The Evolutionary Ecology of Primate Hair Coloration: A Phylogenetic Approach

Abstract

Understanding trait evolution is essential for explaining modern biological diversity, and this is particularly exemplified by studies of coloration. Recent studies have applied evolutionary models to understand animal coloration, yet we have limited knowledge of how this trait evolves in mammals in a comparative context. Here we use phylogenetic methods to examine how different traits are associated with the evolutionary diversity of primate hair color. We hypothesize that hair color evolves independently across body regions, and that variation in biological and ecological traits influence patterns of hair color evolution. To test this, we quantify the phylogenetic signal of coloration for each body region, then compare the fit of three evolutionary models and a null, non-phylogenetic model to explain color variation across 94 primate species. We then test how trait optima and rate of color evolution covary with biological traits, clade membership, and habitat. Phylogenetic signal varies across regions, with head and forelimb coloration exhibiting the highest values. Head and forelimb coloration is best explained by an Ornstein-Uhlenbeck model, which could suggest stabilizing selection, whereas a null model best fits other body regions. Rates of hair color evolution and optimal color values vary across species with different visual systems, activity patterns, habitat types, and clade memberships. These results suggest that selective pressures are acting independently across body regions and across different primate taxa. Our results emphasize the importance of investigating patterns of trait evolution across regions of the body, as well as incorporating relevant biological and ecological traits into evolutionary models.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

Data Availability

Data are archived via the Dryad Digital Repository https://doi.org/10.5061/dryad.dbrv15f16.

Code Availability

Code is archived via the Dryad Digital Repository https://doi.org/10.5061/dryad.dbrv15f16.

References

  1. Allen WL, Moreno N, Gamble T, Chiari Y (2020) Ecological, behavioral, and phylogenetic influences on the evolution of dorsal color pattern in geckos. Evolution 74(6):1033–1047

    PubMed  Article  Google Scholar 

  2. Allen WL, Stevens M, Higham JP (2014) Character displacement of Cercopithecini primate visual signals. Nat Commun 5:1–10

    Article  CAS  Google Scholar 

  3. Anderson TM, Candille SI, Musiani M, Greco C, Stahler DR, Smith DW, Padhukasahasram B, Randi E, Leonard JA, Bustamante CD, Ostrander EA, Tang H, Wayne RK, Barsh GS (2009) Molecular and evolutionary history of melanism in North American gray wolves. Science 323(5919):1339–1343

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  4. Arnold C, Matthews J, Nunn CL (2010) The 10kTrees website: a new online resource for primate phylogeny. Evol Anthropol 19:114–118

    Article  Google Scholar 

  5. Baker J, Venditti C (2019) Rapid change in mammalian eye shape is explained by activity pattern. Curr Biol 29(6):1082–1088

    CAS  PubMed  Article  Google Scholar 

  6. Bell RC, Webster GN, Whiting MJ (2017) Breeding biology and the evolution of dynamic sexual dichromatism in frogs. J Evol Biol 30(12):2104–2115

    CAS  PubMed  Article  Google Scholar 

  7. Bergeron ZT, Fuller RC (2018) Using human vision to detect variation in avian coloration: how bad is it? Am Nat 191:269–276

    PubMed  Article  Google Scholar 

  8. Bergman TJ, Ho L, Beehner JC (2009) Chest color and social status in male geladas (Theropithecus gelada). Int J Primatol 30(6):791–806

    Article  Google Scholar 

  9. Bradley BJ, Gerald MS, Widdig A, Mundy NI (2013) Coat color variation and pigmentation gene expression in rhesus macaques (Macaca mulatta). J Mammal Evol 20:263–270

    Article  Google Scholar 

  10. Bradley BJ, Mundy NI (2008) The primate palette: the evolution of primate coloration. Evol Anthropol 17:97–111

    Article  Google Scholar 

  11. Burnham KP, Anderson DR (2003) Model Selection and Multimodel Inference: A Practical Information-theoretic Approach. Springer Science and Business Media, Berlin

    Google Scholar 

  12. Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65(1):23–35

    Article  Google Scholar 

  13. Butler MA, King AA (2004) Phylogenetic comparative analysis: a modeling approach for adaptive evolution. Am Nat 164:683–695

