Advertisement

Less is more: lemurs (Eulemur spp.) may benefit from loss of trichromatic vision

  • Rachel L. JacobsEmail author
  • Carrie C. Veilleux
  • Edward E. LouisJr
  • James P. Herrera
  • Chihiro Hiramatsu
  • David C. Frankel
  • Mitchell T. Irwin
  • Amanda D. Melin
  • Brenda J. Bradley
Original Article

Abstract

Vertebrate color vision is an ideal system for studying the gains and losses of genetic variation across lineages and impacts on behavior. Among placental mammals, trichromatic vision is unique to primates and is argued to be adaptive for foraging on reddish food. However, trichromacy is variably present in lemurs, including species within the cathemeral genus Eulemur, due to inter- and intra-specific variation in X-linked opsin genes. Although this variation could result from genetic drift, it could also reflect ecological adaptation. To understand ecological contributions to color vision variation, we examined cone opsin genes of 11 Eulemur species. We found that only E. flavifrons and E. macaco have polymorphic trichromacy. Most dichromatic species have an “M” (green-shifted) opsin; uniquely, one species (E. rubriventer) has dichromacy based on an “L” (red-shifted) opsin. This latter result appears to represent loss of polymorphic trichromacy from a dichromatic (M opsin) or polymorphic Eulemur ancestor. To address potential ecological explanations for opsin variation, we studied the dietary behavior of wild E. rubriventer and collected reflectance spectra from plant species consumed. Visual models suggest that trichromacy should provide an advantage for detecting reddish foods; however, luminance contrasts were greatest for dichromats with the L opsin. As E. rubriventer are often active in low-light rainforest conditions, luminance cues may be relatively important, which could favor the L opsin, while also leading to relaxed selection on, or selection against, trichromacy. The presence of different opsin alleles across Eulemur species could represent adaptations related to diet, activity pattern, or habitat.

Significance statement

Loss of genetic variation, often thought to be maladaptive, can occur through natural selection. Among primates, some species have trichromatic color vision, the ability to distinguish reddish and greenish hues; others are red-green colorblind (dichromatic). We examined adaptive explanations for color vision differences by studying cone opsin genes and behavior in wild lemurs (Eulemur)—a genus that is active both day and night. We found that color vision is variable in Eulemur species, and full trichromatic vision was likely lost in at least one lineage. Foraging ecology of dichromatic Eulemur rubriventer indicates that trichromatic vision should be advantageous for foraging on reddish foods, but brightness cues are more salient to this species’ vision. We suggest brightness may be more important than color to this species, particularly at night, and loss of trichromacy could be adaptive in some lemurs.

Keywords

Adaptation Diversity Luminance Opsin Polymorphic trichromacy Sensory ecology 

Notes

Acknowledgements

We thank Benjamin Andriamihaja and MICET, Ministère de l’Environnement, de l’Écologie et des Forêts, Madagascar National Parks, Eileen Larney and the Centre ValBio, and the University of Antananarivo for providing logistical support and research permissions in Madagascar. We thank S. Ambler, C. Angyal, B. Chowdhury, J. Falinomenjanahary, J.P. Lahitsara, A. Minoasy, N. Phelps, T. Randriarimanga, E. Razafimandimby, D. Razafindraibe, J. Razafindramasy, A. Telo, A.V. Tombotiana, Velomaharavo, and J.B. Velontsara for assisting with data collection in Madagascar. We also thank Stephen D. Nash for generously allowing use of his illustrations in this manuscript’s Figs. We thank Lauren Anderson, Melissa T. R. Hawkins, Cynthia Frasier, Shannon Engberg, and Carolyn Bailey for assistance with lab analyses. Finally, we thank three anonymous reviewers for their helpful comments.

