Colours of domestication

During the last decade, coat colouration in mammals has been investigated in numerous studies. Most of these studies addressing the genetics of coat colouration were on domesticated animals. In contrast to their wild ancestors, domesticated species are often characterized by a huge allelic variability of coat‐colour‐associated genes. This variability results from artificial selection accepting negative pleiotropic effects linked with certain coat‐colour variants. Recent studies demonstrate that this selection for coat‐colour phenotypes started at the beginning of domestication. Although to date more than 300 genetic loci and more than 150 identified coat‐colour‐associated genes have been discovered, which influence pigmentation in various ways, the genetic pathways influencing coat colouration are still only poorly described. On the one hand, similar coat colourations observed in different species can be the product of a few conserved genes. On the other hand, different genes can be responsible for highly similar coat colourations in different individuals of a species or in different species. Therefore, any phenotypic classification of coat colouration blurs underlying differences in the genetic basis of colour variants. In this review we focus on (i) the underlying causes that have resulted in the observed increase of colour variation in domesticated animals compared to their wild ancestors, and (ii) the current state of knowledge with regard to the molecular mechanisms of colouration, with a special emphasis on when and where the different coat‐colour‐associated genes act.     

Changes in molluscan neurosecretory cells during reproductive cessation: cause or effect?

The pond snail Lymnaea stagnalis has a maximum life span of about 22 months. At the age of about 250 days animals start to decrease egg laying activity and at about 500 days most animals ceased egg laying activity. At the age of cessation of egg laying the neurosecretory caudodorsal cells (CDCs) which control egg laying in Lymnaea exhibit reduced branching patterns. At this stage the cells still exhibit their physiological properties. CDCs still contain biologically active peptides and in the isolated CNS they still exhibit an afterdischarge upon electrical stimulation. Probably in the intact animal cessation of egg laying occurs because the CDCs are not activated anymore by natural egg laying inducing stimuli. In very old animals CDCs exhibit signs of degeneration indicating that cell death occur. After an extended period of no egg laying of Lymnaea physiological changes occur in the CDCs. CDCs from animals after an extended period of no egg laying failed to exhibit an afterdischarge. In such CDCs chemical and electrical coupling among the CDCs are reduced. Morphologically reduced CDCs predominantly fail to exhibit an afterdischarge. However, there are minimally branched CDCs that still could give an afterdischarge. Probably morphological reduction is not the only factor that defines afterdischarge failure. At present we suggest the following sequence of changes. 1. Morphological reduction of CDC branching patterns. 2. Cessation of egg laying. 3. Physiological changes in the CDCs resulting in afterdischarge failure. 4. Further morphological and physiological deterioration of CDCs.     

A generalised mimicry system involving angiosperm flower colour, pollen and bumblebees’ innate colour preferences

Flower colour is a major advertisement signal of zoophilous plants for pollinators. Bees, the main pollinators, exhibit innate colour preferences, which have often been attributed to only one single floral colour, though most flowers display a pattern of two or several colours. The existing studies of floral colour patterns are mostly qualitative studies. Using a model of bee colour vision we quantitatively investigate two questions: whether or not component colours of floral colour patterns may mimic pollen signals, and whether or not bumblebees exhibit innate preferences for distinct parameters of naturally existing floral colour patterns. We analysed the spectral reflectances of 162 plant species with multicoloured flowers and inflorescences, distiniguishing between inner and outer colours of floral colour patterns irrespective of the particular structures so coloured.We found that:– The inner colour of radially symmetrical flowers and inflorescences and of zygomorphic flowers appears less diverse to bees than the peripheral colour.– The inner colour of most radial flowers and inflorescences as well as the inner colour of a large number of non-related zygomorphic flowers appears to bees to be very similar to that of pollen.– Bumblebees (Bombus terrestris) exhibit innate preferences for two-coloured over single-coloured dummy flowers in a spontaneous choice test.– Bumblebees exhibit innate preferences for dummy flowers with a large over those with a small centre area.– Bumblebees exhibit innate preferences for dummy flowers with a centre colour similar to that of pollen over those with another centre colour.Our findings support the hypotheses that the inner component of floral colour patterns could be interpreted as a generalised and little recognised form of mimicry of the colour of visually displayed pollen, that bumblebees exhibit innate preferences regarding colour and size parameters of floral colour patterns, and that these correspond to visually displayed pollen. These findings together suggest a prominent role of floral colour patterns in advertisement to and guidance of naive flower visitors.     

