Sexual selection and trichromatic color vision in primates: statistical support for the preexisting-bias hypothesis

The evolution of trichromatic color vision in primates may improve foraging performance as well as intraspecific communication; however, the context in which color vision initially evolved is unknown. We statistically examined the hypothesis that trichromatic color vision in primates represents a preexisting bias for the evolution of red coloration (pelage and/or skin) through sexual selection. Our analyses show that trichromatic color vision evolved before red pelage and red skin, as well as before gregarious mating systems that would promote sexual selection for visual traits and other forms of intraspecific communication via red traits. We also determined that both red pelage and red skin were more likely to evolve in the presence of color vision and mating systems that promote sexual selection. These results provide statistical support for the hypothesis that trichromatic color vision in primates evolved in a context other than intraspecific communication with red traits, most likely foraging performance, but, once evolved, represented a preexisting bias that promoted the evolution of red traits through sexual selection.     

Is Brightest Best? Testing the Hamilton-Zuk Hypothesis in Mandrills

Although many primates exhibit striking coloration, including brightly colored pelage and bare areas of skin, our understanding of the function and evolution of these traits pales in the face of knowledge about color in other taxa. However, recent years have seen an increase in the number of studies of individual variation in primate color and evidence is accumulating that these traits can act as important signals to conspecifics. Mandrills are arguably the most colorful of all primates. Here, we review what we have discovered about the signal function of coloration in male and female mandrills from our long-term studies of a semi-free-ranging colony in Franceville, Gabon and test the predictions of the Hamilton-Zuk hypothesis—that bright coloration is condition dependent, and that only individuals of superior quality will be able to express color fully—in this species. We compare measures of facial coloration in both sexes with parasite load (using fecal analysis over 1 annual cycle), immune status (hematological parameters), neutral genetic diversity (microsatellite heterozygosity), and major histocompatability (MHC) genotype to examine whether red coloration acts as an honest signal of individual quality in mandrills. We found that red coloration was unrelated to parasitism and hematological parameters. Red was also unrelated to genome-wide heterozygosity and MHC diversity, although specific MHC genotypes were significantly related to red. The healthy, provisioned nature of the colony and problems associated with observational, correlational studies restrict interpretation of our data, and it would be premature to draw conclusions as to whether color signals individual quality in mandrills. We conclude with some suggestions for future studies on the signal content of color in mandrills and other primates.     

Comparing the accuracy and precision of three techniques used for estimating missing landmarks when reconstructing fossil hominin crania

In some primate species, pelage colorations at birth contrast with adult colorations. The intensity of natal coats and their phylogenetic distribution is highly variable within primates. Natal coat coloration seems to change to adult coloration in most species when infants become independent from their mothers, but an accepted functional explanation for natal coats is not available. Here we describe pelage coloration change in sexually dichromatic redfronted lemurs (Eulemur fulvus rufus) in Kirindy Forest, and propose a new functional hypothesis for this phenomenon. In this species, infants are born with adult male coloration and female infants subsequently undergo a change in coloration. Using digital pictures and behavioral data collected on eight mother-offspring dyads from birth until the end of the coloration change, we 1) described timing and pattern of pelage developmentin redfronted lemur infants and 2) examined behavioral developmental correlates of the coloration change. The color change took place between 7 and 17 weeks of age and coincided with advanced physical independence; a pattern also found in monochromatic primate species with natal coats. No behavioral differences between male and female infants were found. Hypotheses about the ultimate function of natal coats focusing on enhanced infant care or reduced infanticide risk did not explain the pelage change in redfronted lemurs. The natal pelage pattern in this species may instead serve as sexual mimicry. Accordingly, female infants may mimic males during the most vulnerable developmental phase to avoid sex-specific aggression by adult females in a species with intense female-female aggression and competition.     

