Doctoral Dissertation Improvement: Ecological Correlates of Differential Selection on S Opsin Genes in Nocturnal Primates

大多数哺乳动物具有两种类型的视网膜视锥细胞，用于辨别颜色：(1)对蓝色和紫罗兰色最敏感的短波敏视锥(S)视锥；(2)对绿色和黄色最敏感的中/长波长视锥(M/L)视锥。然而，最近的研究发现，编码产生S视锥的S视蛋白基因已经发生突变，并在几种夜间活动的灵长类动物(百合目动物、半尾猴和猫头鹰猴子)中失去了功能。相比之下，S视蛋白基因在其他夜间活动的灵长类动物(眼镜猴和大多数狐猴)中仍然具有功能。夜间活动的非灵长类哺乳动物在有或没有S视锥的情况下也表现出类似的变化。目前，S锥在灵长类动物和其他哺乳动物体内的存留或消失的生态因素尚不清楚。这项研究将考察环境光的变化对夜间灵长类动物保留或失去S视锥的进化压力的影响。更具体地说，这项研究将检验这样一种预测，即生活在短波长光丰富的夜间环境中的灵长类动物将经历更多的选择，以维持功能上的S视蛋白基因。相反，居住在短波长光下的夜间环境中的灵长类动物预计将经历宽松的选择，以维持S视蛋白基因的功能。为了实现这一目标，将在来自五个属(Avahi，Cheirogaleus，Lepelemur，Microcebus和Phaner)的大样本夜间活动狐猴中对S视蛋白基因进行测序。这些属的物种是马达加斯加三种不同的生境类型(多刺森林、干燥落叶森林和热带雨林)中的一种特有物种，根据树叶密度的不同，这三种类型的短波长光的可用性预计会有所不同。S视蛋白基因最近的进化史将直接用于所有物种，使用统计检验可以区分净化选择(即为保持基因功能的选择)和放松选择以保持基因功能。样本的大小和宽度(来自20个物种的152个个体)将允许进行种内和种间选择测试。为了了解生境光照对灵长类动物色觉进化的影响，比较不同生境类型的同类物种对S视蛋白基因的选择类型和选择强度。确定S视锥细胞保留或消失所涉及的选择因素是理解为什么只有一些夜间活动的灵长类动物失去了S视锥细胞而其他灵长类动物保留了它们的原因。目前还存在关于哪种活动模式是现存灵长类动物最后共同祖先的特征的争论。通过测试夜间活动物种中S视锥保留的适应性解释，该项目将有助于解决关于基础灵长类活动模式的分歧，从而对评估当前灵长类起源的适应性假说具有重要意义。此外，确定S视锥细胞丢失的适应性框架将使基于S视蛋白表达变化的灵长类和哺乳动物谱系的古环境重建成为可能。最后，该项目将公开目前为止组装的最大的夜间灵长类动物S视蛋白基因序列样本，并为研究生和本科生提供教育经验和培训。

Most mammals possess two types of retinal cone photoreceptors for color discrimination: (1) short-wavelength-sensitive (S) cones that are most responsive to blues and violets, and (2) medium/long-wavelength-sensitive (M/L) cones that are most responsive to greens and yellows. However, recent research has revealed that the S opsin gene, which codes for the production of S cones, has mutated and lost functionality in several groups of nocturnal primates (lorises, galagos, and owl monkeys). By contrast, the S opsin gene has remained functional in other nocturnal primate groups (tarsiers and most lemurs). Nocturnal non-primate mammals exhibit similar variation in the presence or absence of S cones. Currently the ecological factors involved in the retention or loss of the S cone in primates and other mammals are unclear. This research will examine the influence of variation in ambient light on evolutionary pressures for nocturnal primates to retain or lose their S cones. More specifically, this research will test the prediction that primates inhabiting nocturnal environments rich in short-wavelength light will experience increased selection to maintain a functional S opsin gene. Conversely, primates inhabiting nocturnal environments impoverished in short-wavelength light are expected to experience relaxed selection to maintain S opsin gene functionality. To achieve this goal, the S opsin gene will be sequenced in a large sample of nocturnal lemurs from five genera (Avahi, Cheirogaleus, Lepilemur, Microcebus, and Phaner). Species of these genera are endemic to one of three distinct habitat types in Madagascar (spiny forests, dry deciduous forests, and rainforests) that are expected to vary in the availability of short-wavelength light based on differences in foliage density. The recent evolutionary history of the S opsin gene will be directly examined for all species using statistical tests that can discriminate between purifying selection (i.e., selection to maintain the function of a gene) and relaxed selection to maintain gene functionality. The sample size and breadth (152 individuals from 20 species) will permit both within-species and between-species selection tests. The type and strength of selection acting on the S opsin gene will be compared between congeneric species from different habitat types in order to understand the effects of habitat light on the evolution of primate color vision.Identifying the selective factors involved in the retention or loss of S cones is fundamental to understanding why only some nocturnal primates and have lost their S cones while others have retained them. There is also currently debate regarding which activity pattern characterized the last common ancestor of living primates. By testing an adaptive explanation for S cone retention in nocturnal species, this project will help to resolve disagreements about the activity patterns of basal primates and is thus important for evaluating current adaptive hypotheses of primate origins. Additionally, identifying an adaptive framework for S cone loss would permit paleoenvironmental reconstructions for primate and mammalian lineages based on variation in S opsin expression. Finally, this project will make publicly available the largest sample of nocturnal primate S opsin gene sequences yet assembled and provide educational experience and training for both graduate and undergraduate students.