Data from: Evolutionary renovation of L/M opsin polymorphism confers a fruit discrimination advantage to ateline New World monkeys

New World monkeys exhibit prominent color vision variation due to allelic polymorphism of the long-to-middle wavelength (L/M) opsin gene. The known spectral variation of L/M opsins in primates is broadly determined by amino acid composition at three sites: 180, 277 and 285 (the “three-sites” rule). However, two L/M opsin alleles found in the black-handed spider monkeys (Ateles geoffroyi) are known exceptions, presumably due to novel mutations. The spectral separation of the two L/M photopigments is 1.5 times greater than expected based on the “three-sites” rule. Yet the consequence of this for the visual ecology of the species is unknown, as is the evolutionary mechanism by which spectral shift was achieved. In the present study, we first examine L/M opsins of two other Atelinae species, the long-haired spider monkeys (A. belzebuth) and the common woolly monkeys (Lagothrix lagotricha). By a series of site-directed mutagenesis, we show that a mutation Y213D (tyrosine to aspartic acid at site 213) in the ancestral opsin of the two alleles enabled N294K, which occurred in one allele of the ateline ancestor, and increased the spectral separation between the two alleles. Second, by modeling the chromaticity of dietary fruits and background leaves in a natural habitat of spider monkeys, we demonstrate that chromatic discrimination of fruit from leaves is significantly enhanced by these mutations. This evolutionary renovation of L/M opsin polymorphism in atelines illustrates a previously unappreciated dynamism of opsin genes in shaping primate color vision.

新大陆猴因长中波（long-to-middle wavelength, L/M）视蛋白（opsin）基因的等位基因多态性，呈现出显著的色觉变异。已知灵长类L/M视蛋白的光谱变异大体由180、277和285三个位点的氨基酸组成决定，即所谓的“三位点规则”。然而，黑掌蜘蛛猴（Ateles geoffroyi）中发现的两种L/M视蛋白等位基因属于已知例外，推测由新型突变所致。这两种L/M感光色素的光谱间距较“三位点规则”的预期值高出1.5倍，但该变异对该物种视觉生态的影响，以及实现光谱偏移的进化机制，目前仍属未知。本研究首先对另外两种蛛猴亚科（Atelinae）物种的L/M视蛋白展开研究：长毛蜘蛛猴（A. belzebuth）与普通绒毛猴（Lagothrix lagotricha）。通过一系列定点诱变（site-directed mutagenesis）实验，我们证实：在两种等位基因的祖先视蛋白中发生的Y213D突变（213位酪氨酸突变为天冬氨酸），使得蛛猴亚科祖先等位基因中出现的N294K突变得以发挥功能，进而增大了两种等位基因间的光谱间距。其次，通过对蜘蛛猴自然栖息地内膳食果实与背景叶片的色品（chromaticity）进行建模分析，我们证明上述突变可显著提升果实与叶片的色彩辨别能力。蛛猴亚科L/M视蛋白多态性的这一进化革新，揭示了视蛋白基因在塑造灵长类色觉过程中一种此前未被重视的动态特性。