Leaf‐footed bugs possess multiple hidden contrasting color signals,but only one is associated with increased body size

Antipredatory displays that incorporate hidden contrasting coloration are found in a variety of different animals. These displays are seen in organisms that have drab coloration at rest, but when disturbed reveal conspicuous coloration. Examples include the bright abdomens of mountain katydids and the colorful underwings of hawk moths. Such hidden displays can function as secondary defenses, enabling evasion of a pursuant predator. To begin to understand why some species have these displays while others do not, we conducted phylogenetic comparative analyses to investigate factors associated with the evolution of hidden contrasting coloration in leaf‐footed bugs. First, we investigated whether hidden contrasting coloration was associated with body size because these displays are considered to be more effective in larger organisms. We then investigated whether hidden contrasting coloration was associated with an alternative antipredatory defense, in this case rapid autotomy. We found that leaf‐footed bugs with hidden contrasting coloration tended to autotomize more slowly, but this result was not statistically significant. We also found that the presence of a body size association was dependent upon the form of the hidden color display. Leaf‐footed bugs that reveal red/orange coloration were the same size, on average, as species without a hidden color display. However, species that reveal white patches on a black background were significantly larger than species without a hidden color display. These results highlight the diversity of forms that hidden contrasting color signal can take, upon which selection may act differently.     

Primate natal coats: A preliminary analysis of distribution and function

Pelage coloration of infants was compiled for 138 species of primates. Three functional hypotheses—alloparental, infant defense, and paternity cloak—for primate natal coats are tested. Neonatal pelage contrasted with adult pelage in over half of the species examined. Subtle or inconspicuous contrast was more common than flamboyant contrast. Natal coats began to change at 5.7 weeks and disappeared by 18.0 weeks postpartum on average. The first body part to lose natal coloration was the head and/or dorsum in the majority of species. Functional analyses provided no support for the only published hypothesis—alloparental—while providing partial support for two new hypotheses—infant defense and paternity cloak. A significant association between testes weight and natal coat contrast supports a link between mating system and infant contrast. This is discussed in terms of infanticide avoidance. Natal coats are proposed to be categorically differentiated into inconspicuous and flamboyant types, not differentiated by a continuous gradation, such as color. Subspecific differentiation and patterns of shared ancestry are assessed. Am J Phys Anthropol 104:47–70, 1997. © 1997 Wiley-Liss, Inc.     

Historical contingency in the evolution of primate color vision

Primates are unique among eutherian mammals for possessing three types of retinal cone. Curiously, catarrhines, platyrrhines, and strepsirhines share this anatomy to different extents, and no hypothesis has hitherto accounted for this variability. Here we propose that the historical biogeography of figs and arborescent palms accounts for the global variation in primate color vision. Specifically, we suggest that primates invaded Paleogene forests characterized by figs and palms, the fruits of which played a keystone function. Primates not only relied on such resources, but also provided high-quality seed dispersal. In turn, figs and palms lost or simply did not evolve conspicuous coloration, as this conferred little advantage for attracting mammals. We suggest that the abundance and coloration of figs and palms offered a selective advantage to foraging groups with mixed capabilities for chromatic distinction. Climatic cooling at the end of the Eocene and into the Neogene resulted in widespread regional extinction or decimation of palms and (probably) figs. In regions where figs and palms became scarce, we suggest primates evolved routine trichromatic vision in order to exploit proteinaceous young leaves as a replacement resource. A survey of the hue and biogeography of extant figs and palms provides some empirical support. Where these resources are infrequent, primates are routinely trichromatic and consume young leaves during seasonal periods of fruit dearth. These results imply a link between the differential evolution of primate color vision and climatic changes during the Eocene-Oligocene transition.     

Adaptation of Pelage Color and Pigment Variations in Israeli Subterranean Blind Mole Rats,Spalax Ehrenbergi

Background

Concealing coloration in rodents is well established. However, only a few studies examined how soil color, pelage color, hair-melanin content, and genetics (i.e., the causal chain) synergize to configure it. This study investigates the causal chain of dorsal coloration in Israeli subterranean blind mole rats, Spalax ehrenbergi.

