The dark side of coloration: Ecogeographical evidence supports Gloger's rule in American marsupials

Geographical distribution of color phenotypes and associations with ecological predictors remains poorly understood. An important geographic pattern concerning this topic is Gloger's rule, which predicts the increase of pigmentation in endothermic animals from cold and dry to warm and wet environments. Didelphid marsupials exhibit a variety of color patterns, ranging from light and dark uniform to more complex colorations. However, surprisingly little is known about the adaptive significance of dark coloration in this singular group of mammals. Using a phylogenetic comparative approach, we investigated whether coloration in different body regions of didelphids (i.e., dorsum and face) is associated with variables representing heat and humidity of the environment, as predicted by Gloger's rule. We demonstrated that Gloger's rule explains the interspecific color variation in American marsupials, especially when considering the facial region. Thus, dark coloration was more frequent among didelphid species occupying warm and wet environments than cold and dry environments. We also discuss the selective forces that can potentially explain coat color variation in didelphid marsupials, including camouflage, pathogen resistance, and pleiotropy hypotheses.     

Eggshells as hosts of bacterial communities: An experimental test of the antimicrobial egg coloration hypothesis

Oviparous animals have evolved multiple defenses to prevent microbes from penetrating their eggs and causing embryo mortality. In birds, egg constituents such as lysozyme and antibodies defend against microbial infestation, but eggshell pigments might also impact survival of bacteria. If so, microbes could exert an important selective pressure on the evolution of eggshell coloration. In a previous lab experiment, eggshell protoporphyrin caused drastic mortality in cultures of Gram positive, but not Gram negative, bacteria when exposed to light. Here, we test this “photodynamic antimicrobial hypothesis” in a field experiment. In a paired experimental design, we placed sanitized brown, protoporphyrin‐rich chicken eggs alongside white eggs that lack protoporphyrin. We deployed eggs for 48 hr without incubation, as can occur between laying and incubation, when microbial infection risk is highest. Eggs were placed on the open ground exposed to sunlight and in dark underground storm‐petrel burrows. We predicted that the proportion of Gram‐positive bacteria on brown eggs should be lower when exposed to sunlight than when kept in the dark, but we expected no such difference for white eggs. Although our data revealed variation in bacterial community composition, the proportion of Gram‐positive bacteria on eggshells did not vary by egg color, and there was no interaction between egg color and location. Instead, Gram‐positive bacteria were proportionally more common on eggs on the ground than eggs in burrows. Overall, our experiment did not support the photodynamic antimicrobial hypothesis. The diverse range of avian egg colors is generated by just two pigments, but over 10 hypotheses have been proposed for the evolution of eggshell color. If our results are generalizable, eggshell protoporphyrin might not play a substantial role in defending eggs against microbes, which narrows the field of candidate hypotheses for the evolution of avian eggshell coloration.     

Contrasting coloration in terrestrial mammals

Here I survey, collate and synthesize contrasting coloration in 5000 species of terrestrial mammals focusing on black and white pelage. After briefly reviewing alternative functional hypotheses for coloration in mammals, I examine nine colour patterns and combinations on different areas of the body and for each mammalian taxon to try to identify the most likely evolutionary drivers of contrasting coloration. Aposematism and perhaps conspecific signalling are the most consistent explanations for black and white pelage in mammals; background matching may explain white pelage. Evidence for contrasting coloration is being involved in crypsis through pattern blending, disruptive coloration or serving other functions, such as signalling dominance, lures, reducing eye glare or in temperature regulation has barely moved beyond anecdotal stages of investigation. Sexual dichromatism is limited in this taxon and its basis is unclear. Astonishingly, the functional significance of pelage coloration in most large charismatic black and white mammals that were new to science 150 years ago still remains a mystery.     

