Mottled coloration in a rainbow trout is associated with mosaicism for albinism

Within a group of rainbow trout at a commercial farm, a single individual was noted for its mottled yellow and dark skin pigmentation. This female fish was reared to sexual maturity and sublots of its eggs were crossed to rainbow trout males from golden, albino, and wild-type (dark-pigmented) strains. Development in other eggs was activated to produce diploid gynogenetic offspring. Coloration within each progeny group was scored at 10 weeks following initiation of feeding. Mottled coloration was observed in none of the progeny at this time. The phenotypes observed (palomino, albino, and/or wild type) and their proportions within progeny groups indicated that the mottled female was originally heterozygous for albinism. The fish apparently became mosaic for this trait following mutation of the wild-type allele at the albinism locus within a cell(s) early in embryonic development. Curiously, at approximately 6 months after initiation of feeding, mottled coloration became apparent in 2 fish from among 25 progeny of the cross to the golden male. No change in phenotype was noted at this time in 9 gynogenetic progeny nor in 68 progeny from the cross to the albino male. Apparently additional mutations and/or other genetic and regulatory processes affecting coloration came into play during juvenile development of these latter two fish.     

Extensive hybridization reveals multiple coloration genes underlying a complex plumage phenotype

Coloration is an important target of both natural and sexual selection. Discovering the genetic basis of colour differences can help us to understand how this visually striking phenotype evolves. Hybridizing taxa with both clear colour differences and shallow genomic divergences are unusually tractable for associating coloration phenotypes with their causal genotypes. Here, we leverage the extensive admixture between two common North American woodpeckers—yellow-shafted and red-shafted flickers—to identify the genomic bases of six distinct plumage patches involving both melanin and carotenoid pigments. Comparisons between flickers across approximately 7.25 million genome-wide SNPs show that these two forms differ at only a small proportion of the genome (mean F_ST = 0.008). Within the few highly differentiated genomic regions, we identify 368 SNPs significantly associated with four of the six plumage patches. These SNPs are linked to multiple genes known to be involved in melanin and carotenoid pigmentation. For example, a gene (CYP2J19) known to cause yellow to red colour transitions in other birds is strongly associated with the yellow versus red differences in the wing and tail feathers of these flickers. Additionally, our analyses suggest novel links between known melanin genes and carotenoid coloration. Our finding of patch-specific control of plumage coloration adds to the growing body of literature suggesting colour diversity in animals could be created through selection acting on novel combinations of coloration genes.     

Trade-off between warning signal efficacy and mating success in the wood tiger moth

The coloration of species can have multiple functions, such as predator avoidance and sexual signalling, that directly affect fitness. As selection should favour traits that positively affect fitness, the genes underlying the trait should reach fixation, thereby preventing the evolution of polymorphisms. This is particularly true for aposematic species that rely on coloration as a warning signal to advertise their unprofitability to predators. Nonetheless, there are numerous examples of aposematic species showing remarkable colour polymorphisms. We examined whether colour polymorphism in the wood tiger moth is maintained by trade-offs between different functions of coloration. In Finland, males of this species have two distinct colour morphs: white and yellow. The efficacy of the warning signal of these morphs was tested by offering them to blue tits in the laboratory. Birds hesitated significantly longer to attack yellow than white males. In a field experiment, the survival of the yellow males was also higher than white males. However, mating experiments in the laboratory revealed that yellow males had lower mating success than white males. Our results offer an explanation for the maintenance of polymorphism via trade-off between survival selection and mating success.     

Coloration,Paternity, and Assortative Mating in Western Bluebirds

Coloration in birds can act as an important sexual signal in males, yet in many species, both sexes display bright colors. Social selection may account for this pattern, with more brightly colored individuals pairing together on the best territories. Mutual mate choice may also explain this, as males investing a great deal of parental care in the offspring should be choosy about their social mates. It is less clear whether this pattern of mate choice can apply to extra‐pair partners as well. We examined western bluebirds (Sialia mexicana) to determine whether more colorful individuals tended to pair with one another, both in social pairs and between females and their extra‐pair partners. Both male and female western bluebirds display both UV‐blue structural plumage and a melanin‐based chestnut breast patch, although females are duller than males. Social pairs mated assortatively with regard to UV‐blue brightness, but not chestnut coloration. There was no evidence that extra‐pair partners mated assortatively, but males with brighter UV‐blue coloration had fewer extra‐pair offspring in their nests. Older males were more successful at siring extra‐pair offspring, despite displaying no differences in coloration compared to younger males. Coloration did not play a role in determining extra‐pair male success. These results suggest that coloration plays a role in the formation of social pairs, but not mate choice for extra‐pair partners.     