Spottier targets are less attractive to tabanid flies: on the tabanid-repellency of spotty fur patterns

During blood-sucking, female members of the family Tabanidae transmit pathogens of serious diseases and annoy their host animals so strongly that they cannot graze, thus the health of the hosts is drastically reduced. Consequently, a tabanid-resistant coat with appropriate brightness, colour and pattern is advantageous for the host. Spotty coats are widespread among mammals, especially in cattle (Bos primigenius). In field experiments we studied the influence of the size and number of spots on the attractiveness of test surfaces to tabanids that are attracted to linearly polarized light. We measured the reflection-polarization characteristics of living cattle, spotty cattle coats and the used test surfaces. We show here that the smaller and the more numerous the spots, the less attractive the target (host) is to tabanids. We demonstrate that the attractiveness of spotty patterns to tabanids is also reduced if the target exhibits spottiness only in the angle of polarization pattern, while being homogeneous grey with a constant high degree of polarization. Tabanid flies respond strongly to linearly polarized light, and we show that bright and dark parts of cattle coats reflect light with different degrees and angles of polarization that in combination with dark spots on a bright coat surface disrupt the attractiveness to tabanids. This could be one of the possible evolutionary benefits that explains why spotty coat patterns are so widespread in mammals, especially in ungulates, many species of which are tabanid hosts.     

Mutations in ASIP and MC1R: dominant black and recessive black alleles segregate in native Swedish sheep populations

By studying genes associated with coat colour, we can understand the role of these genes in pigmentation but also gain insight into selection history. North European short‐tailed sheep, including Swedish breeds, have variation in their coat colour, making them good models to expand current knowledge of mutations associated with coat colour in sheep. We studied ASIP and MC1R, two genes with known roles in pigmentation, and their association with black coat colour. We did this by sequencing the coding regions of ASIP in 149 animals and MC1R in 129 animals from seven native Swedish sheep breeds in individuals with black, white or grey fleece. Previously known mutations in ASIP [recessive black allele: g.100_105del (D₅) and/or g.5172T>A] were associated with black coat colour in Klövsjö and Roslag sheep breeds and mutations in both ASIP and MC1R (dominant black allele: c.218T>A and/or c.361G>A) were associated with black coat colour in Swedish Finewool. In Gotland, Gute, Värmland and Helsinge sheep breeds, coat colour inheritance was more complex: only 11 of 16 individuals with black fleece had genotypes that could explain their black colour. These breeds have grey individuals in their populations, and grey is believed to be a result of mutations and allelic copy number variation within the ASIP duplication, which could be a possible explanation for the lack of a clear inheritance pattern in these breeds. Finally, we found a novel missense mutation in MC1R (c.452G>A) in Gotland, Gute and Värmland sheep and evidence of a duplication of MC1R in Gotland sheep.     

An investigation into the genetic background of coat colour dilution in a Charolais x German Holstein F2 resource population

The molecular background of many loci affecting coat colour inheritance in cattle is still incompletely characterized, although it is known that coat colour results from the joint effects of several loci, e.g. agouti, extension and dilution. Dilution alleles are responsible for a dilution effect on the original coat colour of an individual, which is determined by the agouti and extension loci. Different loci affecting dilution of pigment are suggested in Charolais (Dc) and Simmental (Ds). To enable chromosomal mapping of the Dc mutation, 133 animals from an F2 full-sib resource population generated from a cross of Charolais and German Holstein were scored for the coat colour dilution phenotype. Linkage analysis covering all autosomes revealed a significant linkage of the dilution phenotype with microsatellite markers on bovine chromosome 5. No recombination was observed between marker ETH10 and the Dc locus. Positional and functional information identified the bovine silver homolog (SILV) gene as a candidate for the Dc mutation. Results from comparative sequencing of the SILV gene in individuals with different dilution coat colour phenotypes confirmed the presence of a c.64G>A non-synonymous mutation, which had previously been identified in the Charolais breed. The alleles at this locus were associated with coat colour dilution in this study. However, further investigation of colour inheritance within the F2 resource population indicated that a single diallelic mutation in the SILV gene cannot explain the total observed variation of coat colour dilution.     