    PubMed  Article  Google Scholar 

  14. Caro T (2005) The adaptive significance of coloration in mammals. BioScience 55:125–136

    Article  Google Scholar 

  15. Caro T (2008) Contrasting coloration in terrestrial mammals. Philos Trans R Soc B: Biol Sci 364:537–548

    Article  Google Scholar 

  16. Caro T, Beeman K, Stankowich T, Whitehead H (2011) The functional significance of colouration in cetaceans. Evol Ecol 25(6):1231

    Article  Google Scholar 

  17. Caro T, Mallarino R (2020) Coloration in mammals. Trends Ecol Evol 35(4):357–366

    PubMed  Article  Google Scholar 

  18. Caro T, Stankowich T, Mesnick SL, Costa DP, Beeman K (2012) Pelage coloration in pinnipeds: functional considerations. Behav Ecol 23(4):765–774

    Article  Google Scholar 

  19. Caro T, Walker H, Rossman Z, Hendrix M, Stankowich T (2017a) Why is the giant panda black and white? Behav Ecol 28(3):657–667

    Article  Google Scholar 

  20. Caro T, Walker H, Santana SE, Stankowich T (2017b) The evolution of anterior coloration in carnivorans. Behav Ecol Sociobiol 71(12):177

    Article  Google Scholar 

  21. Clavel J, Escarguel G, Merceron G (2015) mvMORPH: an R package for fitting multivariate evolutionary models to morphometric data. Methods Ecol Evol 6:1311–1319

    Article  Google Scholar 

  22. Clough D, Heistermann M, Kappeler PM (2009) Individual facial coloration in male Eulemur fulvus rufus: a condition-dependent ornament? Int J Primatol 30(6):859–875

    PubMed  PubMed Central  Article  Google Scholar 

  23. Cooper N, Thomas GH, Venditti C, Meade A, Freckleton RP (2016) A cautionary note on the use of Ornstein Uhlenbeck models in macroevolutionary studies. Biol J Linnean Soc 118:64–77

    Article  Google Scholar 

  24. Cramer JD, Gaetano T, Gray JP, Grobler P, Lorenz JG, Freimer NB, Schmitt CA, Turner TR (2013) Variation in scrotal color among widely distributed vervet monkey populations (Chlorocebus aethiops pygerythrus and Chlorocebus aethiops sabaeus). Am J Primatol 75(7):752–762

    PubMed  Article  Google Scholar 

  25. Crouch NM, Ricklefs RE (2019) Speciation rate is independent of the rate of evolution of morphological size, shape, and absolute morphological specialization in a large clade of birds. Am Nat 193:E78-E91

    PubMed  Article  Google Scholar 

  26. Cuthill IC, Allen WL, Arbuckle K, Caspers B, Chaplin G, Hauber ME, Hill GE, Jablonski NG, Jiggins CD, Kelber A, Mappes J (2017) The biology of color. Science 357:eaan0221

    PubMed  Article  CAS  Google Scholar 

  27. Darwin C (1859) On the Origin of Species by Means of Natural Selection, or, the Preservation of Favoured Races in the Struggle for Life. John Murray, London

    Google Scholar 

  28. delBarco-Trillo J, Burkert BA, Goodwin TE, Drea CM (2011) Night and day: the comparative study of strepsirrhine primates reveals socioecological and phylogenetic patterns in olfactory signals. J Evol Biol 24:82–98

    CAS  PubMed  Article  Google Scholar 

  29. Dubuc C, Allen WL, Maestripieri D, Higham JP (2014) Is male rhesus macaque red color ornamentation attractive to females? Behav Ecol Sociobiol 68(7):1215–1224

    PubMed  PubMed Central  Article  Google Scholar 

  30. Dunn PO, Armenta JK, Whittingham LA (2015) Natural and sexual selection act on different axes of variation in avian plumage color. Sci Adv 1(2):e1400155

    PubMed  PubMed Central  Article  Google Scholar 

  31. Endler JA (1980) Natural selection on color patterns in Poecilia reticulata. Evolution 34(1):76–91

    PubMed  Article  Google Scholar 

  32. Fernandez AA, Morris MR (2007) Sexual selection and trichromatic color vision in primates: statistical support for the preexisting-bias hypothesis. Am Nat 170(1):10–20

    PubMed  Article  Google Scholar 

  33. Fleagle JG (2013) Primate Adaptation and Evolution. 3rd Ed. Academic Press, Cambridge

    Google Scholar 

  34. Fleagle JG, Gilbert CC, Baden AL (2010) Primate cranial diversity. Am J Phys Anthropol 142:565–578

    PubMed  Article  Google Scholar 

  35. Friedman NR, Remeš V (2015) Rapid evolution of elaborate male coloration is driven by visual system in Australian fairy-wrens (Maluridae). J Evol Biol 28(12):2125–2135