Importance of colour in the reaction of passerine predators to aposematic prey: experiments with mutants of Pyrrhocoris apterus (Heteroptera)

Persistent questions concerning the warning coloration of unpalatable insects address whether the bright aposematic colour itself or its combination with a species-specific dark pattern is the key factor in their protection against insectivorous birds, and how chromatic polymorphism originates and is maintained in aposematics. In the present study, these questions were tested experimentally, using the birds Parus major , Parus caeruleus , Erithacus rubecula , and Sylvia atricapilla as predators, and chromatically polymorphic firebug Pyrrhocoris apterus : red wild form, white, yellow, and orange mutants (all four of them with the same black melanin pattern, the mutants differing in colour of pteridine pigments only) and the nonaposematic brown-painted wild form as prey. The results show that a specific colour is essential for the birds to recognize the specific aposematic prey; the melanin pattern is not sufficient. White mutants were no better protected than nonaposematic firebugs; red wild-type and orange mutants were equally well protected against all bird species; and the reaction of birds to yellow mutants was species-specific. An evolutionary scenario of 'recurrent recessive mutations' is formulated to explain the origin of colour polymorphism in some aposematics.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 143–153.     

Aposematism and gregariousness: the combined effect of group size and coloration on signal repellence

Many aposematic species have evolved an aggregated lifestyle, and one possible advantage of grouping in warningly coloured prey is that it makes the aposematic signal more effective by generating a greater aversion in predators. Here we investigate the effect of prey group size on predator behaviour, both when prey are aposematic and when they are not aposematic, to separate the effects of warning coloration and prey novelty. Naive domestic chicks (Gallus gallus domesticus) were presented with either solitary or groups of 3, 9 or 27 live larvae of the aposematic bug Tropidothorax leucopterus. Other naive chicks were presented with larvae of the non-aposematic bug Graptostethus servus either solitary or in groups of 27. Attack probability decreased with increasing group size of aposematic prey, both when birds were naive and when they had prior experience, whereas prey gregariousness did not affect the initial attack probability on the G. servus larvae. In a separate experiment, groups of mealworms were shown to be even more attractive than solitary mealworms to naive chicks. We conclude that the aversiveness of prey grouping in this study can be explained as increased signal repellence of specific prey coloration, in this case a classical warning coloration. These experiments thus support the idea of gregariousness increasing the signalling effect of warning coloration.     

Aposematic coloration does not deter corallivory by fish on the coral <Emphasis Type="Italic">Montastraea cavernosa</Emphasis>

Predation on corals by visual predators is a significant source of partial or total mortality on coral reefs, and corals have evolved strategies, including chemical defenses, to deter predation. One mechanism that organisms use to communicate the presence of chemical defenses is aposematic coloration, or the display of bright coloration as a warning to visual predators such as fish. Corals exhibit multiple colors, and it has been hypothesized that one role for this variability in coloration is as an aposematic warning of adverse palatability. Here, we test green and orange color morphs of the Caribbean coral Montastraea cavernosa for the presence of chemical defenses and whether their differences in coloration elicited different feeding responses. While M. cavernosa is chemically defended, there is no difference in feeding deterrence between color morphs; thus, the different color morphs of this coral species do not appear to represent an example of aposematic coloration.     

