Why colour in subterranean vertebrates? Exploring the evolution of colour patterns in caecilian amphibians

The proximate functions of animal skin colour are difficult to assign as they can result from natural selection, sexual selection or neutral evolution under genetic drift. Most often colour patterns are thought to signal visual stimuli; so,their presence in subterranean taxa is perplexing. We evaluate the adaptive nature of colour patterns in nearly a third of all known species of caecilians, an order of amphibians most of which live in tropical soils and leaf litter. We found that certain colour pattern elements in caecilians can be explained based on characteristics concerning above-ground movement. Our study implies that certain caecilian colour patterns have convergently evolved under selection and we hypothesize their function most likely to be a synergy of aposematism and crypsis, related to periods when individuals move overground. In a wider context, our results suggest that very little exposure to daylight is required to evolve and maintain a varied array of colour patterns in animal skin.     

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.     

Geographic patterns in fruit colour diversity: do leaves constrain the colour of fleshy fruits?

We tested for geographic patterns in fruit colour diversity. Fruit colours are thought to promote detection by seed dispersers. Because seed dispersers differ in their spectral sensitivities, we predicted that fruit colour diversity would be higher in regions with higher seed disperser diversity (i.e. the tropics). We collected reflectance data on 232 fruiting plant species and their natural backgrounds in seven localities in Europe, North and South America, and analysed fruit colour diversity according to the visual system of birds—the primary consumer types of these fruits. We found no evidence that fruit colours are either more conspicuous or more diverse in tropical areas characterised by higher seed disperser diversity. Instead, fruit colour diversity was lowest in central Brazil, suggesting that fruit colours may be more diverse in temperate regions. Although we found little evidence for geographic variation in fruit hues, the spectral properties of fruits were positively associated with the spectral properties of backgrounds. This result implies that fruit colours may be influenced by selection on the reflectance properties of leaves, thus constraining the evolution of fruit colour. Overall, the results suggest that fruit colours in the tropics are neither more diverse nor more conspicuous than temperate fruits, and that fruit colours may be influenced by correlated selection on leaf reflectance properties. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Colour vision: Is colour constancy real?

Colour constancy is typically weaker in the laboratory than it seems in our everyday experience. New measurements using real-world stimuli show that colour constancy is in fact almost perfect, and that several different perceptual mechanisms contribute to achieving it.     

Vision: can colour contribute to motion?

Whether colour patterns that have no luminance variation can evoke the perception of visual motion has long been a controversial issue. Recent studies using new and old techniques have now provided compelling evidence that colour can indeed contribute to motion perception.     

How does insect visitation trigger floral colour change?

Abstract.  1. Visitation by the key pollinator, Bombus terrestris , was implicated in inducible flower colour change in Lupinus pilosus . Behaviour at the flower and rate of visitation by these bumble bees had specific effects; exclusion of this flower visitor led to retarded onset, and reduced rate, of colour change.
2. The foraging behaviour of B. terrestris was influenced by floral colour change in L. pilosus . Choice of pre-change flowers was greater than random in relation to the proportion of colour phases available within the plant population.
3. Levels of floral manipulation that mimicked the flower handling characteristics of visiting bumble bees confirmed that triggering of the pollen release mechanism is necessary for the instigation of colour change.
4. Moreover, this study suggests that, in L. pilosus , an aspect of pollination (pollen deposition by bees and/or subsequent pollen tube growth within the style) is linked with colour change and may act as the trigger for such change.     

Is colour polymorphism advantageous to populations and species?

I am writing in response to an article by Bolton, Rollins and Griffith (2015) entitled ‘The danger within: the role of genetic, behavioural and ecological factors in population persistence of colour polymorphic species’ that was recently published as an Opinion under the NEWS AND VIEWS section in Molecular Ecology. Bolton et al. (Molecular Ecology, 2015, 24 , 2907) argue that colour polymorphism may reduce population fitness and increase extinction risk and emphasize that this is contrary to predictions put forward by Forsman et al. (Ecology, 89 , 2008, 34) and Wennersten & Forsman (Biological Reviews 87 , 2012, 756) that the existence of multiple colour morphs with co‐adapted gene complexes and associated trait values may increase the ecological and evolutionary success of polymorphic populations and species. Bolton et al. (Molecular Ecology, 2015, 24 , 2907) further state that there is no clear evidence from studies of ‘true polymorphic species’ that polymorphism promotes population persistence. In response, I (i) challenge their classifications of polymorphisms and revisit the traditional definitions recognizing the dynamic nature of polymorphisms, (ii) review empirical studies that have examined whether and how polymorphism is associated with extinction risk, (iii) discuss the roles of trait correlations between colour pattern and other phenotypic dimensions for population fitness and (iv) highlight that the causes and mechanisms that influence the composition and maintenance of polymorphisms are different from the consequences of the polymorphic condition and how it may impact on aspects of ecological success and long‐term persistence of populations and species.     

