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Opsin Genes and Visual Ecology in a Nocturnal Folivorous Lemur

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Abstract

Primate color vision has traditionally been examined in the context of diurnal activity, but recent genetic and ecological studies suggest that color vision plays a role in nocturnal primate behavior and ecology as well. In this study, we united molecular analyses of cone visual pigment (opsin) genes with visual modeling analyses of food items to explore the evolution of color vision in the folivorous woolly lemur (genus Avahi). Previous studies have shown that leaf quality, e.g., protein content, leaf toughness, and protein/toughness ratio, is significantly correlated with green-red and blue-yellow chromatic differences, suggesting a potential role of color in leaf discrimination in Avahi, and, consequently, a potential adaptive advantage to color vision in this taxon. Phylogenetic selection tests determined that the strength of selection on the SWS1 opsin gene to retain blue-sensitive SWS cones did not significantly differ in Avahi compared to day-active primates. Genotyping of the M/LWS opsin gene in 60 individuals from nine species found that the 558-nm-sensitive (red-sensitive) allele is conserved across all Avahi. Finally, we measured spectral reflectance from five species of young leaves consumed by Avahi and background foliage in Ranomafana National Park and modeled performance of possible S and M/L pigment pairs for detecting these food items under different nocturnal illuminations (e.g. twilight, moonlight). We found that the observed cone pigment pair in Avahi was optimally tuned for color-based detection of young green leaves in all nocturnal light environments, suggesting a potential adaptive role of nocturnal color vision in selection for dichromacy in this genus.

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Acknowledgments

We thank Amanda Melin and Lauren Brent for the opportunity to participate in this special issue and two anonymous reviewers for invaluable comments. We are grateful to Clara Scarry, Kelsey Ellis, Caroline Bailey (OHDZA), and Cynthia Fraser (OHDZA) for comments, discussion, and laboratory assistance. We want to acknowledge the staff, drivers, and field teams of the Madagascar Biodiversity Partnership, ONG for collecting the Avahi genetic samples. We thank the Ministére des Eaux et Foréts, University of Antananarivo, and Madagascar National Parks for permission to conduct research in Madagascar; Institute for the Conservation of Tropical Environments (USA and Madagascar); Centre ValBio staff, especially Rasabo Paul and Pela Auguste for assisting with plant sample identification and collection. We further thank Conservation International, Margot Marsh Biodiversity Foundation, Primate Action Fund, Primate Conservation, Inc., and OHDZA for supporting field expeditions to collect genetic samples; the University of Texas at Austin for research funds to D. A. Bolnick; and Wenner-Gren Foundation, Leakey Foundation, and National Science Foundation (DDIG, BSC 1232535) to R. L. Jacobs for plant sample analysis in Madagascar.

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Authors and Affiliations

  1. Department of Anthropology, University of Texas at Austin, Austin, Texas, 78712, USA

    Carrie C. Veilleux

  2. Interdepartmental Doctoral Program in Anthropological Sciences, Stony Brook University, Stony Brook, New York, 11794, USA

    Rachel L. Jacobs

  3. Section of Integrative Biology, University of Texas at Austin, Austin, Texas, 78712, USA

    Molly E. Cummings

  4. Molecular Genetics, Omaha’s Henry Doorly Zoo and Aquarium, Omaha, Nebraska, 68107, USA

    Edward E. Louis

  5. Department of Anthropology and Population Research Center, University of Texas at Austin, Austin, Texas, 78712, USA

    Deborah A. Bolnick

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  1. Carrie C. Veilleux
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Correspondence to Carrie C. Veilleux.

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Veilleux, C.C., Jacobs, R.L., Cummings, M.E. et al. Opsin Genes and Visual Ecology in a Nocturnal Folivorous Lemur. Int J Primatol 35, 88–107 (2014). https://doi.org/10.1007/s10764-013-9708-6

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