Thermobiological effects of temperature‐induced color variations in Aglais urticae (Lepidoptera,Nymphalidae)

Coloration of animals is important for camouflage, for social behavior, or for physiological fitness. This study investigates the color variation in adults of Aglais urticae obtained on subjecting some pre‐imaginal stages to different temperature conditions and their thermobiological consequences. To investigate the evolutionary–ecological interactions of temperature and pigmentation in butterflies, caterpillars, and pupae of the small tortoiseshell, Aglais urticae (Lepidoptera, Nymphalidae), larvae from Central Europe and Scandinavia were reared at temperatures between 7 and 34°C in the laboratory or in the field. After emergence, the intensity of pigmentation of the imagines and their increase in body temperature under defined full‐spectrum light irradiation were quantified by image analysis and thermal imaging. At constant conditions, ambient rearing temperature and pigmentation intensity of imagines were negatively and linearly correlated in Central European butterflies, regardless of whether the pupal stage alone or, additionally, the last period of the larval stage was exposed to these conditions: low temperatures induced darker coloration and high temperatures led to lighter individuals. A thermal pulse of a few days alone at the beginning of pupal dormancy led to a similar, albeit weakened, effect. Caterpillars of the Scandinavian subspecies A. urticae polaris, whose pupal dormancy took place under Central European field conditions, developed into strongly pigmented imagines. The thermobiological relevance of more intense pigmentation was shown by significantly higher absorption of light, and thus stronger increased body temperature after 5 min of defined illumination, but this difference ceased after 15 min. Our results show that phenotypic plasticity in wing coloration is adaptive since temperature‐induced developmental changes provide thermobiological benefit in adult butterflies. We propose that, in subpolar latitudes, darker coloration likely has a selection advantage favoring individuals with reaction norms gradually shifted to stronger pigmented phenotypes, possibly leading to the establishment of a pigmentation cline.     

The effects of predator learning, forgetting, and recognition errors on the evolution of warning coloration

This paper demonstrates that the specifics of predator avoidance learning, information loss, and recognition errors may heavily influence the evolution of aposematism. I establish a mathematical model of the change in frequency over time of bright individuals of a distasteful prey species. Warning color spreads through green beard selection as reformulated by Guilford (1990); bright colored forms gain an advantage due to their phenotypic resemblance to other bright forms, which have been sampled by the predator. I use a general classical conditioning model to examine gradual predator learning and forgetting, and then consider the extreme of one-trial learning and no forgetting over time that may occur with very toxic prey. The advantage of conspicuous coloration under these latter conditions depends upon its role in lowering a constant probability of the prey being misidentified and thus mistakenly attacked by a predator, a rarely emphasized factor in the evolution of warning coloration. This constant probability of mistaken attacks can also be interpreted as a constant probability that forgetting has occurred (forgetting does not increase with time) or a periodic decision by the predator to resample avoided prey. I show that when predators learn and forget gradually, as under the general classical conditioning model, it is very difficult for aposematic coloration to become established unless bright individuals cross an often high threshold frequency through chance factors. In contrast, the conditions expected with highly toxic prey promote the evolution of warning coloration more easily, by means from the fixation of very bright mutations to the fixation of successive mutations each of which causes a small increase in a prey's conspicuousness. The results therefore predict that aposematic coloration may have evolved in a different manner in different predator and prey systems. They also suggest that it may be extremely difficult for warning coloration to evolve in more mildly toxic or distasteful prey outside of a mimicry system.     

Increased predation of nutrient-enriched aposematic prey

Avian predators readily learn to associate the warning coloration of aposematic prey with the toxic effects of ingesting them, but they do not necessarily exclude aposematic prey from their diets. By eating aposematic prey ‘educated’ predators are thought to be trading-off the benefits of gaining nutrients with the costs of eating toxins. However, while we know that the toxin content of aposematic prey affects the foraging decisions made by avian predators, the extent to which the nutritional content of toxic prey affects predators'' decisions to eat them remains to be tested. Here, we show that European starlings (Sturnus vulgaris) increase their intake of a toxic prey type when the nutritional content is artificially increased, and decrease their intake when nutritional enrichment is ceased. This clearly demonstrates that birds can detect the nutritional content of toxic prey by post-ingestive feedback, and use this information in their foraging decisions, raising new perspectives on the evolution of prey defences. Nutritional differences between individuals could result in equally toxic prey being unequally predated, and might explain why some species undergo ontogenetic shifts in defence strategies. Furthermore, the nutritional value of prey will likely have a significant impact on the evolutionary dynamics of mimicry systems.     