Methods

We examined pelage coloration of 128 adult animals from 11 populations belonging to four species of Spalax ehrenbergi superspecies (Spalax galili, Spalax golani, Spalax carmeli, and Spalax judaei) and the corresponding coloration of soil samples from the collection sites using a digital colorimeter. Additionally, we quantified hair-melanin contents of 67 animals using HPLC and sequenced the MC1R gene in 68 individuals from all four mole rat species.

Results

Due to high variability of soil colors, the correlation between soil and pelage color coordinates was weak and significant only between soil hue and pelage lightness. Multiple stepwise forward regression revealed that soil lightness was significantly associated with all pelage color variables. Pelage color lightness among the four species increased with the higher southward aridity in accordance to Gloger''s rule (darker in humid habitats and lighter in arid habitats). Darker and lighter pelage colors are associated with darker basalt and terra rossa, and lighter rendzina soils, respectively. Despite soil lightness varying significantly, pelage lightness and eumelanin converged among populations living in similar soil types. Partial sequencing of the MC1R gene identified three allelic variants, two of which were predominant in northern species (S. galili and S. golani), and the third was exclusive to southern species (S. carmeli and S. judaei), which might have caused the differences found in pheomelanin/eumelanin ratio.

Conclusion/Significance

Darker dorsal pelage in darker basalt and terra rossa soils in the north and lighter pelage in rendzina and loess soils in the south reflect the combined results of crypsis and thermoregulatory function following Gloger''s rule.     

Perceptual considerations in the use of colored photographic and video stimuli to study nonhuman primate behavior

The use of photographs, slides, computerized images, and video to study behavior is increasingly being employed in nonhuman primates. However, since these mediums have been designed to simulate natural coloration for normal trichromatic human vision, they can fail to reproduce color in meaningful and accurate ways for viewers with different visual systems. Given the range of color perception that exists both across and within different species, it is necessary to consider this variation in order to discern the suitability of these mediums for experimental use. Because of the high degree of visual similarity among humans, Old World monkeys, and apes, the use of photographic and video stimuli should be acceptable in terms of replicating naturalistic coloration and making noticeable color manipulations. However, among New World primates and prosimians, there exists a considerable degree of variation in color perceptual abilities depending on the species, sex, and allelic combination of the animals involved. Therefore, the use of these mediums to study behavior is problematic for these species, and should be done with caution.     

The primate palette: The evolution of primate coloration

Flip through The Pictorial Guide to the Living Primates¹ and you will notice a striking yet generally underappreciated aspect of primate biology: primates are extremely colorful. Primate skin and pelage coloration were highlighted examples in Darwin's² original discussions of sexual selection but, surprisingly, the topic has received little research attention since. Here we summarize the patterns of color variation observed across the primate order and examine the selective forces that might drive and maintain this aspect of primate phenotypic diversity. We discuss how primate color patterns might be adaptive for physiological function, crypsis, and communication. We also briefly summarize what is known about the genetic basis of primate pigmentation and argue that understanding the proximate mechanisms of primate coloration will be essential, not only for understanding the evolutionary forces shaping phenotypic variation, but also for clarifying primate taxonomies and conservation priorities.     

The adaptive significance of coloration in lagomorphs

Lagomorph pelage coloration was matched to habitat type, geographical region, altitude and behaviour to explore the adaptive significance of coloration patterns in this little-studied order of mammals. Analyses were conducted with and without taking phylogeny into account. The former analyses were based on a weighted, phylogenetic supertree for all extant species of lagomorphs that we constructed using morphological and molecular data from 146 papers in the literature. Although our analyses represent an initial, somewhat crude investigation, several clear trends are evident. First, overall body coloration across lagomorphs tends to match the background as shown for pale and red coloration and perhaps seasonal pelage change. The case for countershading being a method of concealment is far less strong. Second, ear tips appear to have a communicative role since they are conspicuous in many different habitats. Third, hypotheses for tail tips having a communicative role, for extremities being dark for physiological reasons, and for Gloger's rule received only partial support.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79, 309–328.     