Effects of substrate color on intraspecific body color variation in the toad‐headed lizard,Phrynocephalus versicolor

Diversity in animal coloration is generally associated with adaptation to their living habitats, ranging from territorial display and sexual selection to predation or predation avoidance, and thermoregulation. However, the mechanism underlying color variation in toad‐headed Phrynocephalus lizards remains poorly understood. In this study, we investigated the population color variation of Phrynocephalus versicolor. We found that lizards distributed in dark substrate have darker dorsal coloration (melanic lizards) than populations living in light substrates. This characteristic may improve their camouflage effectiveness. A reciprocal substrate translocation experiment was conducted to clarify the potential role of morphological adaptation and physiological plasticity of this variation. Spectrometry technology and digital photography were used to quantify the color variation of the above‐mentioned melanic and nonmelanic P. versicolor populations and their native substrate. Additionally, substrate color preference in both populations was investigated with choice experiments. Our results indicate that the melanic and nonmelanic populations with remarkable habitat color difference were significantly different on measured reflectance, luminance, and RGB values. Twenty‐four hours, 30 days, and 60 days of substrate translocation treatment had little effects on dorsal color change. We also found that melanic lizards choose to live in dark substrate, while nonmelanic lizards have no preference for substrate color. In conclusion, our results support that the dorsal coloration of P. versicolor, associated with substrate color, is likely a morphological adaptation rather than phenotypic plasticity.     

Maintenance of larval color polymorphism in Orgyia antiqua (Lepidoptera: Lymantriidae): evaluating the role of thermal adaptation

Intraspecific color polymorphism is widespread in insects, and various mechanisms have been proposed to explain its maintenance. Some explanations rely on the effect of body color on the organism's thermal physiology. Darker individuals accumulate solar energy more efficiently, and therefore, dark body coloration in insects is frequently presumed to be an adaptation to low temperature conditions. However, it is largely unclear what is the importance of the thermal biology in comparison to other potential selective forces on body coloration. In this study, we evaluated the role of temperature as a potential selective factor maintaining color polymorphism in aposematic larvae of the moth Orgyia antiqua L. It was found that darker, and thus less aposematic, larvae accumulated solar energy more efficiently. However, in a set of laboratory and outdoor experiments, we found no evidence of temperature-dependent performance of different color morphs or in development of different morphs induced by rearing temperature. We conclude that the effects related to thermal physiology are not likely important determinants of optimal coloration in O. antiqua. The reasons may lie in high mobility of the larvae, which allows for effective behavioral thermoregulation, which is also shown in this study. Our results caution against an uncritical extrapolation of results obtained for model organisms and indicate the need for giving more attention to the species-specific ecological background in ecophysiological studies.     

Background matching,disruptive coloration,and differential use of microhabitats in two neotropical grasshoppers with sexual dichromatism

Cryptic coloration is an adaptative defensive mechanism against predators. Color patterns can become cryptic through background coloration‐matching and disruptive coloration. Disruptive coloration may evolve in visually heterogeneous microhabitats, whereas background matching could be favored in chromatically homogeneous microhabitats. In this work, we used digital photography to explore the potential use of disruptive coloration and background matching in males and females of two grasshopper species of the Sphenarium genus in different habitats. We found chromatic differences in the two grasshopper species that may be explained by local adaptation. We also found that the females and males of both species are dichromatic and seem to follow different color cryptic strategies, males are more disruptive than females, whereas females have a high background matching with less disruptive elements. The selective pressures of the predators in different microhabitats and the differences in mobility between sexes may explain the color pattern divergence between females and males. Nevertheless, more field experiments are needed in order to understand the relative importance of disruptive and background matching coloration in the evolution of sexual dichromatism in these grasshoppers.     

Defining disruptive coloration and distinguishing its functions

Disruptive coloration breaks up the shape and destroys the outline of an object, hindering detection. The principle was first suggested approximately a century ago, but, although research has significantly increased, the field remains conceptually unstructured and no unambiguous definition exists. This has resulted in variable use of the term, making it difficult to formulate testable hypotheses that are comparable between studies, slowing down advancement in this field. Related to this, a range of studies do not effectively distinguish between disruption and other forms of camouflage. Here, we give a formal definition of disruptive coloration, reorganize a range of sub-principles involved in camouflage and argue that five in particular are specifically related to disruption: differential blending; maximum disruptive contrast; disruption of surface through false edges; disruptive marginal patterns; and coincident disruptive coloration. We discuss how disruptive coloration can be optimized, how it can relate to other forms of camouflage markings and where future work is particularly needed.     

