The niche variation hypothesis and the evolution of colour polymorphism in birds: a comparative study of owls, nightjars and raptors

We studied the evolution of colour polymorphism in diurnal raptors, owls and nightjars, the avian taxa in which this trait is most widespread, in relation to species ecological niche width and diet. Two main mechanisms have been put forward to explain the maintenance of polymorphism, namely apostatic selection and disruptive selection. The niche variation hypothesis states that species with broader ecological niches should be more variable compared with those with narrow niches because of the action of disruptive selection; the apostatic selection hypothesis conversely suggests that intraspecific colour variation should be promoted in predators by prey forming an avoidance image for the more common colour morph. Our aim was to determine if colour polymorphism occurrence was associated with broad ecological niches as predicted by the niche variation hypothesis, or with predation on intelligent and sharp‐sighted prey as predicted by the avoidance image hypothesis. Pairwise comparisons were made between pairs of closely related species differing in variables expected to influence the occurrence of polymorphism. We found that polymorphic species of all three groups showed wider and more continuous distribution ranges, frequented many different habitats, both open and closed, and lived in seasonally alternating dry/wet climates. Polymorphic species were more migratory compared with monomorphic ones, and they showed an activity pattern covering both day and night. Conversely, colour polymorphism was not higher in species preying on birds and mammals. All these findings support the hypothesis that colour polymorphism evolved in bird species with wider niche breadth and not in species preying on intelligent prey. Therefore, we propose that disruptive selection may be the main mechanism maintaining colour polymorphism in these bird groups by favouring different morphs in different environmental conditions. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82 , 237–248.     

Predator-prey relationships and the evolution of colour polymorphism: a comparative analysis in diurnal raptors

Genetically based variation in coloration occurs in populations of many organisms belonging to various taxa, including birds, mammals, frogs, molluscs, insects and plants. Colour polymorphism has evolved in raptors more often than in any other group of birds, suggesting that predator–prey relationships was a driving evolutionary force. Individuals displaying a new invading colour morph may enjoy an initial foraging advantage because prey have difficulties in learning the colour of a rare morph (apostatic selection), or because morphs provide alternative foraging benefits allowing differently coloured individuals to exploit distinct food niches (disruptive selection). Plumage polymorphism should therefore have evolved in species that prey upon animals having the physiological ability to distinguish between differently coloured predators but also to flee once a predator has been detected. From this assumption, we can predict that closely related polymorphic and monomorphic species prey upon different animals. They may also differ in morphology, because foraging upon different prey may require different foraging modes, and in turn different morphological structures. We tested these two predictions in a comparative study of raptors. As expected, polymorphic and monomorphic species had a different diet, and there was a difference in wing length between polymorphic and monomorphic species within two genera ( Buteo and Accipiter ). Across all raptors for which phylogenetic relationships are known, polymorphic species preyed more often upon mammals than did monomorphic ones. These two types of raptor did not differ in the frequency of birds, insects and reptiles in their diets. We discuss these results in the light of the hypothesis that predator–prey relationships played a role in the evolution of colour polymorphism. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 565–578.     

Foraging differences between white and dark morphs of the Pacific Reef Heron Egretta sacra

Among the species of diurnal herons (Ardeinae) showing light-dark colour polymorphism in plumage, colour phase is age-related in one species, closely associated with geography in three species, and found in most populations in three closely related species of reef herons. In Pacific Reef Herons Egretta sacra white-phased birds sought prey by a flight, land, and freeze hunting style in breaking surf, while dark birds pursued prey by actively walking or running on reef flats. On Mangaia, in the southern Cook Islands, more white-phased birds used the windward side of the island and more dark-phased birds used the lee side. On Rarotonga, 204 km from Mangaia, reef herons foraged almost exclusively in shaded streams and no entirely white-phased bird was encountered. These results provide the first evidence of differences in hunting techniques associated with colour morph and only the second observation of differences in habitat use by white- and dark-phased herons at single localities. As such they support Murton's (1971) idea that colour polymorphism serves herons in their role as predators. For reasons discussed in the text such differences are more expected in reef herons than in most other colour-polymorphic herons.     