Conspicuous male coloration impairs survival against avian predators in Aegean wall lizards,Podarcis erhardii

Animal coloration is strikingly diverse in nature. Within‐species color variation can arise through local adaptation for camouflage, sexual dimorphism and conspicuous sexual signals, which often have conflicting effects on survival. Here, we tested whether color variation between two island populations of Aegean wall lizards (Podarcis erhardii) is due to sexual dimorphism and differential survival of individuals varying in appearance. On both islands, we measured attack rates by wild avian predators on clay models matching the coloration of real male and female P. erhardii from each island population, modeled to avian predator vision. Avian predator attack rates differed among model treatments, although only on one island. Male‐colored models, which were more conspicuous against their experimental backgrounds to avian predators, were accordingly detected and attacked more frequently by birds than less conspicuous female‐colored models. This suggests that female coloration has evolved primarily under selection for camouflage, whereas sexually competing males exhibit costly conspicuous coloration. Unexpectedly, there was no difference in avian attack frequency between local and non‐local model types. This may have arisen if the models did not resemble lizard coloration with sufficient precision, or if real lizards behaviorally choose backgrounds that improve camouflage. Overall, these results show that sexually dimorphic coloration can affect the risk of predator attacks, indicating that color variation within a species can be caused by interactions between natural and sexual selection. However, more work is needed to determine how these findings depend on the island environment that each population inhabits.     

Hormonal regulation of female nuptial coloration in a fish

Physiological color change in camouflage and mating is widespread among fishes, but little is known about the regulation of such temporal changes in nuptial coloration and particularly concerning female coloration. To better understand regulation of nuptial coloration we investigated physiological color change in female two-spotted gobies (Gobiusculus flavescens). Females of this species develop an orange belly that acts as an ornament. The orange color is caused by the color of the gonads combined with the chromathophore based pigmentation and transparency of the skin. Often during courtship and female–female competition, a rapid increase in orange coloration, in combination with lighter sides and back that increases skin and body transparency, gives the belly an intense ‘glowing’ appearance. To understand how this increased orange coloration can be regulated we analysed chromatic and transparency effects of neurohumoral agents on abdominal skin biopsies in vitro. We found prolactin and α-melanocyte stimulating hormone (MSH) to increase orange coloration of the skin. By contrast, melatonin and noradrenaline increased skin transparency, but had a negative effect on orange coloration. However, mixtures of melatonin and MSH, or melatonin and prolactin, increased both orange coloration and transparency. This effect mimics the chromatic ‘glow’ effect that commonly takes place during courtship and intra sexual aggression. Notably, not only epidermal chromatophores but also internal chromatophores lining the peritoneum responded to hormone treatments. There were no chromatic effects of the sex steroids 17β-estradiol, testosterone or 11-ketotestosterone. We hypothesize that similar modulation of nuptial coloration by multiple hormones may be widespread in nature.     

Roosting ecology and the evolution of pelage markings in bats

Multiple lineages of bats have evolved striking facial and body pelage makings, including spots, stripes and countershading. Although researchers have hypothesized that these markings mainly evolved for crypsis, this idea has never been tested in a quantitative and comparative context. We present the first comparative study integrating data on roosting ecology (roost type and colony size) and pelage coloration patterns across bats, and explore the hypothesis that the evolution of bat pelage markings is associated with roosting ecologies that benefit from crypsis. We find that lineages that roost in the vegetation have evolved pelage markings, especially stripes and neck collars, which may function in crypsis through disruptive coloration and a type of countershading that might be unique to bats. We also demonstrate that lineages that live in larger colonies and are larger in size tend not to have pelage markings, possibly because of reduced predation pressures due to the predator dilution effect and a lower number of potential predators. Although social functions for pelage color patterns are also possible, our work provides strong support for the idea that roosting ecology has driven the evolution of pelage markings in bats.     