Ontogenetic colour change and the evolution of aposematism: a case study in panic moth caterpillars

1. Aposematism is a widely used antipredator strategy in which an organism possesses both warning coloration and unprofitable characters. Theoretical evidence suggests that aposematic colour should develop when high opportunity costs imposed by crypsis force an organism to engage in conspicuous behaviours. Hence, it is expected that ontogenetic colour change (OCC) in larval insects should include aposematism when foraging needs compel behavioural modifications that preclude a continued state of crypsis. 2. To test this idea, I first investigated whether OCC in caterpillars of the panic moth Saucrobotys futilalis was indicative of a switch from cryptic to aposematic coloration. I then examined the context of panic moth OCC as it related to foraging patterns and behavioural conspicuousness. 3. Early Saucrobotys instars are a cryptic green, but later instars become progressively more orange and develop black spots. Early instar larvae forage cryptically on the inner parenchyma of silked-together host plant leaves to avoid predation, but are rapidly forced to engage in conspicuous foraging behaviours as they outgrow the resources afforded by their shelters. Both coloration and behaviour reach maximal conspicuousness in final instar larvae. 4. As predicted, OCC encompassed a change from crypsis to aposematism in Saucrobotys. Aposematic function was demonstrated by changes in both antipredator behaviour patterns and effectiveness of predator deterrence in early and late instars. Moreover, increased opportunity costs of crypsis and behavioural conspicuousness coincided with the onset of aposematic coloration. 5. This pattern of OCC suggests that aposematic coloration in Saucrobotys develops as a response to constraints imposed by crypsis. Moreover, my study illustrates the importance of the study of ontogenetic patterns in determining how behaviour, morphology, and predator responses interact to influence the initial evolution of phenomena such as aposematism.     

A Potential Benefit of Albinism in Astyanax Cavefish: Downregulation of the oca2 Gene Increases Tyrosine and Catecholamine Levels as an Alternative to Melanin Synthesis

Albinism, the loss of melanin pigmentation, has evolved in a diverse variety of cave animals but the responsible evolutionary mechanisms are unknown. In Astyanax mexicanus, which has a pigmented surface dwelling form (surface fish) and several albino cave-dwelling forms (cavefish), albinism is caused by loss of function mutations in the oca2 gene, which operates during the first step of the melanin synthesis pathway. In addition to albinism, cavefish have evolved differences in behavior, including feeding and sleep, which are under the control of the catecholamine system. The catecholamine and melanin synthesis pathways diverge after beginning with the same substrate, L-tyrosine. Here we describe a novel relationship between the catecholamine and melanin synthesis pathways in Astyanax. Our results show significant increases in L-tyrosine, dopamine, and norepinephrine in pre-feeding larvae and adult brains of Pachón cavefish relative to surface fish. In addition, norepinephrine is elevated in cavefish adult kidneys, which contain the teleost homologs of catecholamine synthesizing adrenal cells. We further show that the oca2 gene is expressed during surface fish development but is downregulated in cavefish embryos. A key finding is that knockdown of oca2 expression in surface fish embryos delays the development of pigmented melanophores and simultaneously increases L-tyrosine and dopamine. We conclude that a potential evolutionary benefit of albinism in Astyanax cavefish may be to provide surplus L-tyrosine as a precursor for the elevated catecholamine synthesis pathway, which could be important for adaptation to the challenging cave environment.     

Avoidance of aposematic prey in European tits (Paridae): learned or innate?

Predators may either learn to avoid aposematic prey or may avoidit because of an innate bias. Learned as well as innate avoidancehas been observed in birds, but the existing evidence is basedon experiments with rather few unrelated model species. We comparedthe origin of avoidance in European species of tits (Paridae).First, we tested whether wild-caught birds (blue tits, greattits, crested tits, coal tits, willow tits, and marsh tits)avoid aposematic (red and black) adult firebugs Pyrrhocorisapterus (Heteroptera) more than nonaposematic (brown painted)ones. Larger proportion of birds avoided aposematic than brown-paintedfirebugs in majority of species (except coal tits). Second,we tested whether naive hand-reared birds of 4 species (bluetits, great tits, crested tits, and coal tits) attack or avoidaposematic and nonaposematic firebugs, both novel for them.Behavior of the naive blue tits and coal tits was similar tothat of the wild-caught birds; majority of them did not attackthe firebugs. Contrastingly, the naive great tits and crestedtits behaved differently than the wild-caught conspecific adults;majority of the wild-caught birds avoided the aposematic firebugs,whereas the naive birds usually did not show any initial avoidanceand had to learn to avoid the aposematic prey. Our results showthat the origin of avoidance may be different even in closelyrelated species. Because blue tits and coal tits avoided notonly aposematic firebugs but also their brown-painted form,we interpret their behavior as innate neophobia rather thaninnate bias against the warning coloration.     