Red dominates black: agonistic signalling among head morphs in the colour polymorphic Gouldian finch

Recent sexual selection studies on the evolution of bird colouration have mainly focused on signals with a high level of condition-dependent variation, with much less attention given to colour traits whose expression is genetically controlled. Here, we experimentally tested the relative importance of a genetic colour polymorphism in determining male dominance in the Gouldian finch (Erythrura gouldiae), a species displaying three completely discrete but naturally co-occurring genetically inherited phenotypes; yellow-, red- (carotenoid) and black-headed (melanin) morphs. First, in staged dominance contests between unfamiliar birds of different head morphs, red-headed males dominated black-headed males, both of which dominated the yellow-headed birds. Second, within morphs, the intensity and size of the strongly ultraviolet-blue collar determined the outcome of these contests, and among the red-headed males, redder males dominated less chromatic birds. Lastly, when the dominance signal of red-headed birds was experimentally destabilized (i.e. blackened or reddened), naturally red-headed morphs continued to dominate both the black-and yellow-headed morphs. Together, these results suggest that intrinsic dominance-related behavioural differences between the three colour morphs, which are likely to influence the relative fitness of each morph, contribute to the complex selective patterns maintaining these three discrete phenotypes in relatively stable frequencies in wild populations.     

Beyond morphs: Inter-individual colour variation despite strong genetic determinism of colour morphs in a wild bird

Categorizing individuals into discrete forms in colour polymorphic species can overlook more subtle patterns in coloration that can be of functional significance. Thus, quantifying inter-individual variation in these species at both within- and between-morph levels is critical to understand the evolution of colour polymorphisms. Here we present analyses of inter-individual colour variation in the Reunion grey white-eye (Zosterops borbonicus), a colour polymorphic wild bird endemic to the island of Reunion in which all highland populations contain two sympatric colour morphs, with birds showing predominantly grey or brown plumage, respectively. We first quantified colour variation across multiple body areas by using a continuous plumage colour score to assess variation in brown-grey coloration as well as smaller scale variation in light patches. To examine the possible causes of among-individual variation, we tested if colour variation in plumage component elements could be explained by genotypes at two markers near a major-effect locus previously related to back coloration in this species, and by other factors such as age, sex and body condition. Overall, grey-brown coloration was largely determined by genetic factors and was best described by three distinct clusters that were associated to genotypic classes (homozygotes and heterozygote), with no effect of age or sex, whereas variation in smaller light patches was primarily related to age and sex. Our results highlight the importance of characterizing subtle plumage variation beyond morph categories that are readily observable since multiple patterns of colour variation may be driven by different mechanisms, have different functions and will likely respond in different ways to selection.     

Colour pattern as a single trait driving speciation in Hypoplectrus coral reef fishes?

Theory shows that speciation in the presence of gene flow occurs only under narrow conditions. One of the most favourable scenarios for speciation with gene flow is established when a single trait is both under disruptive natural selection and used to cue assortative mating. Here, we demonstrate the potential for a single trait, colour pattern, to drive incipient speciation in the genus Hypoplectrus (Serranidae), coral reef fishes known for their striking colour polymorphism. We provide data demonstrating that sympatric Hypoplectrus colour morphs mate assortatively and are genetically distinct. Furthermore, we identify ecological conditions conducive to disruptive selection on colour pattern by presenting behavioural evidence of aggressive mimicry, whereby predatory Hypoplectrus colour morphs mimic the colour patterns of non-predatory reef fish species to increase their success approaching and attacking prey. We propose that colour-based assortative mating, combined with disruptive selection on colour pattern, is driving speciation in Hypoplectrus coral reef fishes.     

Signal convergence in fruits: a result of selection by frugivores?