Bold coloration and the evolution of aposematism in terrestrial carnivores

Several species of terrestrial carnivores (Mammalia: Carnivora) have bold contrasting color patterns that, in some species, apparently signal possession of noxious anal gland secretions, or even physical strength and great ferocity; yet the evolutionary drivers of both placement and patterning of these contrasting pelage colors on the body, and the ecological selection pressures underlying them, have yet to be systematically examined. Here we explore these issues and find not only that both boldly colored and dichromatic species do indeed often use anal gland secretions for defense, but also that such species are stockier, and live in more exposed habitats where other forms of antipredator defense are limited. We also show that white dorsa are found in sprayers that are primarily nocturnal; that horizontal stripes are found in species that have an ability to spray anal secretions accurately; and that facial stripes are found in burrowing species that typically leave only their heads exposed to attack. Our phylogenetic reconstructions suggest that aposematic coloration has evolved more than once in terrestrial carnivores. We finish by outlining five evolutionary routes for patterns of pelage coloration in this taxon.     

Evidence from rhesus macaques suggests that male coloration plays a role in female primate mate choice

Male animals of many species use conspicuous coloration to attract mates. Among mammals, primates possess the most brilliant secondary sexual coloration. However, whether colour plays a part in primate female mate choice remains unknown. Adult male rhesus macaques undergo a hormonally regulated increased reddening of facial and anogenital skin during their mating season. We experimentally investigated whether red male facial coloration is preferred by simultaneously presenting female rhesus macaques (n = 6) with computer-manipulated pale and red versions of 24 different male faces. The duration and direction of gaze were measured to discern visual preferences. Females exhibited preferences for the red versions of male faces. It is proposed that male coloration might provide a cue to male quality.     

Pelage color variation in pocket gophers (Rodentia: Geomyidae) in relation to sex,age and differences in habitat

Pelage coloration is a phenotypic characteristic in mammals that could be associated with an individual's survival and fitness; thus coloration gains adaptive importance. In geomyids, pelage coloration shows a relationship with the color of soils on which they live, mainly freshly dug soil of their burrows. This characteristic could be due to a camouflage adaptation to avoid predators. Pocket gophers disperse aboveground to establish a territory before they reach reproductive condition, and males disperse longer distances than females. The aim of this study was to evaluate pelage color variation in pocket gophers (Thomomys anitae) in relation to habitat differences, sex, and age, and determine its association to the color of the soil on which they live. Brightness of T. anitae's dorsal pelage coloration and that of soil samples from five different habitats in the Baja California peninsula, Mexico were measured to test four hypotheses: (1) Subadults show a wide coloration range, but extreme colors are lost in adulthood due to natural selection. (2) Males are more vulnerable to depredation than females; therefore, males’ coloration is more homogenous as a protective camouflage. (3) In open habitats pocket gophers are more exposed to being detected by predators, therefore their pelage coloration pattern is less variable than that of individuals from habitats with more vegetation cover. (4) Pelage coloration better matches soil coloration in moist conditions similar to that of freshly dug soil of their burrows. The results confirmed our predictions; however, selection does not impose an equal pressure on pelage coloration on the five habitats evaluated; other factors such as population density and predator presence need to be assessed. The strongest effects are found in the most open habitat, and there is less strong support for predictions in habitats where predator assemblage is diminished.     

