Adaptive evolution of facial colour patterns in Neotropical primates

Abstract

The rich diversity of primate faces has interested naturalists for over a century. Researchers have long proposed that social behaviours have shaped the evolution of primate facial diversity. However, the primate face constitutes a unique structure where the diverse and potentially competing functions of communication, ecology and physiology intersect, and the major determinants of facial diversity remain poorly understood. Here, we provide the first evidence for an adaptive role of facial colour patterns and pigmentation within Neotropical primates. Consistent with the hypothesis that facial patterns function in communication and species recognition, we find that species living in smaller groups and in sympatry with a higher number of congener species have evolved more complex patterns of facial colour. The evolution of facial pigmentation and hair length is linked to ecological factors, and ecogeographical rules related to UV radiation and thermoregulation are met by some facial regions. Our results demonstrate the interaction of behavioural and ecological factors in shaping one of the most outstanding facial diversities of any mammalian lineage.

Color in competition contexts in non-human animals

“…I concentrate on phenotypically plastic skin colour, and within species and within-individual differences, but note that also primates show wonderful coloured pelage (Bradley & Mundy, 2008;Gerald, 2003), including outstanding facial diversity which may function in species recognition (Santana, Lynch Alfaro, & Alfaro, 2012). I end with conclusions and future directions for the study of the influence of colour on the behaviour of non-human animals in contests for mates and resources.…”

Adaptive response to sociality and ecology drives the diversification of facial colour patterns in catarrhines

“…Although explicit tests for a link between ecology and facial diversity in catarrhines are lacking, ecological factors significantly predict levels of facial diversity in Neotropical primates (Platyrrhini), which form the sister group to catarrhines. In platyrrhines, darker faces evolved in species living in regions occupied by forests, such as the Amazon 8 . Social factors also explain some aspects of platyrrhine facial diversity, with complex colour patterns tending to evolve in species that live in small social groups and in high levels of congeneric sympatry 8 .…”

Plain faces are more expressive: comparative study of facial colour, mobility and musculature in primates

“…Supporting our hypothesis, plainly coloured faces evolved in tandem with enhanced ability for facial expressions. It is thus possible that there is a trade-off in the evolution of these two types of facial cues; while complex facial colour patterns may be beneficial for advertising identity [4,5], a highly 'cluttered' face may mask the visibility of facial expressions used to convey behavioural intention. At a neural level, although there is some degree of separation between the mechanisms for recognition of identity and expression, these complex tasks involve the concerted action of potentially overlapping functional components [20], which could explain part of this result.…”

“…For each species, we quantified facial colour patterns as facial colour pattern complexity (FCPC; the total number of uniquely coloured facial areas [5]; electronic supplementary material), using high-resolution, close-up photographs of male faces. Higher FCPC represents a more complexly patterned face.…”

“…Facial coloration patterns evolved in tandem with sociality and sympatry in primates [4,5]. In most primate radiations, highly social and sympatric species evolved multi-coloured faces, while less social species tend to have less colourful faces [4].…”