Does colour polymorphism enhance survival of prey populations?

That colour polymorphism may protect prey populations from predation is an old but rarely tested hypothesis. We examine whether colour polymorphic populations of prey exposed to avian predators in an ecologically valid visual context were exposed to increased extinction risk compared with monomorphic populations. We made 2976 artificial pastry prey, resembling Lepidoptera larvae, in four different colours and presented them in 124 monomorphic and 124 tetramorphic populations on tree trunks and branches such that they would be exposed to predation by free-living birds, and monitored their ‘survival’. Among monomorphic populations, there was a significant effect of prey coloration on survival, confirming that coloration influenced susceptibility to visually oriented predators. Survival of polymorphic populations was inferior to that of monomorphic green populations, but did not differ significantly from monomorphic brown, yellow or red populations. Differences in survival within polymorphic populations paralleled those seen among monomorphic populations; the red morph most frequently went extinct first and the green morph most frequently survived the longest. Our findings do not support the traditional protective polymorphism hypothesis and are in conflict with those of earlier studies. As a possible explanation to our findings, we offer a competing ‘giveaway cue’ hypothesis: that polymorphic populations may include one morph that attracts the attention of predators and that polymorphic populations therefore may suffer increased predation compared with some monomorphic populations.     

Does genome size in Dasypyrum villosum vary with fruit colour?

Dasypyrum villosum (2n=14), a Mediterranean grass species of the Triticeae, exhibits intraindividual fruit colour polymorphism from pale yellow to almost black. Several studies have reported differences between the plants emerging from pale and dark fruits. They include histone content in root meristem nuclei, cell cycle duration, heterochromatin banding pattern, frequency of a tandemly repeated sequence, and nuclear genome size. In the present study, we examine whether the reports of genome size being up to 1.24-fold larger in seedlings from the lighter caryopses are reproducible. In all, 29 accessions from various countries, totaling 186 plants, were investigated for genome size using flow cytometry with propidium iodide as the DNA stain. Individuals differed 1.12-fold at most and accessions 1.07-fold. The mean genome size (1C-value) was 5.07 pg or 4954 Mbp. Within-accession comparisons of seedlings derived from light and dark caryopses were insignificant (P>0.100). Thus, we found no evidence for a modificatory genome size plasticity in D. villosum. In the light of our data, the previously reported genome size variation, up to 1.66-fold within populations and 1.67-fold between populations, appears unrealistically high. Suboptimal technical procedures for quantitative Feulgen staining are probably responsible for these earlier observations.     

Does leg-ring colour affect song tutor choice in zebra finches?

Young male zebra finches, Taeniopygia guttata, reared by their mothers alone showed no preference between males with red and with light-green colour rings in their choice of song tutor. Behavioural observations showed that the tutee associated more with the adult from which it was subsequently found to have learnt. In a second experiment, birds reared by both parents wearing either light-blue or light-green colour rings and then given a choice of tutors wearing these ring combinations also showed no preference between them. These young males did, however, more often approach the tutor ringed as their parents had been. This may explain why they did not show more interest in the tutor whose song they learnt. The majority of the tutors were used twice, with the ring colour swapped before they were used the second time. There was a strong tendency for the same male to be copied by the two young birds exposed to him. This could not be attributed to a difference in song rate between the two tutors. Further work will be required to discover the basis of that individual's greater attractiveness. Copyright 1999 The Association for the Study of Animal Behaviour.     

Do group dynamics affect colour morph clines during a range shift?

Species exhibiting colour polymorphism are thought to have an ecological advantage at the landscape scale, because spatial segregation of alternatively adapted ecotypes into diverse habitats can increase the species' niche breadth and thus confer greater geographic range size. However, morph frequencies are also influenced by intrapopulational processes such as frequency‐ or density‐dependent social interactions. To identify how social feedback may affect clinal variation in morph frequencies, we investigated reciprocal interactions between morph‐specific thermal tolerance, local climatic conditions and social environments, in the context of a colour‐morph frequency cline associated with a recent range expansion in blue‐tailed damselflies (Ischnura elegans) in Sweden. Cold tolerances of gynochromes (female‐like female morph) were positively correlated with local gynochrome frequencies, suggesting a positive frequency‐dependent fitness benefit. In contrast, androchrome (male‐mimic female morph) cold tolerances were improved following recent exposure to cold weather, suggesting a beneficial environmental acclimation effect. Thus, according to an environment‐matching hypothesis for clinal variation, androchrome frequencies should therefore increase towards the (cooler) range limit. In contrast to this prediction, gynochrome frequencies increased at the expanding range limit, consistent with a positive frequency‐dependent social feedback that is beneficial when invading novel climates. Our results suggest that when phenotypes or fitnesses are affected by interactions with conspecifics, beneficial social effects on environmental tolerances may (i) facilitate range shifts, and (ii) reverse or counteract typical patterns of intraspecific interactions and environment‐matching clines observed in stable populations observed over broader geographic scales.     

