The predictability of genomic changes underlying a recent host shift in Melissa blue butterflies

Despite accumulating evidence that evolution can be predictable, with populations employing similar genetic solutions in response to similar environmental pressures, studies quantifying the predictability of evolution are still rare. Herein, we measured the predictability of genome-wide evolutionary changes associated with a recent host shift in the Melissa blue butterfly (Lycaeides melissa). We asked whether and to what extent genome-wide patterns of evolutionary change in nature could be predicted (1) by comparisons among instances of repeated evolution, and (2) from SNP-performance associations in lab experiments. We delineated the genetic loci (SNPs) mostly strongly associated with host use during two independent shifts of L. melissa onto alfalfa. Whereas most SNPs were strongly associated with host use in one of the two alfalfa-feeding lineages, we detected a two-fold (range = 1.5--2.8) excess of SNPs associated with host use in both lineages. Similarly, we found that host-associated SNPs in nature could also be partially predicted from SNP x performance (survival and weight) associations in lab rearing experiment. But the extent of overlap, and thus degree of predictability, was somewhat reduced (range of x-fold enrichment = 0.5--2.5). Although we were able to predict (to a modest extent) the SNPs most strongly associated with host use in nature (in terms of parallelism and from the experiment), we had little to no ability to predict the direction of evolutionary change during the colonization of alfalfa. We suspect that this limit on predictability occurred because patterns (including the direction) of linkage disequilibrium between the unknown causal variants and our SNP markers varied among populations. Thus, our results show that different aspects of evolution associated with recent adaptation can be more or less predictable, and highlight how stochastic and deterministic processes interact to drive patterns of genome-wide evolutionary change.