Funding

This research was funded in part by the National Science Foundation (DDIG, BCS 1232535), the Leakey Foundation, the Wenner-Gren Foundation, the RW Primate Fund, Yale University, The George Washington University, and the Interdepartmental Doctoral Program in Anthropological Sciences at Stony Brook University.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All behavioral protocols and animal handling procedures were approved by and adhered to institutional animal care requirements (Stony Brook IACUC# 2011-1895, Omaha’s Henry Doorly Zoo and Aquarium IACUC# 97-001, 12-101, and Northern Illinois University IACUC #LA12-0011) and national laws. Data collection, sample collection, and export permits were obtained from Madagascar National Parks, formerly Association Nationale pour la Gestion des Aires Protégées (ANGAP), and the Ministère de l’Environnement, de l’Écologie et des Forêts. Samples were exported/imported under the Convention on International Trade in Endangered Species (CITES) Appendix I permits.

Supplementary material

265_2018_2629_MOESM1_ESM.docx (2.9 mb)
ESM 1 (DOCX 2.90 mb)
265_2018_2629_MOESM2_ESM.txt (3 kb)
ESM 2 (TXT 3.11 kb)
265_2018_2629_MOESM3_ESM.txt (2 kb)
ESM 3 (TXT 2.47 kb)
265_2018_2629_MOESM4_ESM.docx (65 kb)
ESM 4 (DOCX 65 kb)

