The Consequences of Parallel Selection on Genome Divergence during the Early Stages of Speciation

Speciation is facilitated by divergent natural selection and adaptation to different ecological conditions. Thus, quantifying selection's effect on genome differentiation between incipient species is important for understanding speciation. However the nature of the genetic variation that contributes most to local adaptation and the genome-level consequences of divergent natural selection are not yet well known. Herein we analyze whole genome re-sequencing data from replicated natural and experimental stick insect populations to test hypotheses regarding the genetic basis of local adaptation and genome differentiation during the early stages of speciation. We document heterogeneous genetic differentiation between populations, with many small genetic regions exhibiting elevated (but not fixed) allele frequency differences and distinct patterns of differentiation between allopatric and parapatric populations. We identified tens of genetic loci that differed consistently between stick insect populations adapted to different host plants, with an excess of parallel differentiation in coding regions. Nonetheless, patterns of genetic differentiation were largely dissimilar between population pairs. We conducted a field transplant experiment to test the hypothesis that high genetic differentiation was in part caused by divergent host plant associated selection. Despite considerable genetic drift during the experiment, we detected significant concordance between parallel genetic differentiation in nature and parallel allele frequency change during the experiment consistent with our hypothesis. These results provide evidence that genome divergence between locally adapted stick insect populations was caused by geographic isolation and divergent selection, and that the latter has acted disproportionately on coding variants.