Coat colours in the Massese sheep breed are associated with mutations in the agouti signalling protein (ASIP) and melanocortin 1 receptor (MC1R) genes

Massese is an Italian dairy sheep breed characterized by animals with black skin and horns and black or apparent grey hairs. Owing to the presence of these two coat colour types, this breed can be considered an interesting model to evaluate the effects of coat colour gene polymorphisms on this phenotypic trait. Two main loci have been already shown to affect coat colour in sheep: Agouti and Extension coding for the agouti signalling protein (ASIP) and melanocortin 1 receptor (MC1R) genes, respectively. The Agouti locus is affected by a large duplication including the ASIP gene that may determine the Agouti white and tan allele (A(Wt)). Other disrupting or partially inactivating mutations have been identified in exon 2 (a deletion of 5 bp, D(5); and a deletion of 9 bp, D(9)) and in exon 4 (g.5172T>A, p.C126S) of the ASIP gene. Three missense mutations in the sheep MC1R gene cause the dominant black E(D) allele (p.M73K and p.D121N) and the putative recessive e allele (p.R67C). Here, we analysed these ASIP and MC1R mutations in 161 Massese sheep collected from four flocks. The presence of one duplicated copy allele including the ASIP gene was associated with grey coat colour (P = 9.4E-30). Almost all animals with a duplicated copy allele (37 out of 41) showed uniform apparent grey hair and almost all animals without a duplicated allele (117 out of 120) were completely black. Different forms of duplicated alleles were identified in Massese sheep including, in almost all cases, copies with exon 2 disrupting or partially inactivating mutations making these alleles different from the A(Wt) allele. A few exceptions were observed in the association between ASIP polymorphisms and coat colour: three grey sheep did not carry any duplicated copy allele and four black animals carried a duplicated copy allele. Of the latter four sheep, two carried the E(D) allele of the MC1R gene that may be the cause of their black coat colour. The coat colour of all other black animals may be determined by non-functional ASIP alleles (non-agouti alleles, A(a)) and in a few cases by the E(D) Extension allele. At least three frequent ASIP haplotypes ([D(5):g.5172T], [N:g.5172A] and [D(5):g.5172A]) were detected (organized into six different diplotypes). In conclusion, the results indicated that coat colours in the Massese sheep breed are mainly derived by combining ASIP and MC1R mutations.     

Avian egg colour and sexual selection: does eggshell pigmentation reflect female condition and genetic quality?

Avian egg colour has been explained as mainly serving crypsis or mimetism, although the function of certain colours (e.g. blue and green) has not yet been demonstrated. We interpret egg colour as a sexually selected signal of the laying female's genetic quality to its mate in order to induce a higher allocation of paternal care. The blue–green pigment biliverdin is an antioxidant, the deposition of which may signal antioxidant capacity whereas the deposition of the brown pigment protoporphyrin, a pro‐oxidant, may signal tolerance of oxidative stress. Egg ground colour is presumably heritable and phylogenetically labile. The hypothesis can be applied to animals with colourful eggs and paternal care.     

Molecular genetics of coat colour variations in White Galloway and White Park cattle

White Galloway cattle exhibit three different white coat colour phenotypes, that is, well marked, strongly marked and mismarked. However, mating of individuals with the preferred well or strongly marked phenotype also results in offspring with the undesired mismarked and/or even fully black coat colour. To elucidate the genetic background of the coat colour variations in White Galloway cattle, we analysed four coat colour relevant genes: mast/stem cell growth factor receptor (KIT), KIT ligand (KITLG), melanocortin 1 receptor (MC1R) and tyrosinase (TYR). Here, we show that the coat colour variations in White Galloway cattle and White Park cattle are caused by a KIT gene (chromosome 6) duplication and aberrant insertion on chromosome 29 (Cs₂₉) as recently described for colour‐sided Belgian Blue. Homozygous (Cs₂₉/Cs₂₉) White Galloway cattle and White Park cattle exhibit the mismarked phenotype, whereas heterozygous (Cs₂₉/wt₂₉) individuals are either well or strongly marked. In contrast, fully black individuals are characterised by the wild‐type chromosome 29. As known for other cattle breeds, mutations in the MC1R gene determine the red colouring. Our data suggest that the white coat colour variations in White Galloway cattle and White Park cattle are caused by a dose‐dependent effect based on the ploidy of aberrant insertions and inheritance of the KIT gene on chromosome 29.     