References

  1. Birkinshaw C (2001) Fruit characteristics of species dispersed by the black lemur (Eulemur macaco) in the Lokobe Forest, Madagascar. Biotropica 33:478–486CrossRefGoogle Scholar
  2. Bollen A, Donati G, Fietz J, Schwab D, Ramanamanjato J-P, Randrihasipara L, van Elsacker L, Ganzhorn J (2005) An intersite comparison of fruit characteristics in Madagascar: evidence for selection pressure through abiotic constraints rather than through co-evolution. In: Dew JL, Boubli JP (eds) Tropical fruits and frugivores: the search for strong interactors. Springer, The Hague, pp 93–119CrossRefGoogle Scholar
  3. Borges R, Khan I, Johnson WE, Gilbert MTP, Zhang G, Jarvis ED, O’Brien SJ, Antunes A (2015) Gene loss, adaptive evolution and the co-evolution of plumage coloration genes with opsins in birds. BMC Genomics 16:751PubMedPubMedCentralCrossRefGoogle Scholar
  4. Bradley BJ, Lawler RR (2011) Linking genotypes, phenotypes, and fitness in wild primate populations. Evol Anthropol 20:104–119PubMedCrossRefGoogle Scholar
  5. Brenneman RA, Johnson SE, Bailey CA, Ingraldi C, Delmore K, Wyman TM, Andriamaharoa HE, Ralainasolo FB, Ratsimbazafy JH, Louis EE Jr (2012) Population genetics and abundance of the endangered grey-headed lemur Eulemur cinereiceps in south-east Madagascar: assessing risks for fragmented and continuous populations. Oryx 46:298–307CrossRefGoogle Scholar
  6. Caine NG, Osorio D, Mundy NI (2010) A foraging advantage for dichromatic marmosets (Callithrix geoffroyi) at low light intensity. Biol Lett 6:36–38PubMedCrossRefGoogle Scholar
  7. Carvalho LS, Davies WL, Robinson PR, Hunt DM (2012) Spectral tuning and evolution of primate short-wavelength-sensitive visual pigments. Proc R Soc Lond B 279:387–393CrossRefGoogle Scholar
  8. Dew JL, Wright P (1998) Frugivory and seed dispersal by four species of primates in Madagascar’s eastern rain forest. Biotropica 30:425–437CrossRefGoogle Scholar
  9. Dominy NJ (2004) Fruits, fingers, and fermentation: the sensory cues available to foraging primates. Integr Comp Biol 44:295–303PubMedCrossRefGoogle Scholar
  10. Dominy NJ, Lucas PW (2001) Ecological importance of trichromatic vision to primates. Nature 410:363–366PubMedCrossRefPubMedCentralGoogle Scholar
  11. Dominy NJ, Lucas PW (2004) Significance of color, calories, and climate to the visual ecology of catarrhines. Am J Primatol 62:189–207PubMedCrossRefPubMedCentralGoogle Scholar
  12. Donati G, Campera M, Balestri M, Serra V, Barresi M, Schwitzer C, Curtis DJ, Santini L (2016) Ecological and anthropogenic correlates of activity patterns in Eulemur. Int J Primatol 37:29–46CrossRefGoogle Scholar
  13. Du Puy DJ, Moat J (1996) A refined classification of the primary vegetation of Madagascar based on the underlying geology: using GIS to map its distribution and to assess its conservation status. In: Lourenço WR (ed) Proceedings of the International Symposium on the Biogeography of Madagascar. Editions de l’ORSTOM, Paris, pp 205–218 + 3 mapsGoogle Scholar
  14. Dulai KS, von Dornum M, Mollon JD, Hunt DM (1999) The evolution of trichromatic color vision by opsin gene duplication in New World and Old World primates. Genome Res 9:629–638PubMedPubMedCentralGoogle Scholar
  15. Endler JA (1993) The color of light in forests and its implications. Ecol Monogr 63:1–27CrossRefGoogle Scholar
  16. Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508CrossRefGoogle Scholar
  17. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140CrossRefGoogle Scholar
  18. Futuyma DJ (1998) Evolutionary biology, 3rd edn. Sinauer Associates Inc, SunderlandGoogle Scholar
  19. Herrera JP, Dávalos LM (2016) Phylogeny and divergence times of lemurs inferred with recent and ancient fossils in the tree. Syst Biol 65:772–791PubMedCrossRefPubMedCentralGoogle Scholar
