title: Howler monkey foraging ecology suggests convergent evolution of routine trichromacy as an adaptation for folivory.
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 (genusAlouatta) 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, sequencedM/LWSopsin genes in four social groups ofAlouatta palliata,and conducted colorimetric analysis of leaves consumed in Sector Santa Rosa, Costa Rica. For a majority of food species, includingFicustrees, 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 wereMWS/LWShybrids; when combined with previous research, the incidence of hybridM/LWSopsins 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.
authors.affiliation: Department of Anthropology and Archaeology University of Calgary Calgary AB Canada; Department of Medical Genetics and Alberta Children's Hospital Research Institute University of Calgary Calgary AB Canada.
authors.forename: Amanda D
authors.initials: AD
authors.lastname: Melin
authors.affiliation: Department of Anthropology Washington University in St. Louis St. Louis MO USA.
authors.forename: Vishal
authors.initials: V
authors.lastname: Khetpal
authors.affiliation: Department of Integrated Biosciences Graduate School of Frontier Sciences The University of Tokyo Tokyo Japan.
authors.forename: Yuka
authors.initials: Y
authors.lastname: Matsushita
authors.affiliation: Department of Integrated Biosciences Graduate School of Frontier Sciences The University of Tokyo Tokyo Japan; Department of Plant Protection College of Agriculture and Biotechnology Zhejiang University Hangzhou Zhejiang China.
authors.forename: Kaile
authors.initials: K
authors.lastname: Zhou
authors.affiliation: Department of Anthropology and Archaeology University of Calgary Calgary AB Canada; Department of Anthropology Tulane University New Orleans LA USA.
authors.forename: Fernando A
authors.initials: FA
authors.lastname: Campos
authors.affiliation: Department of Anthropology State University of New York at Geneseo Geneseo NY USA.
authors.forename: Barbara
authors.initials: B
authors.lastname: Welker
authors.affiliation: Department of Integrated Biosciences Graduate School of Frontier Sciences The University of Tokyo Tokyo Japan.
authors.forename: Shoji
authors.initials: S
authors.lastname: Kawamura
keywords: Alouatta; Ficus; color vision; molecular evolution; opsin; polymorphism; primate evolution; sensory ecology