    CAS  PubMed  Article  Google Scholar 

  36. Gloger CL (1833) Das Abandern der Vogel durch Einfluss des Klimas. August Schulz, Breslau

    Google Scholar 

  37. Haitina T, Ringholm A, Kelly J, Mundy NI, Schiöth HB (2007) High diversity in functional properties of melanocortin 1 receptor (MC1R) in divergent primate species is more strongly associated with phylogeny than coat color. Mol Biol Evol 24:2001–2008

    CAS  PubMed  Article  Google Scholar 

  38. Hall MI, Kamilar JM, Kirk EC (2012) Eye shape and the nocturnal bottleneck of mammals. Proc R Soc B 279:4962–4968

    PubMed  Article  Google Scholar 

  39. Harmon LJ, Losos JB, Jonathan Davies T, Gillespie RG, Gittleman JL, Bryan Jennings W, Kozak KH, McPeek MA, Moreno-Roark F, Near TJ, Purvis A, Ricklefs RE, Schluter D, Schulte II JA, Seehausen O, Sidlauskas BL, Torres-Carvajal O, Weir JT, Mooers AØ (2010) Early bursts of body size and shape evolution are rare in comparative data. Evolution 64:2385–2396

    PubMed  Google Scholar 

  40. Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W (2008) GEIGER: investigating evolutionary radiations. Bioinformatics 24:129–131

    CAS  PubMed  Article  Google Scholar 

  41. Henzi SP (1985) Genital signalling and the coexistence of male vervet monkeys (Cercopithecus aethiops pygerythrus) Folia Primatol 45(3–4):129–147

    CAS  Article  Google Scholar 

  42. Hill GE, McGraw KJ (2006) Bird Coloration, Volume 1: Mechanisms and Measurements. Harvard University Press, Cambridge

    Google Scholar 

  43. Hoekstra HE (2006) Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity 97:222–234

    CAS  PubMed  Article  Google Scholar 

  44. Hoekstra HE, Drumm KE, Nachman MW (2004) Ecological genetics of adaptive color polymorphism in pocket mice: geographic variation in selected and neutral genes. Evolution 58(6):1329–1341

    CAS  PubMed  Article  Google Scholar 

  45. Hoekstra HE, Nachman MW (2003) Different genes underlie adaptive melanism in different populations of rock pocket mice. Mol Ecol 12(5):1185–1194

    CAS  PubMed  Article  Google Scholar 

  46. Hofreiter M, Schöneberg T (2010) The genetic and evolutionary basis of colour variation in vertebrates. Cell Mol Life Sci 67:2591–2603

    CAS  PubMed  Article  Google Scholar 

  47. Jacobs GH (1993) The distribution and nature of colour vision among the mammals. Biol Rev Biol Proc Camb Philos Soc 68(3):413-471

  48. Jacobs RL, MacFie TS, Spriggs AN, Baden AL, Morelli TL, Irwin MT, Lawler RR, Pastorini J, Mayor M, Lei R, Culligan R, Hawkins MTR, Kappeler PM, Wright PC, Louis Jr EE, Mundy NI, Bradley BJ (2017) Novel opsin gene variation in large-bodied, diurnal lemurs. Biol Lett 13:20170050

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  49. Jacobs RL, Veilleux CC, Louis EE, Herrera JP, Hiramatsu C, Frankel DC, Irwin MT, Melin AD, Bradley BJ (2019) Less is more: lemurs (Eulemur spp.) may benefit from loss of trichromatic vision. Behav Ecol Sociobiol 73(2):22

    Article  Google Scholar 

  50. Jones MR, Mills LS, Alves PC, Callahan CM, Alves JM, Lafferty DJ, Jiggins FM, Jensen JD, Melo-Ferreira J, Good JM (2018) Adaptive introgression underlies polymorphic seasonal camouflage in snowshoe hares. Science 360(6395):1355–1358

    CAS  PubMed  Article  Google Scholar 

  51. Kamilar JM (2009) Interspecific variation in primate countershading: effects of activity pattern, body mass, and phylogeny. Int J Primatol 30(6):877

