Howler monkey foraging ecology suggests convergent evolution of routine trichromacy as an adaptation for folivory |
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| Authors: | Amanda D Melin Vishal Khetpal Yuka Matsushita Kaile Zhou Fernando A Campos Barbara Welker Shoji Kawamura |
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| Institution: | 1. Department of Anthropology and Archaeology, University of Calgary, Calgary, AB, Canada;2. Department of Medical Genetics and Alberta Children’s Hospital Research Institute, University of Calgary, Calgary, AB, Canada;3. Department of Anthropology, Washington University in St. Louis, St. Louis, MO, USA;4. Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Tokyo, Japan;5. Department of Plant Protection, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, Zhejiang, China;6. Department of Anthropology, Tulane University, New Orleans, LA, USA;7. Department of Anthropology, State University of New York at Geneseo, Geneseo, NY, USA |
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| Abstract: | Primates possess remarkably variable color vision, and the ecological and social factors shaping this variation remain heavily debated. Here, we test whether central tenants of the folivory hypothesis of routine trichromacy hold for the foraging ecology of howler monkeys. Howler monkeys (genus Alouatta) and paleotropical primates (Parvorder: Catarrhini) have independently acquired routine trichromacy through fixation of distinct mid‐ to long‐wavelength‐sensitive (M/LWS) opsin genes on the X‐chromosome. The presence of routine trichromacy in howlers, while other diurnal neotropical monkeys (Platyrrhini) possess polymorphic trichromacy, is poorly understood. A selective force proposed to explain the evolution of routine trichromacy in catarrhines—reliance on young, red leaves—has received scant attention in howlers, a gap we fill in this study. We recorded diet, sequenced M/LWS opsin genes in four social groups of Alouatta palliata, and conducted colorimetric analysis of leaves consumed in Sector Santa Rosa, Costa Rica. For a majority of food species, including Ficus trees, an important resource year‐round, young leaves were more chromatically conspicuous from mature leaves to trichromatic than to hypothetical dichromatic phenotypes. We found that 18% of opsin genes were MWS/LWS hybrids; when combined with previous research, the incidence of hybrid M/LWS opsins in this species is 13%. In visual models of food discrimination ability, the hybrid trichromatic phenotype performed slightly poorer than normal trichromacy, but substantially better than dichromacy. Our results provide support for the folivory hypothesis of routine trichromacy. Similar ecological pressures, that is, the search for young, reddish leaves, may have driven the independent evolution of routine trichromacy in primates on separate continents. We discuss our results in the context of balancing selection acting on New World monkey opsin genes and hypothesize that howlers experience stronger selection against dichromatic phenotypes than other sympatric species, which rely more heavily on cryptic foods. |
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| Keywords: |
Alouatta
color vision
Ficus
molecular evolution opsin polymorphism primate evolution sensory ecology |
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