Abstract
Some carnivorans have striking patches of fur on their faces (spots, bands, eye masks) and blazes on their chests that are primarily visible from a frontal view. We tested five hypotheses to explain the evolution of the complexity and contrast of these color patches. These were: signals of species identity to avoid hybridization, communication between conspecifics, signals used to warn of defensive anal secretions, signals of belligerence or pugnacity, and camouflage-related coloration used to break up the outline and facial features of the predator when approaching prey. Using phylogenetically controlled multifactorial analyses in six different families of carnivorans, examined separately, our analyses uncovered significant positive associations between measures of color pattern complexity and sociality across herpestid faces and canid chests, suggesting use in social communication. Mustelid facial color complexity was associated with ability to direct anal secretions accurately at predators, and facial markings were significantly or marginally associated with pugnacity in mustelids, viverrids, and herpestids. Facial complexity of viverrid and herpestid species was significantly or marginally related to a mammal-based diet. In ursids, facial contrast appeared less variable in species living in greater sympatry with other bears. Facial and chest coloration in Carnivora appears to have evolved under different selection pressures in different families.
Significance statement
The reasons that many carnivorans have colorful and memorable faces and chests are not yet understood. Here, we pit five different hypotheses against each other: species recognition, advertising either toxic anal defenses or pugnacity, recognizing group members, and trying to remain concealed when approaching mammalian prey. We find that measures of facial and chest complexity and contrast have evolved for different reasons depending on the carnivoran family. Anterior coloration appears to be involved with social communication in herpestids and canids; facial coloration is associated noxious secretions in mustelids, with pugnacity in mustelids, viverrids and herpestids; with reliance on a mammal-based diet in viverrids and herpestids; and with avoiding hybridization in bear species. There is no overriding evolutionary explanation for varied facial and chest pelage coloration across carnivorans.
This is a preview of subscription content, access via your institution.



References
Allen WL, Cuthill IC, Scott-Samuel N, Baddeley R (2010) Why the leopard got its spots: relating pattern development to ecology in felids. Proc R Soc B (2011) 278:1373–1380. https://doi.org/10.1098/rspb.2010.1734
Allen WL, Stevens M, Higham JP (2014) Character displacement of Cercopithecini primate visual signals. Nat Commun 5:4266
Arnold C, Matthews LJ, Nunn CL (2010) The 10kTrees website: a new online resource for primate phylogeny. Evol Anthropol 19:114–118
Caro T (2009) Contrasting colouration in terrestrial mammals. Philos T Roy Soc B 364:537–548
Caro T (2013) The colours of extant mammals. Sem cell Devel Biol 24:542–552
Caro T, Allen WL (2017) Interspecific visual signalling in animals and plants: a functional classification. Philos T Roy Soc B 372:20160344
Caro T, Walker H, Rossman Z, Hendrix M, Stankowich T (2017) Why is the giant panda black and white? Behav Ecol 28:657–667
Cott HB (1940) Adaptive coloration in animals. Methuen & Co. Ltd, London
Davis AK, Woodall N, Moskowitz JP, Castleberry N, Freeman BJ (2013) Temporal change in fur color in museum specimens of mammals: reddish-brown species get redder with storage time. Int J Zool 2013:876347
Francis CM (2008) A guide to the mammals of Southeast Asia. Princeton University Press, Princeton
Gorman ML, Trowbridge BJ (1989) The role of odor in the social lives of carnivores. In: Gittleman JL (ed) Carnivore behavior, ecology, and evolution. Chapman & Hall, London, pp 57–88
Hill GE (2015) Sexiness, individual condition, and species identity: the information signaled by ornaments and assessed by choosing females. Evol Biol 42:251–259
Hunter L (2011) Carnivores of the world. Princeton University Press, Princeton, NJ
Kelly BP, Whiteley A, Tallmon D (2010) The Arctic melting pot. Nature 468:891–891
Kingdon J (1977) East African mammals. 3, part a (carnivores). Academic Press, London
Lehman N, Eisenhawer A, Hansen K, Mech LD, Peterson RO, Gogan PJ, Wayne RK (1991) Introgression of coyote mitochondrial DNA into sympatric North American gray wolf populations. Evolution 45:104–119
Myers P, Espinosa R, Parr CS, Jones T, Hammond GS, Dewey TA (2013) The Animal Diversity Web (online), www.animaldiversity.org
Newman C, Buesching CD, Wolff JO (2005) The function of facial masks in “midguild” carnivores. Oikos 108:623–633
Nowak RM (1999) Walker’s mammals of the world, 6th edn. Johns Hopkins University Press, Baltimore
Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N, Pearse W (2012) Caper: comparative analysis of phylogenetics and evolution in R. R package version 0.5, http://CRAN.R-project.org/package=caper
Ortolani A (1999) Spots, stripes, tail tips and dark eyes: predicting the function of carnivore colour patterns using the comparative method. Biol J Linn Soc 67:433–476
Ortolani A, Caro T (1996) The adaptive significance of color patterns in carnivores: phylogenetic tests of classic hypotheses. In: Gittleman JL (ed) Carnivore behavior, ecology and evolution, vol II. Cornell University press, Ithaca, New York, pp 132–188
Osorio D, Vorobyev M (1996) Colour vision as an adaptation to frugivory in primates. Proc R Soc Lond B 263:593–599
R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-project.org
Santana SE, Alfaro JL, Alfaro ME (2012) Adaptive evolution of facial colour patterns in Neotropical primates. Proc R Soc Lond B 279:2204–2211
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 4:2765
Stankowich T, Caro T, Cox M (2011) Bold coloration and the evolution of aposematism in terrestrial carnivores. Evolution 65:3090–3099
Stankowich T, Havercamp P, Caro T (2014) Ecological drivers of antipredator defenses in carnivores. Evolution 68:1415–1425
Stoner CJ, Caro TM, Graham CM (2003) Ecological and behavioral correlates of coloration in artiodactyls: systematic analyses of conventional hypotheses. Behav Ecol 14:823–840
Tibbetts EA, Mullen SP, Dale J (2017) Signal function drives phenotypic and genetic diversity: the effects of signaling individual identity, quality or behavioural strategy. Philos T Roy Soc B 372:20160347
Van Dyck S (2006) In: Strahan R (ed) The mammals of Australia. New Holland Publishing, Sydney
Wilson DE, Mittermeier RA (2009) Handbook of the mammals of the world, vol 1. Carnivores. Lynx Edicions, Barcelona
Wilson DE, Reeder DM (eds) (2005) Mammal species of the world: a taxonomic and geographic reference. John Hopkins University Press, Baltimore
Acknowledgments
We thank anonymous reviewers for their comments.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical statement
All sources of data were from the literature or the web and did not involve ethical approval. There was no funding for this project.
Conflict of interest
The authors declare that they have no conflict of interest.
Data availability
All data generated or analyzed during this study are included in the supplementary information files.
Additional information
Communicated by M. Festa-Bianchet
Rights and permissions
About this article
Cite this article
Caro, T., Walker, H., Santana, S.E. et al. The evolution of anterior coloration in carnivorans. Behav Ecol Sociobiol 71, 177 (2017). https://doi.org/10.1007/s00265-017-2402-5
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-017-2402-5
Keywords
- Carnivores
- Chests
- Color complexity
- Contrast
- Faces