Environmental correlates of internal coloration in frogs vary throughout space and lineages

Internal organs of ectotherms have melanin‐containing cells that confer different degrees of coloration to them. Previous experimental studies analyzed their developmental origin, role in immunity, and hormonal regulation. For example, melanin increases with ultraviolet radiation (UV) and temperature in frogs and fish. However, little is known about how environmental variables influence the amount of coloration on organs among amphibian species over a large spatial extent. Here, we tested how climatic variables (temperature, UV, and photoperiod) influence the coloration of internal organs of anurans. We recorded the level of melanin pigmentation using four categories on 12 internal organs and structures of 388 specimens from 43 species belonging to six anuran families. Then, we tested which climatic variables had the highest covariation with the pigmentation on each organ after controlling for spatial autocorrelation in climatic variables and phylogenetic signal in organ coloration using the extended version of the RLQ ordination. Coloration in all organs was correlated with the phylogeny. However, the coloration of different organs was affected by different variables. Specifically, the coloration of the heart, kidneys, and rectum of hylids, Rhinella schneideri, some Leptodactylus, and Proceratophrys strongly covaried with temperature and photoperiod, whereas that of the testicle, lumbar parietal peritoneum, lungs, and mesenterium of Leiuperinae, Hylodidae, Adenomera, and most Leptodactylus had highest covariation with UV‐B and temperature. Our results support the notion that melanin pigmentation on the surface of organs of amphibians has an adaptive function conferred by the protective functions of the pigment. But most importantly, internal melanin seems to respond differently to climatic variables depending on the lineage and locality in which species occur.     

Caterpillars of Eumaeus childrenae (Lepidoptera: Lycaenidae) feeding on two species of cycads (Zamiaceae) in the Huasteca region, Mexico

There are few genera of butterflies that feed on cycads. Among them the genus Eumaeus (Lycaenidae) presents aposematic coloration in all its life stages. In this work we report for the first time the herbivory of young leaflets of Ceratozamia mexicana and Zamia fischeri (Zamiaceae) by caterpillars of E. childrenae in their natural habitat in the Huasteca region, Mexico.     

Diversity in warning coloration: selective paradox or the norm?

Aposematic theory has historically predicted that predators should select for warning signals to converge on a single form, as a result of frequency‐dependent learning. However, widespread variation in warning signals is observed across closely related species, populations and, most problematically for evolutionary biologists, among individuals in the same population. Recent research has yielded an increased awareness of this diversity, challenging the paradigm of signal monomorphy in aposematic animals. Here we provide a comprehensive synthesis of these disparate lines of investigation, identifying within them three broad classes of explanation for variation in aposematic warning signals: genetic mechanisms, differences among predators and predator behaviour, and alternative selection pressures upon the signal. The mechanisms producing warning coloration are also important. Detailed studies of the genetic basis of warning signals in some species, most notably Heliconius butterflies, are beginning to shed light on the genetic architecture facilitating or limiting key processes such as the evolution and maintenance of polymorphisms, hybridisation, and speciation. Work on predator behaviour is changing our perception of the predator community as a single homogenous selective agent, emphasising the dynamic nature of predator–prey interactions. Predator variability in a range of factors (e.g. perceptual abilities, tolerance to chemical defences, and individual motivation), suggests that the role of predators is more complicated than previously appreciated. With complex selection regimes at work, polytypisms and polymorphisms may even occur in Müllerian mimicry systems. Meanwhile, phenotypes are often multifunctional, and thus subject to additional biotic and abiotic selection pressures. Some of these selective pressures, primarily sexual selection and thermoregulation, have received considerable attention, while others, such as disease risk and parental effects, offer promising avenues to explore. As well as reviewing the existing evidence from both empirical studies and theoretical modelling, we highlight hypotheses that could benefit from further investigation in aposematic species. Finally by collating known instances of variation in warning signals, we provide a valuable resource for understanding the taxonomic spread of diversity in aposematic signalling and with which to direct future research. A greater appreciation of the extent of variation in aposematic species, and of the selective pressures and constraints which contribute to this once‐paradoxical phenomenon, yields a new perspective for the field of aposematic signalling.     