    Article  Google Scholar 

  52. Kamilar JM, Bradley BJ (2011a) Countershading is related to positional behavior in primates. J Zool 283:227–233

    Article  Google Scholar 

  53. Kamilar JM, Bradley BJ (2011b) Interspecific variation in primate coat colour supports Gloger’s rule. J Biogeogr 38:2270–2277

    Article  Google Scholar 

  54. Kamilar JM, Cooper N (2013) Phylogenetic signal in primate behaviour, ecology and life history. Philos Trans R Soc B: Biol Sci 368:20120341

    Article  Google Scholar 

  55. Kamilar JM, Heesy CP, Bradley BJ (2013) Did trichromatic color vision and red hair color coevolve in primates? Am J Primatol 75:740–751

    PubMed  Article  Google Scholar 

  56. Kamilar JM, Muldoon KM (2010) The climatic niche diversity of Malagasy primates: a phylogenetic perspective. PLoS One 5(6):e11073

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  57. Kappeler PM (2012) The behavioral ecology of strepsirrhines and tarsiers. In: Mitani JC, Call P, Kappeler PM, Palombit RA, Silk JB (eds) The Evolution of Primate Societies. University of Chicago Press, Chicago, pp 17–42

    Google Scholar 

  58. Kawamura S (2016) Color vision diversity and significance in primates inferred from genetic and field studies. GENES GENOM 38:779–791

    Article  Google Scholar 

  59. Kawamura S, Kubotera N (2004) Ancestral loss of short wave-sensitive cone visual pigment in lorisiform prosimians, contrasting with its strict conservation in other prosimians. J Mol Evol 58(3):314–321

    CAS  PubMed  Article  Google Scholar 

  60. Luzuriaga-Aveiga VE, Weir JT (2019) Elevational differentiation accelerates trait evolution but not speciation rates in Amazonian birds. Ecol Lett 22(4):624–633

    PubMed  Article  Google Scholar 

  61. Maddison WP, Maddison DR (2017) Mesquite: a modular system for evolutionary analysis. Version 3.31. URL: http://www.mesquiteproject.org

  62. Maia R, Rubenstein DR, Shawkey MD (2013) Key ornamental innovations facilitate diversification in an avian radiation. Prc Natl Acad Sci USA 110(26):10687–10692

    CAS  Article  Google Scholar 

  63. Manceau M, Domingues VS, Linnen CR, Rosenblum EB, Hoekstra HE (2010) Convergence in pigmentation at multiple levels: mutations, genes and function. Philos Trans R Soc B: Biol Sci 365:2439–2450

    CAS  Article  Google Scholar 

  64. Marcondes RS, Brumfield RT (2019) Fifty shades of brown: macroevolution of plumage brightness in the furnariida, a large clade of drab neotropical passerines. Evolution 73:704–719

    PubMed  Article  Google Scholar 

  65. Martin PR, Montgomerie R, Lougheed SC (2015) Color patterns of closely related bird species are more divergent at intermediate levels of breeding-range sympatry. Am Nat 185:443–451

    PubMed  Article  Google Scholar 

  66. McGarigal K, Stafford S, Cushman S (2000) Multivariate Statistics for Wildlife and Ecology Research. Springer, New York

    Book  Google Scholar 

  67. McNaught MK, Owens IPF (2002) Interspecific variation in plumage coloration among birds: species recognition or light environment? J Evol Biol 15:505–514

    Article  Google Scholar 

  68. Mundy NI, Kelly J (2003) Evolution of a pigmentation gene, the melanocortin-1 receptor, in primates. Am J Phys Anthropol 121(1):67–80

    CAS  PubMed  Article  Google Scholar 

  69. Münkemüller T, Lavergne S, Bzeznik B, Dray S, Jombart T, Schiffers K, Thuiller W (2012) How to measure and test phylogenetic signal. Methods Ecol Evol 3:743–756

    Article  Google Scholar 

  70. Nilsson Sköld H, Aspengren S, Wallin M (2013) Rapid color change in fish and amphibians–function, regulation, and emerging applications. Pigment Cell Melanoma Res 26(1):29–38

    PubMed  Article  Google Scholar 

  71. O’Meara BC, Ané C, Sanderson MJ, Wainwright PC (2006) Testing for different rates of continuous trait evolution using likelihood. Evolution 60:922–933

    PubMed  Article  Google Scholar 

  72. Ortolani A (1999) Spots, stripes, tail tips and dark eyes: predicting the function of carnivore colour patterns using the comparative method. Biol J Linnean Soc 67:433–476