The Dispersal Syndrome hypothesis remains contentious, stating that apparently nonrandom associations of fruit characteristics result from selection by seed dispersers. We examine a key assumption under this hypothesis, i.e. that fruit traits can be used as reliable signals by frugivores. We first test this assumption by looking at whether fruit colour allows birds and primates to distinguish between fruits commonly dispersed by birds or primates. Second, we test whether the colours of fruits dispersed by primates are more contrasting to primates than the colours of bird‐dispersed fruits, expected if fruit colour is an adaptation to facilitate the detection by seed dispersers. Third, we test whether fruit colour has converged in unrelated plant species dispersed by similar frugivores. We use vision models based on peak sensitivities of birds’ and primates’ cone cells. We base our analyses on the visual systems of two types of birds (violet and ultraviolet based) and three types of primates (trichromatic primates from the Old and the New Worlds, and a dichromatic New World monkey). Using a Discriminant Function Analysis, we find that all frugivore groups can reliably discriminate between bird‐ and primate‐dispersed fruits. Fruit colour can be a reliable signal to different seed dispersers. However, the colours of primate‐dispersed fruits are less contrasting to primates than those of bird‐dispersed fruits. Fruit colour convergence in unrelated plants is independent of phylogeny and can be better explained by disperser type, which supports the hypothesis that frugivores are important in fruit evolution. We discuss adaptive and nonadaptive hypotheses that can potentially explain the pattern we found.     

Differential foraging success across a light level spectrum explains the maintenance and spatial structure of colour morphs in a polymorphic bird

Detectability of different colour morphs under varying light conditions has been proposed as an important driver in the maintenance of colour polymorphism via disruptive selection. To date, no studies have tested whether different morphs have selective advantages under differing light conditions. We tested this hypothesis in the black sparrowhawk, a polymorphic raptor exhibiting a discrete white and dark morph, and found that prey provisioning rates differ between the morphs depending on light condition. Dark morphs delivered more prey in lower light conditions, while white morphs provided more prey in brighter conditions. We found support for the role of breeding season light level in explaining the clinal pattern of variation in morph ratio across the species range throughout South Africa. Our results provide the first empirical evidence supporting the hypothesis that polymorphism in a species, and the spatial structuring of morphs across its distribution, may be driven by differential selective advantage via improved crypsis, under varying light conditions.     

Hoverflies are imperfect mimics of wasp colouration

Many Batesian mimics are considered to be inaccurate copies of their models, including a number of hoverfly species which appear to be poor mimics of bees and wasps. This inaccuracy is surprising since more similar mimics are expected to deceive predators more frequently and therefore have greater survival. One suggested explanation is that mimics which appear inaccurate to human eyes may be perceived differently by birds, the probable agents of selection. For example, if patterns contain an ultra-violet (UV) component, this would be visible to birds but overlooked by humans. So far, indirect comparisons have been made using human and bird responses to mimetic stimuli, but direct colour measurements of mimetic hoverflies are lacking. We took spectral readings from a wide range of hoverfly and wasp patterns. They show very low reflectance in the UV range, and do not display any human-invisible colour boundaries. We modelled how the recorded spectra would be perceived by both birds and humans. While colour differences between wasps and hoverflies are slightly more distinct according to human visual abilities, bird vision is capable of discriminating the two taxa in almost all cases. We discuss a number of factors that might make the discrimination task more challenging for a predator in the field, which could explain the apparent lack of selection for accurate colour mimicry.     

The evolution of plumage polymorphism in birds of prey and owls: the apostatic selection hypothesis revisited

Co-evolution between phenotypic variation and other traits is of paramount importance for our understanding of the origin and maintenance of polymorphism in natural populations. We tested whether the evolution of plumage polymorphism in birds of prey and owls was supported by the apostatic selection hypothesis using ecological and life-history variables in birds of prey and owls and performing both cross taxa and independent contrast analyses. For both bird groups, we did not find any support for the apostatic selection hypothesis being the maintaining factor for the polymorphism: plumage polymorphism was not more common in taxa hunting avian or mammalian prey, nor in migratory species. In contrast, we found that polymorphism was related to variables such as sexual plumage dimorphism, population size and range size, as well as breeding altitude and breeding latitude. These results imply that the most likely evolutionary correlate of polymorphism in both bird groups is population size, different plumage morphs might simply arise in larger populations most likely because of a higher probability of mutations and then be maintained by sexual selection.     

