Genetic basis of an adaptive polymorphism controlling butterfly silver iridescence.

Identifying the genes and mutations that drive phenotypic variation and which are subject to selection is crucial for understanding evolutionary processes. Mormon Fritillary butterflies (Speyeria mormonia) exhibit a striking wing color polymorphism throughout their range: typical morphs bear silver spots on their ventral surfaces and can co-occur with unsilvered morphs displaying a dull coloration. Through genome-wide association studies in two polymorphic populations, we fine-map this difference in silvering to the 3' region of the transcription factor gene optix. The expression of optix is confined to the unsilvered regions that surround the spots, and these patterns are transformed to a silver identity upon optix RNA interference (RNAi) knockdown, implicating optix as a repressor of silver scales in this butterfly. We show that the unsilvered optix haplotype shows signatures of recent selective sweeps and that this allele is shared with an unsilvered population of Speyeria hydaspe, suggesting that introgressions may facilitate the exchange of variants of adaptive potential across species. Remarkably, these findings parallel the role of allelic sharing and cis-regulatory modulation of optix in shaping the aposematic red patterns of Heliconius butterflies, a lineage that separated from Speyeria 45 million years ago. The genetic basis of adaptive variation can thus be more predictable than often presumed, even for traits that appear divergent across large evolutionary distances.