Fruit or aposematic insect? Context-dependent colour preferences in domestic chicks.

Colours are common stimuli in signalling systems. Requirements to function well as a signal sometimes conflict between different signallers, and the same colour stimulus is used to convey completely different messages to the same receiver. Fruits and aposematic insects both use red coloration as a signal, in the former case to signal profitability and in the latter case as a warning signal. In two experiments, we investigated whether the domestic chick, an omnivorous predator, differed in its unconditioned preference or avoidance of red and green stimuli depending on whether or not the stimulus was an insect. The experiments were designed as preference tests between red and green painted prey. The prey were live insects and artificial fruits (experiment 1), and, to investigate the effect of movement, live and dead insects (experiment 2). The chicks did not show any difference in pecking preference between red and green when fruit-like stimuli were used, but when the prey were insects, green prey were strongly preferred to red prey, and prey movement did not affect this bias. Thus, young chicks may recognize prey as insects and then discriminate between different prey colorations, or one type of food may elicit an unlearned colour preference-avoidance response that is absent with another type of food.     

Sexually selected sexual selection: Can evolutionary retribution explain female ornamental colour?

By preferring mates with increasingly costly ornaments or courtship displays, females cause an escalation of male reproductive costs. Such increased costs should promote male selectivity based on fecundity‐linked female attributes, leading to female ornamentation in species with traditional sex roles. Consequently, female ornamentation should evolve more frequently in taxa where male reproduction is costly than in comparable taxa where it is cheaper. We assessed the prevalence of female ornamental colouration in two clades of viviparous cyprinodontid fish: the Goodeinae, where stringent female choice imposes male mating costs, and the Poeciliinae, whose males can circumvent female mate choice. We found that although in the Poeciliinae female ornamental colour is a correlated, but paler version of male coloration, females of the Goodeinae often display vivid ornamental colours that are distinct from those of males. Thus, male and female ornaments are not (phylo)genetically correlated in the Goodeinae. Furthermore, phylogenetic signal on male and female colour is clearly detectable in the Poeciliinae, but absent in the Goodeinae, suggesting that ornamental colour of males and females in the latter may be the consequence of selection. Given that enforceable female choice has promoted male ornaments, we propose that evolutionary retribution has promoted distinct female ornaments in the Goodeinae.     

WWW design code – a new tool for colour estimation in animal studies

Background

The colour of animals' skin, fur, feathers or cuticula has been estimated in a large number of studies. The methods used to do so are diverse, with some being costly and not available to all researchers. In a study to measure plumage colour in a bird species, a new method of creating a colour chart was developed. While colour-charts have their own limitations, these can be minimised when they have the following properties: 1) being readily available to the majority of biologists, 2) containing a large array of colours to allow accurate recording and differentiation of subtle colour differences, 3) low cost, 4) adhering to a world-wide standard, and 5) being available in both hard-copy and digital formats to allow for various analytical methods. The method described below satisfies all of these requirements.

Results

Colour charts estimated to fit the range of the species' plumage colours were created on the computer screen using web software that allowed for HTML-coding (in this case Dreamweaver?). The charts were adjusted using feathers from dead specimens until a satisfying range of darker and lighter colours were found. The resulting chart was printed out and was successfully used in the field to determine the plumage colour of hand-held birds.

Conclusion

Access to a computer and printer, and the software to enable the creation of a chart, is within the reach of the vast majority of biologists. The numbers of colours that can be generated should suit most studies, with the advantage of the method being that the chart can be individually tailored to the species under study. HTML colour coding is a worldwide standard, thus the colours used in studies can be described in the methods section of journal articles using the six-digit alphanumeric code. We believe this method is very useful as a low-tech method for future estimation of individual colour.     

Is there an intraspecific role for density-dependent colour change in the desert locust?

