Admixture in a butterfly species complex creates a genomic mosaic of ancestry with distinct histories for different chromosomes

Hybridization and admixture give rise to populations with mosaic genomes composed of ancestry segments with distinct origins and histories. Despite a growing number of documented cases of admixture in nature, relatively little is known about how mosaic patterns of ancestry vary simultaneously across the genome and among multiple populations or lineages of hybridizing species. Here, using pooled whole-genome sequence data from more than 20 populations representing three nominal species and multiple admixed or taxonomically ambiguous populations, we show that widespread admixture in Lycaeides butterflies has resulted in distinct evolutionary histories within and among chromosomes, with the most notable differences between the autosomes and the Z sex chromosome. Many populations exhibit substantial evidence of mixed ancestry on the autosomes, whereas the Z chromosome shows a more tree-like evolutionary history. In some cases, the predominant ancestry of the autosomes and the Z chromosome differ. We also find evidence of variation in ancestry within chromosomes, though this appears more idiosyncratic. We also show that differences in autosomal versus Z-chromosome ancestry have the potential to shape ecologically important trait variation. Specifically, using genome-wide association mapping, we demonstrate that wing-pattern elements-traits known to influence mate preference-are affected by genetic variants on both the autosomes and the Z chromosome. In sum, our results show that different chromosomes can exhibit distinct evolutionary histories, with the Z chromosome suggesting more discrete evolutionary lineages or species than the autosomes. These findings have implications both for our basic understanding of species and species boundaries and for how we view the sources of genetic and phenotypic variation that fuel ongoing evolutionary change. Teaser textHow well do bifurcating trees comprising distinct species capture the evolutionary histories of groups of organisms? Answering this question is central to our understanding of species, speciation, and the organization of biological diversity. We show that, at least for Lycaeides butterflies, the answer differs for different parts of the genome. Our results suggest that these butterflies genomes comprise a mixture of genomic regions and chromosomes with distinct evolutionary histories. In particular, we found substantial evidence of historical hybridization and mixed ancestry on the autosomes, but distinct and more tree-like histories on the Z sex chromosome. Our genetic mapping results indicate that these different histories are relevant for polygenic trait variation, specifically wing patterns, which play a central role in mate preference. Thus, our results shed light on the multifaceted nature of species and the sources of variation that fuel evolution.