  20. Higham JP, Brent LJN, Dubuc C, Accamando AK, Engelhardt A, Gerald MS, Heistermann M, Stevens M (2010) Color signal information content and the eye of the beholder: a case study in the rhesus macaque. Behav Ecol 21:739–746PubMedPubMedCentralCrossRefGoogle Scholar
  21. Hiramatsu C, Radlwimmer FB, Yokoyama S, Kawamura S (2004) Mutagenesis and reconstitution of middle-to-long-wave-sensitive visual pigments of New World monkeys for testing the tuning effect of residues at sites 229 and 233. Vis Res 44:2225–2231PubMedCrossRefPubMedCentralGoogle Scholar
  22. Hiramatsu C, Melin AD, Aureli F, Schaffner CM, Vorobyev M, Matsumoto Y, Kawamura S (2008) Importance of achromatic contrast in short-range fruit foraging in primates. PLoS One 3:e3356PubMedPubMedCentralCrossRefGoogle Scholar
  23. Hiramatsu C, Melin A, Allen W, Dubuc C, Higham J (2017) Experimental evidence that primate trichromacy is well suited for detecting primate social colour signals. Proc R Soc B 284:20162458PubMedCrossRefPubMedCentralGoogle Scholar
  24. Hiwatashi T, Okabe Y, Tsutsui T, Hiramatsu C, Melin AD, Oota H, Schaffner CM, Aureli F, Fedigan LM, Innan H, Kawamura S (2010) An explicit signature of balancing selection for colour vision variation in New World monkeys. Mol Biol Evol 27:453–464PubMedCrossRefPubMedCentralGoogle Scholar
  25. Hogan J, Fedigan L, Hiramatsu C, Kawamura S, Melin A (2018) Florivory reveals detection advantage of small, ephemeral resources to trichromatic New World monkeys. Sci Rep 8:10883PubMedPubMedCentralCrossRefGoogle Scholar
  26. Huelsenbeck JP, Nielsen R, Bollback JP (2003) Stochastic mapping of morphological characters. Syst Biol 52:131–158PubMedCrossRefPubMedCentralGoogle Scholar
  27. Hunt DM, Dulai KS, Cowing JA, Julliot C, Mollon JD, Bowmaker JK, Li WH, Hewett-Emmett D (1998) Molecular evolution of trichromacy in primates. Vis Res 38:3299–3306PubMedCrossRefPubMedCentralGoogle Scholar
  28. Jacobs RL, Bradley BJ (2016) Considering the influence of nonadaptive evolution on primate color vision. PLoS One 11:e0149664PubMedPubMedCentralCrossRefGoogle Scholar
  29. Jacobs GH, Deegan JF (1999) Uniformity of colour vision in Old World monkeys. Proc R Soc Lond B 266:2023–2028CrossRefGoogle Scholar
  30. Jacobs GH, Deegan JF (2003) Photopigment polymorphism in prosimians and the origins of primate trichromacy. In: Mollon JD, Pokorny J, Knoblauch K (eds) Normal and defective colour vision. Oxford University Press, Oxford, pp 14–20CrossRefGoogle Scholar
  31. Jacobs GH, Neitz J (1987) Inheritance of color vision in a New World monkey (Saimiri sciureus). Proc Natl Acad Sci U S A 84:2545–2549PubMedPubMedCentralCrossRefGoogle Scholar
  32. Jacobs GH, Neitz J, Neitz M (1993) Genetic basis of polymorphism in the color vision of platyrrhine monkeys. Vis Res 33:269–274PubMedCrossRefGoogle Scholar
  33. Jacobs RL, Spriggs AN, MacFie TS, Baden AL, Irwin MT, Wright PC, Louis EE, Lawler RR, Mundy NI, Bradley BJ (2016) Primate genotyping via high resolution melt analysis: rapid and reliable identification of color vision status in wild lemurs. Primates 57:541–547PubMedCrossRefGoogle Scholar
  34. Jacobs RL, MacFie TS, Spriggs AN et al (2017) Novel opsin gene variation in large-bodied, diurnal lemurs. Biol Lett 13:20170050PubMedPubMedCentralCrossRefGoogle Scholar
  35. Johnsen S, Kelber A, Warrant E, Sweeney AM, Widder EA, Lee RL, Hernández-Andrés J (2006) Crepuscular and nocturnal illumination and its effects on color perception by the nocturnal hawkmoth Deilephila elpenor. J Exp Biol 209:789–800PubMedCrossRefPubMedCentralGoogle Scholar
  36. Johnson WE, Onorato DP, Roelke ME, Land ED, Cunningham M, Belden RC, McBride R, Jansen D, Lotz M, Shindle D, Howard J, Wildt DE, Penfold LM, Hostetler JA, Oli MK, O'Brien SJ (2010) Genetic restoration of the Florida panther. Science 329:1641–1645PubMedCrossRefPubMedCentralGoogle Scholar