No evidence for color or size preference in either sex of a dichromatic stream fish, Percina roanoka

Sexual dimorphism is hypothesized to be the result of differential selection pressures between the sexes. Dimorphic traits can serve as indicators of mate quality, altering mate preferences in the opposite sex in favor of a conspicuous trait. Common indicators of mate quality include color and size, with traditional assumptions and evidence predicting a preference for more colorful and/or larger sized mates in many species. Both male and female preferences for more colorful and larger mates within a species are rarely examined simultaneously, however. We examined a sexually dichromatic freshwater fish, Percina roanoka and found that male coloration is positively correlated with size, suggesting color may function as an indicator of viability. We tested preferences for coloration and size in both sexes in a dichotomous mate choice setup in which only visual signals were exchanged. Neither females nor males exhibited a color or size preference in individuals of the opposite sex. Visual cues alone therefore appear to be insufficient to elicit a significant preference in both sexes of this species. Male coloration in P. roanoka does not appear to be driven solely by female preference.     

Ecological and behavioral correlates of coloration in artiodactyls: systematic analyses of conventional hypotheses

To test the generality of adaptive explanations for coat colorationin even-toed ungulates, we examined the literature for hypothesesthat have been proposed for color patterns exhibited by thistaxon, and we derived a series of predictions from each hypothesis.Next, we collected information on the color, behavioral, andecological characteristics of 200 species of even-toed ungulatesand coded this in binary format. We then applied chi-squareor Fisher's Exact probability tests that pitted presence ofa color trait against presence of an ecological or behavioralvariable for cervids, bovids, and all artiodactyls. Finally,we reanalyzed the data by using concentrated-changes tests anda composite molecular and taxonomic phylogeny. Hinging our findingson whether associations persisted after controlling for sharedancestry, we found strong support for hypotheses suggestingeven-toed ungulates turn lighter in winter to aid in concealmentor perhaps thermoregulation, striped coats in adults and spottedpelage in young act as camouflage, side bands and dark facesassist in communication, and dark pelage coloration is mostcommon in species living in the tropics (Gloger's rule). Whereaswhite faces, dark legs, white legs, dark tails, and white tailsdid not appear to assist in communication alone, legs and tailsthat were either dark or white (i.e., conspicuous) did seemto be linked with communication. There was moderate supportfor hypotheses that countershading aids concealment, that whitefaces are a thermoregulatory device, and that white rumps areused in intraspecific communication. There was weak supportfor spots in adults and stripes in young providing camouflageand for dark leg markings being a form of disruptive coloration.We found little or no evidence that overall coat color servesas background matching, that side bands are disruptive colorationdevices, or that white rumps help in thermoregulation. Concealmentappears the principal force driving the evolution of colorationin ungulates with communication, and then thermoregulation,playing less of a role.     

Color Vision Variation and Foraging Behavior in Wild Neotropical Titi Monkeys (<Emphasis Type="Italic">Callicebus brunneus</Emphasis>): Possible Mediating Roles for Spatial Memory and Reproductive Status

The selective advantages to primates of trichromatic color vision, allowing discrimination among the colors green, yellow, orange, and red, remain poorly understood. We test the hypothesis that, for primates, an advantage of trichromacy over dichromacy, in which such colors are apt to be confused, lies in the detection of yellow, orange, or red (YOR) food patches at a distance, while controlling for the potentially confounding influences of reproductive status and memory of food patch locations. We employ socially monogamous titi monkeys (Callicebus brunneus) which, like most platyrrhine primates, have polymorphic color vision resulting in populations containing both dichromatic and trichromatic individuals. Wild Callicebus brunneus spent most foraging time in YOR food patches, the locations of most of which were likely to have been memorable for the subjects. Overall, both dichromatic and trichromatic females had significantly higher encounter rates than their dichromatic male pair mates for low-yield ephemeral YOR food patches whose locations were less likely to have been remembered. We detected no difference in the encounter rates of dichromatic and trichromatic females for such patches. However, the data suggest that such a difference may be detectable with a larger sample of groups of Callicebus brunneus, a larger sample of foraging observations per group, or both. We propose that a trichromatic advantage for foraging primates may be realized only when individuals’ energy requirements warrant searching for nonmemorable YOR food patches, a context for selection considerably more limited than is often assumed in explanations of the evolution of primate color vision.