Brighter-colored paper wasps (Polistes dominula) have larger poison glands

ABSTRACT: INTRODUCTION: Aposematism is a defense system against predators consisting of the toxicity warning using conspicuous coloration. If the toxin production and aposematic coloration is costly, only individuals in good physical condition can simultaneously produce abundant poison and striking coloration. In such cases, the aposematic coloration not only indicates that the animal is toxic, but also the toxicity level of individuals. The costs associated to the production of aposematic coloration would ensure that individuals indicate honestly their toxicity levels. In the present study, we examine the hypothesis that a positive correlation exists between the brightness of warning coloration and toxicity level using as a model the paper wasp (Polistes dominula). RESULTS: We collected wasps from 30 different nests and photographed them to measure the brightness of warning coloration in the abdomen. We also measured the volume of the poison gland, as well as the length, and the width of the abdomen. The results show a positive relationship between brightness and poison-gland size, which remained positive even after controlling the body size and abdomen width. CONCLUSION: The results suggest that the coloration pattern of these wasps is a true sign of toxicity level: wasps with brighter colors are more poisonous (they have larger poison glands).     

Numbers,neighbors, and hungry predators: What makes chemically defended aposematic prey susceptible to predation?

Many chemically defended aposematic species are characterized by relatively low toxin levels, which enables predators to include them in their diets under certain circumstances. Knowledge of the conditions governing the survival of such prey animals—especially in the context of the co‐occurrence of similar but undefended prey, which may result in mimicry‐like interactions—is crucial for understanding the initial evolution of aposematism. In a one‐month outdoor experiment using fish (the common carp Cyprinus carpio) as predators, we examined the survival of moderately defended aposematic tadpole prey (the European common toad Bufo bufo) with varying absolute densities in single‐species prey systems or varying relative densities in two‐species prey systems containing morphologically similar but undefended prey (the European common frog Rana temporaria). The density effects were investigated in conjunction with the hunger levels of the predator, which were manipulated by means of the addition of alternative (nontadpole) food. The survival of the B. bufo tadpoles was promoted by increasing their absolute density in the single‐species prey systems, increasing their relative density in the two‐species prey systems, and providing ample alternative food for the predator. Hungry predators eliminated all R. temporaria individuals regardless of their proportion in the prey community; in treatments with ample alternative food, high relative B. bufo density supported R. temporaria survival. The results demonstrated that moderately defended prey did benefit from high population densities (both absolute and relative), even under long‐term predation pressure. However, the physiological state of the predator was a crucial factor in the survival of moderately defended prey. While the availability of alternative prey in general should promote the spread and maintenance of aposematism, the results indicated that the resemblance between the co‐occurring defended and undefended prey may impose mortality costs on the defended model species, even in the absence of actual mimicry.     

Inversely related aposematic traits: reduced conspicuousness evolves with increased toxicity in a polymorphic poison-dart frog

Prevailing theory contends that aposematic coloration evolves in tandem with toxicity so that the evolution of increased toxicity will accompany the evolution of greater conspicuousness. Although variation in aposematic coloration within single species should be selectively constrained, because individuals varying from a predator-recognized warning signal will incur greater risk of predation, several species of poison-dart frogs display remarkable phenotypic variation. This variation may have evolved to match different levels of toxicity, and these species provide excellent opportunities to examine the evolution of aposematic coloration. Here, I test whether increased conspicuousness in the granular poison-dart frog evolved in tandem with increased toxicity. Contrary to classical predictions, toxicity assays, spectral reflectance measurements, and phylogenetic reconstruction reveal that the less conspicuous color morphs are actually significantly more toxic than the brightest, most conspicuous phenotypes and that the more toxic, less-conspicuous form evolved from a less toxic, more conspicuous ancestor. Through gas chromatography--mass spectrometry analysis of toxin profiles, I traced the increase in toxicity in the less-conspicuous populations to an acquisition of specific alkaloids, some of which are proven convulsants. These results challenge the tenet that increased conspicuousness always evolves with increased toxicity and support the idea that once aposematism has been established in a species, phenotypic variation may evolve from brightness and toxicity becoming decoupled.