Predation,thermoregulation, and wing color in pierid butterflies

Summary This paper explores two hypotheses about the relationships among predation, thermoregulation, and wing color in butterflies: First, that butterflies are susceptible to predation during thermally marginal periods (e.g., cool weather) when effective thermoregulation and flight are not possible; second, that Pieris butterflies are relatively unpalatable to visual predators, supporting the idea that the white wing pigment of Pieris represents aposematic coloration. Field experiments with Pieris and Colias in 1984 and 1985 demonstrate that substantial predation may occur during the morning period before butterflies are able to actively fly. Circumstantial evidence is presented to suggest that at least some of the predation is by small, cursorial mammals. Feeding experiments in the field using Grey Jays as predators indicate that Pieris napi and P. occidentalis are less palatable than other sympatric butterflies, including confamial Colias alexandra. These and previous results suggest that Pieris are edible but less preferred as prey by birds, and that the degree of palatibility may vary among Pieris species. The relatively low palatability of these Pieris is consistent with the hypothesis that their white pigmentation represents aposematic coloration; however, the cues by which potential bird predators might discriminate against Pieris have not been established.     

Variation of coat color in house mice throughout Asia

Coat color variation due to melanin pigment synthesis in house mice Mus musculus in Asia is described and found to be consistent with Gloger's rule, which states that individuals of endothermic animals are darker in humid habitats than those in drier habitats. Three properties of coat color (hue, value and chroma) were measured, and a lightness variable was derived from a principal components analysis using 428 skin specimens representing three subspecies from 85 localities. Dorsal coat color ranged from yellow through brown to black, whereas ventral coat color ranged from white to black. Dorsal coat color varied less than the ventral color. In our samples, the variation in coat color in natural populations was far less than that observed in the laboratory. We found a significant correlation between the lightness variable of dorsal coat color and precipitation. Dark coat color was observed in more humid and closed habitats (darker background color), and pale coat color in drier, more open habitats (lighter background color). This result might imply the role of concealment as a selective force affecting dorsal coat color that was observed in house mice. We also discussed other selective forces that could affect the coat color variation in house mice, such as resistance to bacterial degradation and thermoregulation. In addition, the color spectra of the dorsal pelage among the three subspecies were different, the major distinction being the environmental background color of the habitats in which they are distributed.     

Sexual selection mediated by the thermoregulatory effects of male colour pattern in the ambush bug Phymata americana

Sexual dimorphism in coloration is a taxonomically widespread phenomenon often attributed to sexual selection on visual signals. However, the ambush bug Phymata americana exhibits sexual dimorphism in coloration that has no apparent signalling function. Here we provide evidence that colour pattern in this species influences male mating success indirectly through its effect on thermoregulation. We demonstrate, using experimental manipulation, that individuals with dark colour pattern achieve higher thoracic temperatures under illumination. We also show that dark colour pattern predicted mate-searching success but only under thermally challenging conditions (i.e. cool ambient temperature). As far as we are aware, this is the first study to provide evidence that sexual dimorphism can be accounted for by sexual selection on thermoregulatory performance.     

Distribution of pigments in the shell of the gastropod <Emphasis Type="Italic">Littorina obtusata</Emphasis> (Linnaeus, 1758)

The patterns of pigment distribution in the shell of the gastropod Littorina obtusata were studied. It was determined that the background coloration of the periwinkle shell resulted from the coloration interaction of the external and internal parts of the ostracum. The coloration of the latter can be monochromatic or twolayer. The external and/or internal zones of the ostracum can be colored purple, white, orange, yellow and greenish. Only 11 of 25 possible color combinations were recorded. Four additional versions of shell background coloration resulted from partial depigmentation of external or internal parts of ostracum. The mottling pattern corresponded to white or depigmented lenticular sites in the external part of the ostracum. The bands on the shell may be subdivided into two groups according to their means of formation. The bands that appeared due to redistribution of pigments forming background coloration belonged to the first group, the bands arising as a layer of additional (white, yellow, orange) pigment belonged to the second group. Various band versions could occur simultaneously in the same individual.     

Investigation of the role of the agouti signaling protein gene (ASIP) in coat color evolution in primates

We investigated variation in the gene encoding the agouti signaling protein (ASIP) in relation to coat color evolution in primates. We found little evidence that mutations in the coding region of ASIP have been involved in color changes among closely related primate species. Among many closely related species with differing coat color, the coding region of ASIP was identical. In two cases (Sulawesi macaque and black lion tamarin) where species with almost completely black coat color had derived point mutations in exon 4 of the ASIP coding sequence, the same mutations did not alter coloration in other mammals and so probably do not affect ASIP function. Evolutionary reconstructions of two key phenotypes that are typically related to ASIP function—transverse phaeomelanin bands on hairs and pale ventral coloration—showed that these usually evolved concurrently, suggesting that loci acting downstream of ASIP may be involved. Analysis of dN/dS ratios revealed a likely change in functional constraint on ASIP following loss of agouti-banded hairs + pale ventral coloration, particularly in catarrhine primates (humans, apes, and Old World monkeys). Together with previous results on a lack of association of coat color with MC1R variation, these results suggest that other loci probably have an important role in primate coat color evolution.     

