Livraghi Luca, Hanly Joseph J, Loh Ling S, Henry Albie, Keck Chloe, Shirey Vaughn M, Tsai Cheng-Chia, Yu Nanfang, Van Belleghem Steven M, Roberts W Mark, Boggs Carol L, Martin Arnaud
Department of Biological Sciences, The George Washington University, Washington, DC 20052, USA.
Department of Biological Sciences, The George Washington University, Washington, DC 20052, USA; Duke University Department of Biology, Duke University, Durham, NC 27708, USA; Smithsonian Tropical Research Institute, Gamboa, Panama.
Curr Biol. 2025 May 5;35(9):2154-2163.e7. doi: 10.1016/j.cub.2025.03.028. Epub 2025 Apr 9.
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.
识别驱动表型变异且受选择作用影响的基因和突变，对于理解进化过程至关重要。摩门豹纹蝶（Speyeria mormonia）在其分布范围内呈现出显著的翅色多态性：典型形态的蝶在腹面有银色斑点，并且可以与呈现暗淡颜色的无银色形态共存。通过对两个多态性种群进行全基因组关联研究，我们将这种银色差异精细定位到转录因子基因optix的3'区域。optix的表达局限于围绕斑点的无银色区域，并且在optix RNA干扰（RNAi）敲低后，这些模式转变为银色特征，这表明optix在这种蝴蝶中是银色鳞片的抑制因子。我们表明，无银色的optix单倍型显示出近期选择性清除的特征，并且该等位基因与Hydaspe豹纹蝶的一个无银色种群共享，这表明基因渗入可能促进了跨物种的具有适应潜力的变异交换。值得注意的是，这些发现与optix的等位基因共享和顺式调控调节在塑造与Speyeria在4500万年前分离的斑蝶科蝴蝶的警戒红色图案中的作用相似。因此，适应性变异的遗传基础可能比通常认为的更具可预测性，即使对于在大的进化距离上看起来不同的性状也是如此。
