Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada.
Department of Cell and Systems Biology, University of Toronto, Toronto, ON, Canada.
Mol Biol Evol. 2018 Jun 1;35(6):1376-1389. doi: 10.1093/molbev/msy025.
The visual systems of snakes are heavily modified relative to other squamates, a condition often thought to reflect their fossorial origins. Further modifications are seen in caenophidian snakes, where evolutionary transitions between rod and cone photoreceptors, termed photoreceptor transmutations, have occurred in many lineages. Little previous work, however, has focused on the molecular evolutionary underpinnings of these morphological changes. To address this, we sequenced seven snake eye transcriptomes and utilized new whole-genome and targeted capture sequencing data. We used these data to analyze gene loss and shifts in selection pressures in phototransduction genes that may be associated with snake evolutionary origins and photoreceptor transmutation. We identified the surprising loss of rhodopsin kinase (GRK1), despite a low degree of gene loss overall and a lack of relaxed selection early during snake evolution. These results provide some of the first evolutionary genomic corroboration for a dim-light ancestor that lacks strong fossorial adaptations. Our results also indicate that snakes with photoreceptor transmutation experienced significantly different selection pressures from other reptiles. Significant positive selection was found primarily in cone-specific genes, but not rod-specific genes, contrary to our expectations. These results reveal potential molecular adaptations associated with photoreceptor transmutation and also highlight unappreciated functional differences between rod- and cone-specific phototransduction proteins. This intriguing example of snake visual system evolution illustrates how the underlying molecular components of a complex system can be reshaped in response to changing selection pressures.
蛇类的视觉系统相对于其他有鳞目动物有很大的改变，这种情况通常被认为反映了它们穴居的起源。在 caenophidian 蛇类中，还观察到了棒状细胞和锥状细胞光感受器之间的进化转变，称为光感受器转换，这种现象在许多谱系中都发生了。然而，之前很少有研究关注这些形态变化的分子进化基础。为了解决这个问题，我们对七种蛇眼转录组进行了测序，并利用新的全基因组和靶向捕获测序数据。我们使用这些数据分析了与蛇类进化起源和光感受器转换相关的光转导基因的基因丢失和选择压力变化。我们发现尽管整体基因丢失程度较低，并且在蛇类进化早期没有放松选择，但 rhodopsin kinase (GRK1) 的惊人丢失。这些结果为缺乏强烈穴居适应的暗光祖先提供了一些进化基因组的首次确证。我们的结果还表明，具有光感受器转换的蛇类经历了与其他爬行动物不同的选择压力。与我们的预期相反，主要在锥状细胞特异性基因中发现了显著的正选择，但在棒状细胞特异性基因中没有发现。这些结果揭示了与光感受器转换相关的潜在分子适应，也突出了棒状细胞和锥状细胞特异性光转导蛋白之间未被认识到的功能差异。这个有趣的蛇类视觉系统进化的例子说明了复杂系统的潜在分子成分如何响应变化的选择压力而重塑。
