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Howler monkey foraging ecology suggests convergent evolution of routine trichromacy as an adaptation for folivory

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 Aloua...

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Autores principales: Melin, Amanda D., Khetpal, Vishal, Matsushita, Yuka, Zhou, Kaile, Campos, Fernando A., Welker, Barbara, Kawamura, Shoji
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5330884/
https://www.ncbi.nlm.nih.gov/pubmed/28261454
http://dx.doi.org/10.1002/ece3.2716
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author Melin, Amanda D.
Khetpal, Vishal
Matsushita, Yuka
Zhou, Kaile
Campos, Fernando A.
Welker, Barbara
Kawamura, Shoji
author_facet Melin, Amanda D.
Khetpal, Vishal
Matsushita, Yuka
Zhou, Kaile
Campos, Fernando A.
Welker, Barbara
Kawamura, Shoji
author_sort Melin, Amanda D.
collection PubMed
description 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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spelling pubmed-53308842017-03-03 Howler monkey foraging ecology suggests convergent evolution of routine trichromacy as an adaptation for folivory Melin, Amanda D. Khetpal, Vishal Matsushita, Yuka Zhou, Kaile Campos, Fernando A. Welker, Barbara Kawamura, Shoji Ecol Evol Original Research 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. John Wiley and Sons Inc. 2017-02-04 /pmc/articles/PMC5330884/ /pubmed/28261454 http://dx.doi.org/10.1002/ece3.2716 Text en © 2017 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution (http://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research
Melin, Amanda D.
Khetpal, Vishal
Matsushita, Yuka
Zhou, Kaile
Campos, Fernando A.
Welker, Barbara
Kawamura, Shoji
Howler monkey foraging ecology suggests convergent evolution of routine trichromacy as an adaptation for folivory
title Howler monkey foraging ecology suggests convergent evolution of routine trichromacy as an adaptation for folivory
title_full Howler monkey foraging ecology suggests convergent evolution of routine trichromacy as an adaptation for folivory
title_fullStr Howler monkey foraging ecology suggests convergent evolution of routine trichromacy as an adaptation for folivory
title_full_unstemmed Howler monkey foraging ecology suggests convergent evolution of routine trichromacy as an adaptation for folivory
title_short Howler monkey foraging ecology suggests convergent evolution of routine trichromacy as an adaptation for folivory
title_sort howler monkey foraging ecology suggests convergent evolution of routine trichromacy as an adaptation for folivory
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5330884/
https://www.ncbi.nlm.nih.gov/pubmed/28261454
http://dx.doi.org/10.1002/ece3.2716
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