Martin Arnaud, Reed Robert D
Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 14853, USA; Department of Developmental and Cellular Biology, Irvine, CA 92697, USA.
Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 14853, USA.
Dev Biol. 2014 Nov 15;395(2):367-78. doi: 10.1016/j.ydbio.2014.08.031. Epub 2014 Sep 6.
Most butterfly wing patterns are proposed to be derived from a set of conserved pattern elements known as symmetry systems. Symmetry systems are so-named because they are often associated with parallel color stripes mirrored around linear organizing centers that run between the anterior and posterior wing margins. Even though the symmetry systems are the most prominent and diverse wing pattern elements, their study has been confounded by a lack of knowledge regarding the molecular basis of their development, as well as the difficulty of drawing pattern homologies across species with highly derived wing patterns. Here we present the first molecular characterization of symmetry system development by showing that WntA expression is consistently associated with the major basal, discal, central, and external symmetry system patterns of nymphalid butterflies. Pharmacological manipulations of signaling gradients using heparin and dextran sulfate showed that pattern organizing centers correspond precisely with WntA, wingless, Wnt6, and Wnt10 expression patterns, thus suggesting a role for Wnt signaling in color pattern induction. Importantly, this model is supported by recent genetic and population genomic work identifying WntA as the causative locus underlying wing pattern variation within several butterfly species. By comparing the expression of WntA between nymphalid butterflies representing a range of prototypical symmetry systems, slightly deviated symmetry systems, and highly derived wing patterns, we were able to infer symmetry system homologies in several challenging cases. Our work illustrates how highly divergent morphologies can be derived from modifications to a common ground plan across both micro- and macro-evolutionary time scales.
大多数蝴蝶翅膀图案被认为源自一组被称为对称系统的保守图案元素。对称系统之所以如此命名，是因为它们通常与平行的彩色条纹相关联，这些条纹围绕着在前翅和后翅边缘之间延伸的线性组织中心呈镜像对称。尽管对称系统是最突出和多样的翅膀图案元素，但由于缺乏关于其发育分子基础的知识，以及难以在具有高度特化翅膀图案的物种间绘制图案同源性，对它们的研究一直受到困扰。在这里，我们通过展示WntA的表达始终与蛱蝶科蝴蝶的主要基部、盘状、中央和外部对称系统图案相关联，首次对对称系统发育进行了分子特征描述。使用肝素和硫酸葡聚糖对信号梯度进行药理学操作表明，图案组织中心与WntA、无翅基因、Wnt6和Wnt10的表达模式精确对应，从而表明Wnt信号在颜色图案诱导中起作用。重要的是，这个模型得到了最近的遗传和群体基因组学研究的支持，这些研究将WntA确定为几种蝴蝶物种翅膀图案变异的致病基因座。通过比较代表一系列典型对称系统、略有偏差的对称系统和高度特化翅膀图案的蛱蝶科蝴蝶之间WntA的表达，我们能够在几个具有挑战性的案例中推断出对称系统的同源性。我们的工作说明了在微观和宏观进化时间尺度上，高度不同的形态是如何通过对共同基础模板的修改而产生的。