Color polymorphism and sex ratio distortion in a cichlid fish as an incipient stage in sympatric speciation by sexual selection

We investigated a Lake Victoria cichlid with a complex colour polymorphism that apparently represents one original species and two incipient species, all of which are sympatric. In laboratory breeding experiments we observed sex ratio distortion in certain matings between original and incipient species. Mate choice experiments show that males of the incipient species exhibit mating preferences against the original species, and males and females of the original species exhibit strong mating preferences against the incipient species. Mating preferences might evolve by sex ratio selection to avoid matings with distorted progeny sex ratios. Phenotype frequencies in nature suggest that mating preferences translate into mating frequencies, thus restricting gene flow and exerting disruptive sexual selection between the original and incipient species. The incipient species do not differ in morphology or ecology from the original species, implying that colour polymorphism, associated with sex ratio distortion, can be an incipient stage in sympatric speciation, and that disruption of gene flow can precede ecological differentiation.     

鸟类羽色多态现象：概念及其进化机制假说

多态现象对了解物种的遗传、变异和进化有着重要意义,鸟类羽色多态现象的进化机制,是多态现象研究中非常重要的内容。鸟类羽色多态现象的进化机制假说主要有：分化选择假说、异类选择假说和非随机性交配假说等。本文对鸟类羽色多态现象的概念和以上进化机制假说进行了综述,并针对鸟类羽色多态现象进化机制研究中存在争议的问题及研究的不足提出了自己的看法。     

Cryptic differences in colour among Müllerian mimics: how can the visual capacities of predators and prey shape the evolution of wing colours?

Antagonistic interactions between predators and prey often lead to co‐evolution. In the case of toxic prey, aposematic colours act as warning signals for predators and play a protective role. Evolutionary convergence in colour patterns among toxic prey evolves due to positive density‐dependent selection and the benefits of mutual resemblance in spreading the mortality cost of educating predators over a larger prey assemblage. Comimetic species evolve highly similar colour patterns, but such convergence may interfere with intraspecific signalling and recognition in the prey community, especially for species involved in polymorphic mimicry. Using spectrophotometry measures, we investigated the variation in wing coloration among comimetic butterflies from distantly related lineages. We focused on seven morphs of the polymorphic species Heliconius numata and the seven corresponding comimetic species from the genus Melinaea. Significant differences in the yellow, orange and black patches of the wing were detected between genera. Perceptions of these cryptic differences by bird and butterfly observers were then estimated using models of animal vision based on physiological data. Our results showed that the most strikingly perceived differences were obtained for the contrast of yellow against a black background. The capacity to discriminate between comimetic genera based on this colour contrast was also evaluated to be higher for butterflies than for birds, suggesting that this variation in colour, likely undetectable to birds, might be used by butterflies for distinguishing mating partners without losing the benefits of mimicry. The evolution of wing colour in mimetic butterflies might thus be shaped by the opposite selective pressures exerted by predation and species recognition.     

Exploring the adjustment to parasite pressure hypothesis: differences in uropygial gland volume and haemosporidian infection in palearctic and neotropical birds