Attempts to uncover the adaptive significance of density-dependent colour polyphenism in the desert locust, Schistocerca gregaria (Orthoptera: Acrididae), have been unsuccessful. Desert locust juveniles can change colour as part of a phenotypically plastic response to changes in local population density known as phase polyphenism. They are typically cryptic in colour at low rearing density (solitarious phase), but become conspicuous at high density (gregarious phase). Recent evidence indicates that this colour change functions interspecifically as an aposematic signal. Other recent evidence, however, suggests that previous attempts to demonstrate an intraspecific function of gregarious coloration in mediating group interactions among locusts may have been confounded by the effects of multiple sensory cues. We reinvestigated the intraspecific function of density-dependent colour polyphenism and specifically controlled for potentially confounding olfactory and tactile cues. We found no effect of gregarious phase (yellow and black) coloration as either a gregarizing stimulus to behaviourally solitarious locusts or as a visual aggregation stimulus behaviourally to gregarious locusts. We did, however, find that nonmoving solitarious phase (green) coloration significantly increased the activity levels of behaviourally gregarious locusts. We cannot explain this result and its biological relevance remains unknown. In the absence of support for the intraspecific visual cue hypothesis, we favour an aposematic perspective on the function of density-dependent colour polyphenism in the desert locust. The aposematic perspective parsimoniously accounts for density-dependent changes in both colour and behaviour. Copyright 2000 The Association for the Study of Animal Behaviour.     

Black or white? Physiological implications of roost colour and choice in a microbat

Although roost choice in bats has been studied previously, little is known about how opposing roost colours affect the expression of torpor quantitatively. We quantified roost selection and thermoregulation in a captive Australian insectivorous bat, Nyctophilus gouldi (n=12) in winter when roosting in black and white coloured boxes using temperature-telemetry. We quantified how roost choice influences torpor expression when food was provided ad libitum or restricted in bats housed together in an outdoor aviary exposed to natural fluctuations of ambient temperature. Black box temperatures averaged 5.1 °C (maximum 7.5 °C) warmer than white boxes at their maximum daytime temperature. Bats fed ad libitum chose black boxes on most nights (92.9%) and on 100% of nights when food-restricted. All bats used torpor on all study days. However, bats fed ad libitum and roosting in black boxes used shorter torpor and spent more time normothermic/active at night than food-restricted bats and bats roosting in white boxes. Bats roosting in black boxes also rewarmed passively more often and to a higher skin temperature than those in white boxes. Our study suggests that N. gouldi fed ad libitum select warmer roosts in order to passively rewarm to a higher skin temperature and thus save energy required for active midday rewarming as well as to maintain a normothermic body temperature for longer periods at night. This study shows that colour should be considered when deploying bat boxes; black boxes are preferable for those bats that use passive rewarming, even in winter when food availability is reduced.     

Cryptosporidiosis and Cryptosporidium species in animals and humans: A thirty colour rainbow?

Parasites of the genus Cryptosporidium (Apicomplexa) cause cryptosporidiosis in humans and animals worldwide. The species names used for Cryptosporidium spp. are confusing for parasitologists and even more so for non-specialists. Here, 30 named species of the genus Cryptosporidium are reviewed and proposed as valid. Molecular and experimental evidence suggests that humans and cattle are the hosts for 14 and 13 out of 30 named species, respectively. Two, four and eight named species are considered of major, moderate and minor public health significance, respectively. There are at least nine named species that are shared between humans and cattle. The aim of this review is to outline available species information together with the most commonly used genetic markers enabling the identification of named Cryptosporidium spp. Currently, 28 of 30 named species can be identified using the complete or partial ssrRNA, serving as a retrospective ‘barcode’. Currently, the ssrRNA satisfies the implicit assumption that the reference databases used for comparison are sufficiently complete and applicable across the whole genus. However, due to unreliable annotation in public DNA repositories, the reference nucleotide entries and alignment of named Cryptosporidium spp. has been compiled. Despite its known limitations, ssrRNA remains the optimal marker for species identification.     

Interspecific variation in plumage colour among birds: species recognition or light environment?

Abstract The traditional explanation for interspecific plumage colour variation in birds is that colour differences between species are adaptations to minimize the risk of hybridization. Under this explanation, colour differences between closely related species of birds represent reproductive character displacement. An alternative explanation is that interspecific variation in plumage colour is an adaptive response to variation in light environments across habitats. Under this explanation, differences in colour between closely related species are a product of selection on signal efficiency. We use a comparative approach to examine these two hypotheses, testing the effects of sympatry and habitat use, respectively, on divergence in male plumage colour. Contrary to the prediction of the Species Isolation Hypothesis, we find no evidence that sympatric pairs of species are consistently more divergent in coloration than are allopatric pairs of species. However, in agreement with the Light Environment Hypothesis, we find significant associations between plumage coloration and habitat use. All of these results remain qualitatively unchanged irrespective of the statistical methodology used to compare reflectance spectra, the body regions used in the analyses, or the exclusion of areas of plumage not used in sexual displays. Our results suggest that, in general, interspecific variation in plumage colour among birds is more strongly influenced by the signalling environment than by the risk of hybridization.