On the measurement and classification of colour in studies of animal colour patterns

In studies of animal colouration it is no longer necessary to rely on subjective assessments of colour and conspicuousness, nor on methods which rely upon human vision. This is important because animals vary greatly in colour vision and colour is context-dependent. New methods make it practical to measure the colour spectrum of pattern elements (patches) of animals and their visual backgrounds for the conditions under which patch spectra reach the conspecific's, predator's or prey's eyes. These methods can be used in both terrestrial and aquatic habitats. A patch's colour is dependent not only upon its reflectance spectrum, but also upon the ambient light spectrum, the transmission properties of air or water, and the veiling light spectrum. These factors change with time of day, weather, season and microhabitat, so colours must be measured under the conditions prevalent when colour patterns are normally used. Methods of measuring, classifying and comparing colours are presented, as well as techniques for assessing the conspicuousness of colour patterns as a whole. Some implications of the effect of environmental light and vision are also discussed.     

Black-ear gene and blood polymorphism in four southern Chinese cattle groups

The gene for black-ear coat colour pattern, commonly found among cattle of tropical origin, was observed in 809 animals of four breeds of local cattle in southern China. Gene frequencies for Tf, Hb and Alb demonstrated that these groups of cattle were quite divergent from Bos taurus. These breeds of cattle are thought to be descended from ancient Chinese cattle. At the same time certain influences observed in coat colour may be derived from Bali cattle.     

Microspatial genetic heterogeneity and gene flow in stray cats (Felis catus L.): a comparison of coat colour and microsatellite loci

We analysed levels of genetic differentiation between nine local urban colonies of stray cats using eight coat colour and nine microsatellite loci. Both types of markers revealed a strong differentiation between colonies (FST = 0.15 and 0.09 for coat colour and microsatellite loci, respectively). Three coat colour loci showed extreme levels of genetic differentiation comparatively to other loci and are strongly suspected to be under divergent selective pressures. Microsatellite loci showed significant heterozygote deficiency within colonies (FIS = 0.14), suggesting that coat colour loci are not appropriate to investigate genetic structure at a fine scale because coat colour allele frequencies are based on Hardy-Weinberg equilibrium. The reported pattern conformed to that predicted from the social structuring of cat colonies: aggressive exclusion of immigrants, inbreeding and very low dispersal rate.     

Why the leopard got its spots: relating pattern development to ecology in felids

A complete explanation of the diversity of animal colour patterns requires an understanding of both the developmental mechanisms generating them and their adaptive value. However, only two previous studies, which involved computer-generated evolving prey, have attempted to make this link. This study examines variation in the camouflage patterns displayed on the flanks of many felids. After controlling for the effects of shared ancestry using a fully resolved molecular phylogeny, this study shows how phenotypes from plausible felid coat pattern generation mechanisms relate to ecology. We found that likelihood of patterning and pattern attributes, such as complexity and irregularity, were related to felids' habitats, arboreality and nocturnality. Our analysis also indicates that disruptive selection is a likely explanation for the prevalence of melanistic forms in Felidae. Furthermore, we show that there is little phylogenetic signal in the visual appearance of felid patterning, indicating that camouflage adapts to ecology over relatively short time scales. Our method could be applied to any taxon with colour patterns that can reasonably be matched to reaction-diffusion and similar models, where the kinetics of the reaction between two or more initially randomly dispersed morphogens determines the outcome of pattern development.     

The butterfly Papilio xuthus detects visual motion using chromatic contrast

Many insects’ motion vision is achromatic and thus dependent on brightness rather than on colour contrast. We investigate whether this is true of the butterfly Papilio xuthus, an animal noted for its complex retinal organization, by measuring head movements of restrained animals in response to moving two-colour patterns. Responses were never eliminated across a range of relative colour intensities, indicating that motion can be detected through chromatic contrast in the absence of luminance contrast. Furthermore, we identify an interaction between colour and contrast polarity in sensitivity to achromatic patterns, suggesting that ON and OFF contrasts are processed by two channels with different spectral sensitivities. We propose a model of the motion detection process in the retina/lamina based on these observations.     