    Article  Google Scholar 

  73. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  74. Paradis E, Schliep K (2019) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35(3):526–528

    CAS  PubMed  Article  Google Scholar 

  75. Pennell MW, Eastman JM, Slater GJ, Brown JW, Uyeda JC, FitzJohn RG, Alfaro ME, Harmon LJ (2014) geiger v2. 0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees. Bioinformatics 30(15):2216–2218

    CAS  PubMed  Article  Google Scholar 

  76. Petersdorf M, Dubuc C, Georgiev AV, Winters S, Higham JP (2017) Is male rhesus macaque facial coloration under intrasexual selection? Behav Ecol 28(6):1472–1481

    PubMed  PubMed Central  Article  Google Scholar 

  77. Price TD (2017) Sensory drive, color, and color vision. Am Nat 190:157–170

    PubMed  Article  Google Scholar 

  78. R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/

  79. Rakotonirina H, Kappeler PM, Fichtel C (2017) Evolution of facial color pattern complexity in lemurs. Sci Rep 7:1–18

    CAS  Article  Google Scholar 

  80. Renoult JP, Schaefer HM, Sallé B, Charpentier MJ (2011) The evolution of the multicoloured face of mandrills: insights from the perceptual space of colour vision. PLoS One 6(12): e29117

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  81. Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223

    Article  Google Scholar 

  82. Ribot RF, Berg ML, Schubert E, Endler JA, Bennett AT (2019) Plumage coloration follows Gloger’s rule in a ring species. J Biogeogr 46(3):584–596

    Article  Google Scholar 

  83. Romero-Diaz C, Rivera JA, Ossip‐Drahos AG, Zúñiga‐Vega JJ, Vital‐García C, Hews DK, Martins EP (2019) Losing the trait without losing the signal: evolutionary shifts in communicative colour signalling. J Evol Biol 32(4):320–330

    PubMed  Article  Google Scholar 

  84. Rowe N, Myers M (2017) All the World’s Primates. Primate Conservation Inc.  http://alltheworldsprimates.org

  85. Rowan J, Beaudrot L, Franklin J, Reed KE, Smail IE, Zamora A, Kamilar JM (2020) Geographically divergent evolutionary and ecological legacies shape mammal biodiversity in the global tropics and subtropics. Proc Natl Acad Sci USA 117(3):1559–1565

    CAS  PubMed  Article  Google Scholar 

  86. Rowan J, Kamilar JM, Beaudrot L, Reed KE (2016) Strong influence of palaeoclimate on the structure of modern African mammal communities. Proc R Soc B 283(1840):20161207

    PubMed  Article  Google Scholar 

  87. Ryan MJ (1990) Sexual selection, sensory systems and sensory exploitation. Oxford Surv Evol Biol 7:157–195

    Google Scholar 

  88. Santana SE, Alfaro JL, Alfaro ME (2012) Adaptive evolution of facial colour patterns in Neotropical primates. Proc R Soc B 279:2204–2211

    PubMed  Article  Google Scholar 

  89. Santana SE, Alfaro JL, Noonan A, Alfaro ME (2013) Adaptive response to sociality and ecology drives the diversification of facial colour patterns in catarrhines. Nat Commun 4(1):1–7

    Article  CAS  Google Scholar 

  90. Schaefer HM, Schaefer V, Levey DJ (2004) How plant–animal interactions signal new insights in communication. Trends Ecol Evol 19:577–584

    Article  Google Scholar 

  91. Schliep KP (2011) phangorn: phylogenetic analysis in R. Bioinformatics 27:592–593

    CAS  PubMed  Article  Google Scholar 

  92. Seehausen O, Mayhew PJ, Van Alphen JJM (1999) Evolution of colour patterns in East African cichlid fish. J Evol Biol 12:514–534

    Article  Google Scholar 

  93. Setchell JM (2005) Do female mandrills prefer brightly colored males? Int J Primatol 26(4):715–735

    Article  Google Scholar 

  94. Setchell JM, Jean Wickings E, Knapp LA (2006) Signal content of red facial coloration in female mandrills (Mandrillus sphinx). Proc R Soc B 273(1599):2395–2400