Parasites are globally widespread pathogenic organisms, which impose important selective forces upon their hosts. Thus, in accordance with the Adjustment to parasite pressure hypothesis, it is expected that defenses among hosts vary relative to the selective pressure imposed by parasites. According to the latitudinal gradient in diversity, species richness and abundance of parasites peak near the equator. The uropygial gland is an important defensive exocrine gland against pathogens in birds. Size of the uropygial gland has been proposed to vary among species of birds because of divergent selection by pathogens on their hosts. Therefore, we should expect that bird species from the tropics should have relatively larger uropygial glands for their body size than species from higher latitudes. However, this hypothesis has not yet been explored. Here, we analyze the size of the uropygial gland of 1719 individual birds belonging to 36 bird species from 3 Neotropical (Peru) and 3 temperate areas (Spain). Relative uropygial gland volume was 12.52% larger in bird species from the tropics than from temperate areas. This finding is consistent with the relative size of this defensive organ being driven by selective pressures imposed by parasites. We also explored the potential role of this gland as a means of avoiding haemosporidian infection, showing that species with large uropygial glands for their body size tend to have lower mean prevalence of haemosporidian infection, regardless of their geographical origin. This result provides additional support for the assumption that secretions from the uropygial gland reduce the likelihood of becoming infected with haemosporidians.     

The evolution of colour polymorphism in British winter‐active Lepidoptera in response to search image use by avian predators

Phenotypic polymorphism in cryptic species is widespread. This may evolve in response to search image use by predators exerting negative frequency‐dependent selection on intraspecific colour morphs, ‘apostatic selection’. Evidence exists to indicate search image formation by predators and apostatic selection operating on wild prey populations, though not to demonstrate search image use directly resulting in apostatic selection. The present study attempted to address this deficiency, using British Lepidoptera active in winter as a model system. It has been proposed that the typically polymorphic wing colouration of these species represents an anti‐search image adaptation against birds. To test (a) for search image‐driven apostatic selection, dimorphic populations of artificial moth‐like models were established in woodland at varying relative morph frequencies and exposed to predation by natural populations of birds. In addition, to test (b) whether abundance and degree of polymorphism are correlated across British winter‐active moths, as predicted where search image use drives apostatic selection, a series of phylogenetic comparative analyses were conducted. There was a positive relationship between artificial morph frequency and probability of predation, consistent with birds utilizing search images and exerting apostatic selection. Abundance and degree of polymorphism were found to be positively correlated across British Lepidoptera active in winter, though not across all taxonomic groups analysed. This evidence is consistent with polymorphism in this group having evolved in response to search image‐driven apostatic selection and supports the viability of this mechanism as a means by which phenotypic and genetic variation may be maintained in natural populations.     

A two-stage model for Cepaea polymorphism

The history of the study of snails in the genus Cepaea is briefly outlined. Cepaea nemoralis and C. hortensis are polymorphic for genetically controlled shell colour and banding, which has been the main interest of the work covered. Random drift, selective predation and climatic selection, both at a macro- and micro-scale, all affect gene frequency. The usual approach to understanding maintenance of the polymorphism, has been to look for centripetal effects on frequency. Possible processes include balance of mutation pressure and drift, heterozygote advantage, relational balance heterosis, frequency-dependent predation, multi-niche selective balance, or some combination of these. Mutational balance is overlaid by more substantial forces. There is some evidence for heterosis. Predation by birds may protect the polymorphism, and act apostatically to favour distinct morphs. Although not substantiated for Cepaea, many studies show that predators behave in the appropriate manner, while shell colour polymorphisms in molluscs occur most commonly in species exposed to visually searching predators. It is not known whether different thermal properties of the shells help to generate equilibria. Migration between colonies is probably greater than originally thought. The present geographical range has been occupied for less than 5000 generations. Climatic and human modification alter snail habitats relatively rapidly, which in turn changes selection pressures. A simple simulation shows that migration coupled with selection which fluctuates but is not centripetal, may retain polymorphism for sufficiently long to account for the patterns we see today. There may therefore be a two-stage basis to the polymorphism, comprising long-term but weak balancing forces coupled with fluctuating selection which does not necessarily balance but results in very slow elimination. Persistence of genetic variants in this way may provide the conditions for evolution of a balanced genome.     