A pre-pattern formation mechanism for the spiral-type patterns of the sunflower head

We propose a reaction-diffusion system for the laying down of the spacing patterns of the sunflower head. A detailed analysis shows that spatially varying diffusion coefficients lead to a spiral-type pre-pattern. The relationship between this pre-pattern and the fructification pattern of the sunflower head is discussed. The reaction kinetics chosen is of the Gierer-Meinhardt type. Furthermore, it is suggested that a pre-pattern formation mechanism of this type may also play a role in phyllotaxis.     

Genetic parameters of coat colour in golden fox (Vulpes vulpes L.)

Genetic parameters (heritability, genetic and phenotypic correlations) of chosen coat colour traits of golden fox were estimated. 1013 animals, born on the Sniaty fox farm (Poland) in 1985-1999 were evaluated. In 1993-1999 colour type was additionally assessed for 833 animals, by detailed evaluation of coat colour on the back and sides of the body, throat colour, belly colour and the amount of silver hair. The REML method was used to estimate genetic (co)variance components. Data were transformed using the probit transformation. Heritability estimates for coat traits were low (0.04 to 0.22). Values of most of the estimated genetic parameters (h2, rG, rP) were comparable to those frequently reported for other colour types of silver fox.     

Pigment-based skin colour in the blue-footed booby: an honest signal of current condition used by females to adjust reproductive investment

In monogamous species, the value of present reproduction is affected by the current condition of the mate, and females may use male ornaments to evaluate his condition and adjust their level of investment according. Many animals display colour in fleshy structures which may be accurate indicators of quality due to their potentially rapid response to changes in condition. Here we show that in the blue-footed booby, Sula nebouxii, male foot colour is structurally (collagen arrays) and pigment based. In 48 h foot colour became duller when males were food deprived and brighter when they were re-fed with fresh fish. Variation of dietary carotenoids induced comparable changes in cell-mediated immune function and foot colour, suggesting that carotenoid-pigmentation reveals the immunological state of individuals. These results suggest that pigment-based foot colour is a rapid honest signal of current condition. In a second experiment, we found that rapid variation in male foot colour caused parallel variation in female reproductive investment. One day after the first egg was laid we captured the males and modified the foot colour of experimental males with a non-toxic and water resistant duller blue intensive make-up, mimicking males in low condition. Females decreased the size of their second eggs, relative to the second egg of control females, when the feet of their mates were experimentally duller. Since brood reduction in this species is related to size differences between brood mates at hatching, by laying lighter second eggs females are facilitating brood reduction. Our data indicate that blue-footed booby females are continuously evaluating their mates and can perform rapid adjustments of reproductive investment by using dynamic sexual traits. We suggest that this fine-tuned adjustment may be widespread in socially monogamous animals.     

Mode Transitions in a Model Reaction–Diffusion System Driven by Domain Growth and Noise

Pattern formation in many biological systems takes place during growth of the underlying domain. We study a specific example of a reaction-diffusion (Turing) model in which peak splitting, driven by domain growth, generates a sequence of patterns. We have previously shown that the pattern sequences which are presented when the domain growth rate is sufficiently rapid exhibit a mode-doubling phenomenon. Such pattern sequences afford reliable selection of certain final patterns, thus addressing the robustness problem inherent of the Turing mechanism. At slower domain growth rates this regular mode doubling breaks down in the presence of small perturbations to the dynamics. In this paper we examine the breaking down of the mode doubling sequence and consider the implications of this behaviour in increasing the range of reliably selectable final patterns.     

Male reproductive senescence: the price of immune-induced oxidative damage on sexual attractiveness in the blue-footed booby

In animals, male reproduction is commonly a function of sexual attractiveness, based on the expression of sexually dimorphic traits that advertise genuinely the male's quality. Male performance may decline with age because physiological functions underlying sexual attractiveness may be affected by senescence. Here we show that a sexual signal (foot colour) declines with age, due probably to the deleterious effects of oxidative damage. We found that in the blue-footed booby Sula nebouxii foot colour during courtship was less attractive in senescent than in middle-aged males. In addition, we increased reactive oxygen species experimentally by immunizing males with lipopolysaccharide, a bacterial cell wall component that induces marked oxidative stress in animals. The immune system activation induced greater lipid peroxidation and invoked changes on colour expression (less attractive), particularly in senescent males. These results support the idea that oxidative stress affects reproductive senescence, and suggest that oxidative damage might be a proximal mechanism underlying age-reproductive patterns in long-lived animals.