    PubMed  Article  Google Scholar 

  95. Sheets AD, Chavez AS (2020) Evolution of pelage luminance in squirrels (Sciuridae). Front Ecol Evol 8:249

    Article  Google Scholar 

  96. Soul LC, Friedman M (2015) Taxonomy and phylogeny can yield comparable results in comparative paleontological analyses. Syst Biol 64:608–620

    CAS  PubMed  Article  Google Scholar 

  97. Stevens M, Parraga CA, Cuthill IC, Partridge JC, Troscianko TS (2007) Using digital photography to study animal coloration. Biol J Linnean Soc 90:211–237

    Article  Google Scholar 

  98. Stoddard MC, Prum RO (2008) Evolution of avian plumage color in a tetrahedral color space: a phylogenetic analysis of New World buntings. Am Nat 171:755–776

    PubMed  Article  Google Scholar 

  99. Stoddard MC, Prum RO (2011) How colorful are birds? Evolution of the avian plumage color gamut. Behav Ecol 22:1042–1052

    Article  Google Scholar 

  100. Stoner CJ, Caro TM, Graham CM (2003) Ecological and behavioral correlates of coloration in artiodactyls: systematic analyses of conventional hypotheses. Behav Ecol 14(6): 823–840

    Article  Google Scholar 

  101. Sumner P, Mollon JD (2003) Colors of primate pelage and skin: objective assessment of conspicuousness. Am J Primatol 59:67–91

    PubMed  Article  Google Scholar 

  102. Tan Y, Li WH (1999) Trichromatic vision in prosimians. Nature 402(6757):36

    CAS  PubMed  Article  Google Scholar 

  103. Tapanes E, Kamilar JM, Bradley BJ (In press) Molecular and cellular processes of pelage pigmentation and growth in primate evolution. In: Pitirri MK, Richtsmeier JT (eds) Evolutionary Cell Processes in Primates: Genes, Skin, Energetics, Breathing, and Feeding, Volume II. Taylor and Francis/CRC Press, New York

  104. 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 30:932–942

    Article  Google Scholar 

  105. 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(1):88–107

    Article  Google Scholar 

  106. Waitt C, Little AC, Wolfensohn S, Honess P, Brown AP, Buchanan-Smith HM, Perrett DI (2003) Evidence from rhesus macaques suggests that male coloration plays a role in female primate mate choice. Proc R Soc B 270(suppl_2):S144-S146

    Article  Google Scholar 

  107. Wallace AR (1870) Contributions to the Theory of Natural Selection: A Series of Essays. Macmillan and Company, London

    Google Scholar 

  108. Wang IJ, Shaffer HB (2008) Rapid color evolution in an aposematic species: a phylogenetic analysis of color variation in the strikingly polymorphic strawberry poison-dart frog. Evolution 62(11):2742–2759

    CAS  PubMed  Article  Google Scholar 

  109. West PM, Packer C (2002) Sexual selection, temperature, and the lion’s mane. Science 297:1339–1343

    CAS  PubMed  Article  Google Scholar 

  110. Wickham H (2009) ggplot2: Elegant Graphic for Data Analysis. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgements

We thank Eileen Westwig at the AMNH and the late Bill Stanley at the FMNH for access to the primate collections and logistical support. We thank Richard Lawler and two anonymous reviewers, whose constructive feedback greatly improved this manuscript.

Funding

Funding to collect museum data was provided to JMK by Washington University (St. Louis), the Field Museum of Natural History, and the Leakey Foundation. JMK’s and BJB’s research on primate hair evolution is also supported by the National Science Foundation (BCS #1546730, BCS #1606360), the Wenner-Gren Foundation, The George Washington University, the University of Massachusetts, Amherst, Yale University, and the Natural Environment Research Council, UK.

Author information

Affiliations

Authors

Contributions

RBB and JMK conceived and designed the analysis. JMK collected the raw hair color data. RBB performed the statistical analyses and drafted the manuscript. RBB, JMK, and BJB interpreted the results and edited the manuscript.

Corresponding author

Correspondence to Rachel B. Bell.

Ethics declarations

Conflicts of Interest

The authors declare no conflicts of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 45.8 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bell, R.B., Bradley, B.J. & Kamilar, J.M. The Evolutionary Ecology of Primate Hair Coloration: A Phylogenetic Approach. J Mammal Evol (2021). https://doi.org/10.1007/s10914-021-09547-8

Download citation

Keywords

  • Pelage
  • Pigmentation
  • Comparative methods
  • Mammal
  • Phenotypic divergence