  37. Kawamura S, Melin AD (2017) Evolution of genes for color vision and the chemical senses in primates. In: Saitou N (ed) Evolution of the human genome I. Springer, Tokyo, pp 181–216CrossRefGoogle Scholar
  38. Kawamura S, Hiramatsu C, Schaffner CM, Melin AD, Aureli F, Fedigan LM (2012) Polymorphic color vision in primates: evolutionary considerations. In: Hirai H, Imai H, Go Y (eds) Post-genome biology of primates. Springer, Tokyo, pp 93–120CrossRefGoogle Scholar
  39. Lacy RC (1997) Importance of genetic variation to the viability of mammalian populations. J Mammal 78:320–335CrossRefGoogle Scholar
  40. Lei R, Engberg SE, Andriantompohavana R, McGuire SM, Mittermeier RA, Zaonarivelo JR, Brenneman RA, Louis EE Jr (2008) Nocturnal lemur diversity at Masoala National Park. Spec Pub MusTexas Tech Univ 53:1–48Google Scholar
  41. Leonhardt SD, Tung J, Camden JB, Leal M, Drea CM (2009) Seeing red: behavioral evidence of trichromatic color vision in strepsirrhine primates. Behav Ecol 20:1–12CrossRefGoogle Scholar
  42. Maia R, Eliason C, Bitton P, Doucet S, Shawkey M (2013) pavo: an R package for the analysis, visualization and organization of spectral data. Methods Ecol Evol 4:906–913Google Scholar
  43. Markolf M, Rakotonirina H, Fichtel C, von Grumbkow P, Brameier M, Kappeler PM (2013) True lemurs…true species – species delimitation using multiple data sources in the brown lemur complex. BMC Evol Biol 13:233PubMedPubMedCentralCrossRefGoogle Scholar
  44. Martin PR, Grunert U (1999) Analysis of short wavelength sensitive (“blue”) cone mosaic in the primate retina: a comparison of New World and Old World monkeys. J Comp Neurol 406:1–14PubMedCrossRefPubMedCentralGoogle Scholar
  45. Matsumoto Y, Hiramatsu C, Matsushita Y et al (2014) Evolutionary renovation of L/M opsin polymorphism confers a fruit discrimination advantage to ateline New World monkeys. Mol Ecol 7:1799–1812CrossRefGoogle Scholar
  46. Melin AD, Fedigan LM, Hiramatsu C, Sendall CL, Kawamura S (2007) Effects of colour vision phenotype on insect capture by a free-ranging population of white-faced capuchins, Cebus capucinus. Anim Behav 73:205–214CrossRefGoogle Scholar
  47. Melin AD, Fedigan LM, Hiramatsu C, Kawamura S (2008) Polymorphic color vision in white-faced capuchins (Cebus capucinus): is there foraging niche divergence among phenotypes? Behav Ecol Sociobiol 62:659–670CrossRefGoogle Scholar
  48. Melin AD, Fedigan LM, Young HC, Kawamura S (2010) Can color vision variation explain sex differences in invertebrate foraging by capuchin monkeys? Curr Zool 56:300–312Google Scholar
  49. Melin AD, Moritz GL, Fosbury RAE, Kawamura S, Dominy NJ (2012) Why aye-ayes see blue. Am J Primatol 74:185–192PubMedCrossRefGoogle Scholar
  50. Melin AD, Matsushita Y, Moritz G, Dominy NJ, Kawamura S (2013) Inferred M/L cone opsin polymorphism of ancestral tarsiers sheds dim light on the origin of anthropoid primates. Proc R Soc B 208:1759Google Scholar
  51. Melin AD, Chiou K, Walco E, Bergstrom M, Kawamura S, Fedigan LM (2017a) Trichromacy increases fruit intake rates of wild capuchins (Cebus capucinus imitator). Proc Natl Acad Sci U S A 114:10402–10407PubMedPubMedCentralCrossRefGoogle Scholar
  52. Melin AD, Khetpal V, Matsushita Y, Zhou K, Campos FA, Welker B, Kawamura S (2017b) Howler monkey foraging ecology suggests convergent evolution of routine trichromacy as an adaptation for folivory. Ecol Evol 7:1421–1434PubMedPubMedCentralCrossRefGoogle Scholar
  53. Mittermeier RA, Louis EE, Richardson M et al (2010) Lemurs of Madagascar, 3rd edn. Conservation International, ArlingtonGoogle Scholar
  54. Nathans J (1999) The evolution and physiology of human color vision: insights from molecular genetic studies of visual pigments. Neuron 24:299–312PubMedCrossRefPubMedCentralGoogle Scholar