Hormonal control of pupal coloration in the painted lady butterfly Vanessa cardui

Pupae of the painted lady butterfly Vanessa cardui exhibit pupal color polyphenism consisting of white, dark and intermediate types. We investigated environmental factors affecting pupal coloration and the physiological mechanisms underlying the control of pupal color polyphenism in this species. Over 80% of larvae reared at 16 °C developed into pupae of dark types, whereas over 82% of larvae at 32 °C developed into pupae of white types irrespective of long/short-day photoperiod conditions. When mature larvae reared at 32 °C were ligatured between thoracic and abdominal parts at three different pharate pupal stages, all of the head-thoracic parts developed into white pupae regardless of pupal stage, but all abdominal parts ligatured at the early pharate pupal stage only developed into dark pupae. These results indicate that temperature during larval stages is an important element affecting pupal coloration as an environmental cue in V. cardui, and that a factor(s) inducing white pupae is released from head-thoracic parts under conditions of high temperature. Additionally, when ligatured abdomens destined to develop into dark pupae were treated with crude extracts prepared from the central nervous system, all of the ligatured abdomens developed into white pupae at a level dependent on dose and pupal stage. These results suggest that the factor inducing white pupae is a key molecule controlling pupal color polyphenism in V. cardui.     

Warning coloration can be disruptive: aposematic marginal wing patterning in the wood tiger moth

Warning (aposematic) and cryptic colorations appear to be mutually incompatible because the primary function of the former is to increase detectability, whereas the function of the latter is to decrease it. Disruptive coloration is a type of crypsis in which the color pattern breaks up the outline of the prey, thus hindering its detection. This delusion can work even when the prey's pattern elements are highly contrasting; thus, it is possible for an animal's coloration to combine both warning and disruptive functions. The coloration of the wood tiger moth (Parasemia plantaginis) is such that the moth is conspicuous when it rests on vegetation, but when it feigns death and drops to the grass‐ and litter‐covered ground, it is hard to detect. This death‐feigning behavior therefore immediately switches the function of its coloration from signaling to camouflage. We experimentally tested whether the forewing patterning of wood tiger moths could function as disruptive coloration against certain backgrounds. Using actual forewing patterns of wood tiger moths, we crafted artificial paper moths and placed them on a background image resembling a natural litter and grass background. We manipulated the disruptiveness of the wing pattern so that all (marginal pattern) or none (nonmarginal pattern) of the markings extended to the edge of the wing. Paper moths, each with a hidden palatable food item, were offered to great tits (Parus major) in a large aviary where the birds could search for and attack the “moths” according to their detectability. The results showed that prey items with the disruptive marginal pattern were attacked less often than prey without it. However, the disruptive function was apparent only when the prey was brighter than the background. These results suggest that warning coloration and disruptive coloration can work in concert and that the moth, by feigning death, can switch the function of its coloration from warning to disruptive.     

Function of bright coloration in the wasp spider Argiope bruennichi (Araneae: Araneidae)

There are two major competing explanations for the counter-intuitive presence of bright coloration in certain orb-web spiders. Bright coloration could lure insect prey to the web vicinity, increasing the spider's foraging success. Alternatively, the markings could function as disruptive camouflage, making it difficult for the insect prey to distinguish spiders from background colour variation. We measured the prey capture rates of wasp spiders, Argiope bruennichi, that were blacked out, shielded from view using a leaf fragment, or left naturally coloured. Naturally coloured spiders caught over twice the number of prey as did either blacked-out or leaf-shielded spiders, and almost three times as many orthopteran prey. Spectrophotometer measurements suggest that the bright yellow bands on the spider's abdomen are visible to insect prey, but not the banding on the legs, which could disguise the spider's outline. Thus, our results provide strong support for the hypothesis that bright coloration in the wasp spider acts as a visual lure for insect prey and weak support for the hypothesis that the arrangement of the banding pattern across the spider's body disguises the presence of the spider on the web.     