Colouration in Atlantic puffins and blacklegged kittiwakes: monochromatism and links to body condition in both sexes

Sexual dimorphism is widely used as an indirect measure of the intensity of sexual selection. It is also a way to evaluate whether different selective pressures act on males and females. Dichromatism, defined as a difference in colouration between males and females, may for instance result from selection for crypsis in females and selection for conspicuousness in males. Here, we conducted a study to investigate whether differential sexual selective pressures might act on the colour traits of two colonial seabird species, the Atlantic puffin Fratercula artica and the black‐legged kittiwake Rissa tricactyla. First, we used spectrophotometry and visual modelling to determine whether these presumed monomorphic birds are really monochromatic from an avian perspective (birds and humans have a different vision). Second, we estimated whether some of their colourations have the potential to be sexually or socially selected by determining whether these colourations were related to body condition in males and females, and whether the yellow, orange and red colourations may contain carotenoid pigments. Our results indicated that both species were fully monochromatic from an avian perspective. Moreover, our preliminary analyses suggested that the yellow, orange and red colours of these birds contained carotenoids. Lastly, some indices of colouration were positively linked to estimates of condition. Birds in better condition had redder gape (both species) and bill (puffins). In puffins, the relation between condition and gape colouration was significantly stronger in females than males. By contrast, the size of the gape rosette was larger in males than females. The positive links we found between colour indices and condition, together with the absence of sexual dichromatism, suggest that mutual sexual selection may act in these two species.     

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.     

Colour polymorphism is associated with lower extinction risk in birds

Colour polymorphisms have played a major role in enhancing current understanding of how selection and demography can impact phenotypes. Because different morphs often display alternative strategies and exploit alternative ecological niches, colour polymorphism can be expected to promote adaptability to environmental changes. However, whether and how it could influence populations' and species' response to global changes remains debated. To address this question, we built an up‐to‐date and complete database on avian colour polymorphism based on the examination of available data from all 10,394 extant bird species. We distinguished between true polymorphism (where different genetically determined morphs co‐occur in sympatry within the same population) and geographic variation (parapatric or allopatric colour variation), because these two patterns of variation are expected to have different consequences on populations' persistence. Using the IUCN red list, we then showed that polymorphic bird species are at lesser risk of extinction than nonpolymorphic ones, after controlling for a range of factors such as geographic range size, habitat breadth, life history, and phylogeny. This appears consistent with the idea that high genetic diversity and/or the existence of alternative strategies in polymorphic species promotes the ability to adaptively respond to changing environmental conditions. In contrast, polymorphic species were not less vulnerable than nonpolymorphic ones to specific drivers of extinction such as habitat alteration, direct exploitation, climate change, and invasive species. Thus, our results suggest that colour polymorphism acts as a buffer against environmental changes, although further studies are now needed to understand the underlying mechanisms. Developing accurate quantitative indices of sensitivity to specific threats is likely a key step towards a better understanding of species response to environmental changes.     

The fruits of selectivity: how birds forage on Goupia glabra fruits of different ripeness

Although many studies have been published on avian fruit selection, few have addressed the effects of fruit scarcity on the patterns of fruit choice. Here, we compared the consumption of seven bird species for six simultaneously present maturation stages of Goupia glabra fruits. Ripe G. glabra fruits contain more lipids, carbohydrates and energy, and fewer phenols, than unripe fruits. All bird species selected from among ripening stages and removed a higher proportion of ripe fruits than of intermediate or unripe fruits. Importantly, however, fruit choice was flexible in all species. Whether birds preferred or avoided fruits of intermediate ripeness depended on the overall fruit supply. When ripe fruits were scarce, birds showed a higher acceptance of fruits of intermediate ripeness, but still rejected the least ripe fruit stages. In a foraging bout, most birds fed on fruits of the same ripeness. By doing so, birds maximised instantaneous energy gain per time, because search time was longer for riper fruits while energy intake was lower for less ripe fruits. The results suggest that birds select fruits based on fine-scale differences in profitability, but accept less profitable fruits during low fruit abundance. If environmental factors such as overall fruit availability influence avian fruit choice, we suggest that the potential for directional selective pressures on fruit compounds is restricted.