  55. Neitz M, Neitz J, Jacobs GH (1991) Spectral tuning of pigments underlying red-green color vision. Science 252:971–974PubMedCrossRefPubMedCentralGoogle Scholar
  56. Nevo O, Valenta K, Razafimandimby D, Melin AD, Ayasse M, Chapman CA (2018) Frugivores and the evolution of fruit colour. Biol Lett 14:20180377PubMedCrossRefPubMedCentralGoogle Scholar
  57. Nsubuga AM, Robbins MM, Roeder AD, Morin PA, Boesch C, Vigilant L (2004) Factors affecting the amount of genomic DNA extracted from ape faeces and the identification of an improved sample storage method. Mol Ecol 13:2089–2094PubMedCrossRefPubMedCentralGoogle Scholar
  58. Olsson P, Lind O, Kelber K (2018) Chromatic and achromatic vision: parameter choice and limitations for reliable model predictions. Behav Ecol 29:273–282CrossRefGoogle Scholar
  59. Osorio D, Vorobyev M (2018) Principles and application of the receptor noise model of color discrimination: a comment on Olsson et al. Behav Ecol 29:283–284CrossRefGoogle Scholar
  60. Osorio D, Ruderman DL, Cronin TW (1998) Estimation of errors in luminance signals encoded by primate retina resulting from sampling of natural images with red and green cones. J Opt Soc Am A 15:16–22CrossRefGoogle Scholar
  61. Osorio D, Smith AC, Vorobyev M, Buchanan-Smith HM (2004) Detection of fruit and the selection of primate visual pigments for color vision. Am Nat 164:696–708PubMedCrossRefPubMedCentralGoogle Scholar
  62. Overdorff DJ (1996) Ecological correlates to activity and habitat use of two prosimian primates: Eulemur rubriventer and Eulemur fulvus rufus in Madagascar. Am J Primatol 40:327–342CrossRefGoogle Scholar
  63. Pariente GF (1980) Quantitative and qualitative study of the light available in the natural biotope of Malagasy prosimians. In: Charles-Dominique P, Cooper HM, Hladik A, Hladik CM, Pages E, Pariente GF, Petter-Rousseaux A, Petter JJ, Schilling A (eds) Nocturnal Malagasy primates: ecology, physiology and behaviour. Academic Press, New York, pp 117–134Google Scholar
  64. Pessoa D, Maia R, Ajuz R, Moraes P, Spyrides M, Pessoa V (2014) The adaptive value of primate color vision for predator detection. Am J Primatol 76:721–729PubMedCrossRefPubMedCentralGoogle Scholar
  65. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna https://www.R-project.org/ Google Scholar
  66. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna https://www.R-project.org/ Google Scholar
  67. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237CrossRefGoogle Scholar
  68. Regan BC, Julliot C, Simmen B, Vienot F, Charles-Dominique P, Mollon JD (2001) Fruits, foliage and the evolution of primate colour vision. Philos Trans R Soc B 356:229–283CrossRefGoogle Scholar
  69. Rennison DJ, Owens GL, Taylor GS (2012) Opsin gene duplication and divergence in ray-finned fish. Mol Phylogenet Evol 62:986–1008PubMedCrossRefPubMedCentralGoogle Scholar
  70. Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223CrossRefGoogle Scholar
  71. Roth LSV, Balkenius A, Kelber A (2008) The absolute threshold of colour vision in the horse. PLoS One 3:e3711PubMedPubMedCentralCrossRefGoogle Scholar
  72. Sambrook J, Fritch EF, Maniatus T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Press, New YorkGoogle Scholar
  73. Smith AC, Surridge AK, Prescott MJ, Osorio D, Mundy NI, Buchanan-Smith HM (2012) The effect of colour vision status on insect prey capture efficiency by captive and wild tamarins (Saguinus spp.). Anim Behav 83:479–486CrossRefGoogle Scholar
  74. Springer MS, Meredith RW, Gatesy J, Emerling CA, Park J, Rabosky DL, Stadler T, Steiner C, Ryder OA, Janečka JE, Fisher CA, Murphy WJ (2012) Macroevolutionary dynamics and historical biogeography of primate diversification inferred from a species supermatrix. PLoS One 7:e49521PubMedPubMedCentralCrossRefGoogle Scholar