Proximate mechanisms of colour variation in the frillneck lizard: geographical differences in pigment contents of an ornament

Animal coloration has evolved in contexts such as communication, camouflage, and thermoregulation. Most studies of animal coloration focus on its adaptive benefits, whereas its underlying mechanisms have received less attention despite their potential influence on adaptive benefits. In fish and reptiles, for example, colour variation from yellow to red can be produced by carotenoid and/or pteridine pigments, which differ dramatically in the way they are obtained (carotenoids through diet and pteridines synthesized de novo). Hence, potential adaptive benefits could differ greatly depending on the relative contribution to coloration of different pigments. In the present study, we investigate the mechanisms underlying colour variation in the frill of the Australian frillneck lizard (Sauropsida: Chlamydosaurus kingii). Frill colour varies between populations across the species' range (red, orange, yellow or white). We argue that this geographical variation results from different concentrations of carotenoids and pteridines in the frill. Frill carotenoid concentrations were lower in eastern populations (yellow and white forms), and pteridines were present only in the red and orange forms, thereby explaining their redder hues. The observed geographical variation in frill carotenoids suggests variation in carotenoid availability across the species' range, which is backed up by the finding that plasma carotenoid concentrations were higher in the red (western) compared to the yellow (eastern) form. Although no correlations were found between individual colour measurements, frill pigments and plasma carotenoids, our results suggest that selective pressures vary across the species' range and we speculate that predation pressures and/or intrasexual signalling context differ between forms.     

A blond coat color variation in meadow vole (Microtus pennsylvanicus)

Color mutations occur frequently among rodents. Here we describe a blond coat color mutation in the meadow vole (Microtus pennsylvanicus) that arose in a captive breeding colony established from wild-caught animals from southern Illinois. The blond coat coloration results from changes in the color and distribution of pigments in the hair. The mutation is monogenic autosomal recessive.     

Carapace color change in Uca pugilator as a response to temperature

Brachyurid species have various coloration patterns that fluctuate among individuals due to behavioral interactions or a changing environment. In the fiddler crab Uca pugilator, the historical notion is that color change is regulated by circadian rhythms. In this study, color patterns of U. pugilator were affected by changes in temperature; crab carapaces become light in warm temperatures and dark in colder temperatures. The response to temperature occurred within 15 min (often within 5 min of exposure to the treatment), suggesting that temperature may play a key role in color change, and it is activated not through a hormonal pathway, but rather a direct response of the chromatophores. Color change occurred differently between day and night for each sex, which implies that endogenous rhythms are not the sole mechanism for color change in U. pugilator. Both sexes became darker in the cold treatment, however there were differences between the sexes with high temperatures. Females did not show significant coloration changes, while males became significantly lighter and more speckled. Results from this study suggest sex-specific constraints in response to temperature that could be associated to morphological body mass to surface area ratios, as males have large cheliped, which may be involved in thermoregulation. Constraints could also be associated to different diel activities that each sex performs or visual cues associated with mating behaviors.     

Some like it hot: Intra-Population Variation in behavioral Thermoregulation in Color-Polymorphic pygmy Grasshoppers

Ectothermic animals rely on external heat sources and behavioral thermoregulation to control body temperature, and are characterized by possessing physiological and behavioural traits which are temperature dependent. It has therefore been suggested that constraints on the range of body temperatures available to individuals imposed by phenotypic properties, such as coloration, may translate into differential fitness and selection against thermally inferior phenotypes. In this paper, I report an association between thermal preferences and thermal capacity (the ability to warm up when insolated) across different genetically coded color morphs of the pygmy grasshopper Tetrix subulata. Data on behavioral thermoregulation of individuals in a laboratory thermal gradient revealed a preference for higher body temperatures in females than in males, and significant variation among colour morphs in preferred body temperatures in females, but not in males. The variation in females was in perfect accordance with estimates of morph-specific differences in thermal capacity. Thus, dark morphs not only attain higher temperatures when exposed to augmented illumination, but also prefer higher body temperatures, compared to paler morphs. This intra-population divergence probably reflects an underlying variation among colour morphs in temperature optima, and is consistent with the notion that coloration, behaviour and physiology evolve in concert.     

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.