Testing the niche differentiation hypothesis in wild capuchin monkeys with polymorphic color vision

The polymorphic color vision system of most North, Central, and South American monkeys is a textbook case of balancing selection, yet the mechanism behind it is poorly understood. Previous work has established task-specific foraging advantages to different color vision phenotypes: dichromats (red-green colorblind) are more efficient foraging for invertebrates, while trichromats (color "normal" relative to humans) are more efficient foraging for "reddish" ripe fruit, suggesting that niche differentiation may underlie the maintenance of color vision variation. We explore a prediction of the niche differentiation hypothesis by asking whether dichromatic and trichromatic capuchin monkeys (Cebus imitator) diverge in their foraging activity budget, specifically testing whether dichromats forage more frequently for invertebrates and trichromats forage more frequently for "reddish" ripe fruit. To assess this, we analyze a large dataset of behavioral scan samples (n = 21,984) from 48 wild adult female capuchins of known color vision genotype, dominance rank and reproductive status, together with models of food conspicuity. We find no significant differences between dichromats and trichromats in the frequency of scans spent foraging for different food types but do find that nursing females forage less overall than cycling females. Our results suggest that the potential for color vision-based niche differentiation in foraging time may be curtailed by the energetic requirements of reproduction, behavioral synchrony caused by group-living, and/or individual preferences. While niche differentiation in activity budgets by color vision type is not apparent, fine-scale niche differentiation may be occurring. This research enhances our understanding of the evolutionary processes maintaining sensory polymorphisms.

绝大多数北美、中美洲以及南美洲猴类的多态性色觉系统，是平衡选择（balancing selection）的经典教科书案例，但其背后的维持机制仍未得到充分阐释。既往研究已证实，不同色觉表型（color vision phenotype）具备特化的觅食优势：二色视觉者（dichromats，红绿色盲）在搜寻无脊椎动物时效率更高，而三色视觉者（trichromats，相对于人类的正常色觉）则更擅长觅取"泛红"的成熟果实，这提示生态位分化（niche differentiation）可能是色觉变异得以维持的核心机制。本研究针对生态位分化假说的一项预测展开验证：检验二色视觉与三色视觉的卷尾猴（Cebus imitator）在觅食活动预算上是否存在差异，具体验证二色视觉者是否更频繁地搜寻无脊椎动物，而三色视觉者是否更常觅取"泛红"成熟果实。为验证上述假设，本研究分析了一项大型行为扫描采样（behavioral scan samples）数据集（样本量n=21,984），数据来源于48只已知色觉基因型、优势等级与繁殖状态的野生成年雌性卷尾猴，同时结合了食物显眼度（food conspicuity）模型。研究结果显示，二色视觉者与三色视觉者在针对不同食物类型的觅食扫描频次上并无显著差异，但哺乳雌性的整体觅食频次显著低于发情周期雌性。本研究结果表明，基于色觉的觅食时间生态位分化潜力，可能因繁殖的能量需求、群居行为引发的活动同步性，以及/或是个体偏好而受到限制。尽管基于色觉类型的活动预算生态位分化并不显著，但精细尺度的生态位分化仍有可能存在。本研究有助于深化我们对维持感觉多态性的进化过程的理解。