  75. Sumner P, Mollon JD (2000) Catarrhine photopigments are optimized for detecting targets against a foliage background. J Exp Biol 203:1963–1986PubMedGoogle Scholar
  76. Surridge AK, Osorio D, Mundy NI (2003) Evolution and selection of trichromatic vision in primates. Trends Ecol Evol 18:198–205CrossRefGoogle Scholar
  77. Tan Y, Li WH (1999) Vision - trichromatic vision in prosimians. Nature 402(36):36PubMedCrossRefGoogle Scholar
  78. Valenta K, Burke RJ, Styler SA, Jackson DA, Melin AD, Lehman SM (2013) Colour and odour drive fruit selection and seed dispersal by mouse lemurs. Sci Rep 3:2424PubMedPubMedCentralCrossRefGoogle Scholar
  79. Valenta K, Edwards M, Rafaliarison RR, Johnson SE, Holmes SM, Brown KA, Dominy NJ, Lehman SM, Parra EJ, Melin AD (2016) Visual ecology of true lemurs suggests a cathemeral origin for the primate cone opsin polymorphism. Funct Ecol 30:932–942CrossRefGoogle Scholar
  80. Veilleux CC, Bolnick DA (2009) Opsin gene polymorphism predicts trichromacy in a cathemeral lemur. Am J Primatol 71:86–90PubMedCrossRefPubMedCentralGoogle Scholar
  81. Veilleux CC, Cummings ME (2012) Nocturnal light environments and species ecology: implications for nocturnal color vision in forests. J Exp Biol 215:4085–4096PubMedCrossRefPubMedCentralGoogle Scholar
  82. Veilleux CC, Jacobs RL, Cummings ME, Louis EE, Bolnick DA (2014) Opsin genes and visual ecology in a nocturnal folivorous lemur. Int J Primatol 35:88–107CrossRefGoogle Scholar
  83. Veilleux CC, Scarry CJ, Di Fiore A, Kirk EC, Bolnick DA, Lewis RJ (2016) Group benefit associated with polymorphic trichromacy in a Malagasy primate (Propithecus verreauxi). Sci Rep 6:38418PubMedPubMedCentralCrossRefGoogle Scholar
  84. Vogel ER, Neitz M, Dominy NJ (2007) Effect of color vision phenotype on the foraging of wild white-faced capuchins, Cebus capucinus. Behav Ecol 18:292–297CrossRefGoogle Scholar
  85. Williams AJ, Hunt DM, Bowmaker JK, Mollon JD (1992) The polymorphic photopigments of the marmoset: spectral tuning and genetic basis. EMBO J 11:2039–2045PubMedPubMedCentralCrossRefGoogle Scholar
  86. Wright PC (1992) Primate ecology, rainforest conservation, and economic development: building a national park in Madagascar. Evol Anthropol 1:25–33CrossRefGoogle Scholar
  87. Wyszecki G, Stiles WS (1982) Color science: concepts and methods, quantitative data and formulae, 2nd edn. Wiley, New YorkGoogle Scholar
  88. Yamashita N, Stoner K, Riba-Hernández P, Dominy N, Lucas P (2005) Light levels used during feeding by primate species with different color vision phenotypes. Behav Ecol Sociobiol 58:618–629CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Rachel L. Jacobs
    • 1
    Email author
  • Carrie C. Veilleux
    • 2
  • Edward E. LouisJr
    • 3
  • James P. Herrera
    • 4
  • Chihiro Hiramatsu
    • 5
    • 6
  • David C. Frankel
    • 1
  • Mitchell T. Irwin
    • 7
  • Amanda D. Melin
    • 2
    • 8
  • Brenda J. Bradley
    • 1
  1. 1.Center for the Advanced Study of Human Paleobiology, Department of AnthropologyThe George Washington UniversityWashingtonUSA
  2. 2.Department of Anthropology and ArchaeologyUniversity of CalgaryCalgaryCanada
  3. 3.Conservation Genetics DepartmentOmaha’s Henry Doorly Zoo and AquariumOmahaUSA
  4. 4.Department of Evolutionary AnthropologyDuke UniversityDurhamUSA
  5. 5.Department of Human Science, Faculty of DesignKyushu UniversityFukuokaJapan
  6. 6.Physiological Anthropology Research CenterKyushu UniversityFukuokaJapan
  7. 7.Department of AnthropologyNorthern Illinois UniversityDeKalbUSA
  8. 8.Department of Medical Genetics and Alberta Children’s Hospital Research InstituteUniversity of CalgaryCalgaryCanada

Personalised recommendations