Data from: Transcriptome analysis reveals novel patterning and pigmentation genes underlying Heliconius butterfly wing pattern variation

BACKGROUND: Heliconius butterfly wing pattern diversity offers a unique opportunity to investigate how natural genetic variation can drive the evolution of complex adaptive phenotypes. Positional cloning and candidate gene studies have identified a handful of regulatory and pigmentation genes implicated in Heliconius wing pattern variation, but little is known about the greater developmental networks within which these genes interact to pattern a wing. Here we took a large-scale transcriptomic approach to identify the network of genes involved in Heliconius wing pattern development and variation. This included applying over 140 transcriptome microarrays to assay gene expression in dissected wing pattern elements across a range of developmental stages and wing pattern morphs of Heliconius erato. RESULTS: We identified a number of putative early prepattern genes with color-pattern related expression domains. We also identified 51 genes differentially expressed in association with natural color pattern variation. Of these, the previously identified color pattern “switch gene” optix was recovered as the first transcript to show color-specific differential expression. Most differentially expressed genes were transcribed late in pupal development and have roles in cuticle formation or pigment synthesis. These include previously undescribed transporter genes associated with ommochrome pigmentation. Furthermore, we observed upregulation of melanin-repressing genes such as ebony and Dat1 in non-melanic patterns. CONCLUSIONS: This study identifies many new genes implicated in butterfly wing pattern development and provides a glimpse into the number and types of genes affected by variation in genes that drive color pattern evolution.

研究背景：釉蛱蝶属（Heliconius）蝴蝶的翅型多样性为探究自然遗传变异如何驱动复杂适应性表型的演化提供了独一无二的研究契机。过往的定位克隆与候选基因研究已确定数个与釉蛱蝶翅型变异相关的调控基因及色素沉着基因，但对于这些基因相互作用以构建翅型模式的更大规模发育调控网络，我们仍知之甚少。本研究采用大规模转录组学方法，对参与釉蛱蝶翅型发育与变异的基因网络进行鉴定。具体而言，我们使用超过140套转录组微阵列（transcriptome microarrays），对红带袖蝶（Heliconius erato）不同发育阶段、不同翅型形态的解剖翅型元件中的基因表达水平进行检测。研究结果：我们鉴定出多个具备与颜色模式相关表达结构域的推定早期预模式基因。同时，我们还发现51个与自然颜色模式变异相关的差异表达（differentially expressed）基因。其中，此前已被报道的颜色模式「开关基因」optix是首个表现出颜色特异性差异表达的转录本。绝大多数差异表达基因在蛹发育后期被转录，且参与表皮形成或色素合成过程，包括若干此前未被报道的与眼黄素（ommochrome）色素沉着相关的转运蛋白基因。此外，我们观察到在非黑色素型翅型中，诸如ebony与Dat1这类黑色素抑制基因的表达水平出现上调。研究结论：本研究鉴定出诸多参与蝴蝶翅型发育的全新基因，并为解析驱动颜色模式演化的基因变异所影响的基因数量与类型提供了新的研究视角。