic architecture of local adaptation to climate in lodgepole pine, Pinus contorta, based on associations with environments.

We identify many clusters of candidate genes and SNPs associated with distinct environments, including aspects of aridity and freezing, and discover low recombination rates among some candidate genes in different clusters. Only a few genes contain SNPs with effects on more than one distinct aspect of climate. There is limited correspondence between co-association networks and gene regulatory networks. We further show how associations with environmental principal components can lead to misinterpretation. Finally, simulations illustrate both benefits and caveats of co-association networks.

Our results support the prediction that different selection pressures favor the evolution of distinct groups of genes, each associating with a different aspect of climate. But our results went against the prediction that loci experiencing different sources of selection would have high recombination among them. These results give new insight into evolutionary debates about the extent of modularity, pleiotropy, and linkage in the evolution of genetic architectures.