The Evolution of Sex Ratio Distorter Suppression Affects a 25 cM Genomic Region in the Butterfly Hypolimnas bolina

Symbionts that distort their host's sex ratio by favouring the production and survival of females are common in arthropods. Their presence produces intense Fisherian selection to return the sex ratio to parity, typified by the rapid spread of host ‘suppressor’ loci that restore male survival/development. In this study, we investigated the genomic impact of a selective event of this kind in the butterfly Hypolimnas bolina. Through linkage mapping, we first identified a genomic region that was necessary for males to survive Wolbachia-induced male-killing. We then investigated the genomic impact of the rapid spread of suppression, which converted the Samoan population of this butterfly from a 100∶1 female-biased sex ratio in 2001 to a 1∶1 sex ratio by 2006. Models of this process revealed the potential for a chromosome-wide effect. To measure the impact of this episode of selection directly, the pattern of genetic variation before and after the spread of suppression was compared. Changes in allele frequencies were observed over a 25 cM region surrounding the suppressor locus, with a reduction in overall diversity observed at loci that co-segregate with the suppressor. These changes exceeded those expected from drift and occurred alongside the generation of linkage disequilibrium. The presence of novel allelic variants in 2006 suggests that the suppressor was likely to have been introduced via immigration rather than through de novo mutation. In addition, further sampling in 2010 indicated that many of the introduced variants were lost or had declined in frequency since 2006. We hypothesize that this loss may have resulted from a period of purifying selection, removing deleterious material that introgressed during the initial sweep. Our observations of the impact of suppression of sex ratio distorting activity reveal a very wide genomic imprint, reflecting its status as one of the strongest selective forces in nature.通过偏好雌性的产生与存活来改变宿主性比的共生菌在节肢动物中十分常见。这类共生菌的存在会引发强烈的费希尔选择（Fisherian selection），促使性比回归平衡，其典型特征为宿主的“抑制”基因座快速扩散，该基因座可恢复雄性的存活与发育。本研究以幻紫斑蛱蝶（Hypolimnas bolina）为对象，探究此类选择事件对基因组造成的影响。通过连锁作图，我们首先鉴定出一个基因组区域，该区域是雄性个体在沃尔巴克氏体（Wolbachia）诱导的雄性致死现象中得以存活的必要条件。随后我们研究了抑制现象快速扩散对基因组的影响——该过程将该蝴蝶的萨摩亚种群从2001年的100:1雌性偏倚性比，在2006年扭转至1:1的平衡性比。对此过程的模型分析揭示了其存在全染色体效应的可能性。为直接量化此次选择事件的影响，我们对比了抑制现象扩散前后的遗传变异模式。我们在抑制基因座周围25厘摩（cM）的区域内观测到了等位基因频率的变化，且与该抑制基因座共分离的基因座的整体多样性有所降低。这些变化幅度超出了遗传漂变的预期，且伴随连锁不平衡（linkage disequilibrium）的产生。2006年样本中出现的新型等位变异表明，该抑制基因座大概率是通过移民迁入而非从头突变引入的。此外，2010年的进一步采样显示，自2006年以来，许多引入的变异已丢失或频率降低。我们推测此类丢失可能源于一段时期的纯化选择，该过程清除了初始选择扫掠过程中渐渗进入的有害遗传物质。我们针对性比扭曲抑制活动影响的观测结果显示，该过程留下了极为广泛的基因组印记，这也反映出其作为自然界最强选择力量之一的地位。