The evolution, maintenance and adaptive function of genetic colour polymorphism in birds

The hypothesis that ornaments can honestly signal quality only if their expression is condition-dependent has dominated the study of the evolution and function of colour traits. Much less interest has been devoted to the adaptive function of colour traits for which the expression is not, or is to a low extent, sensitive to body condition and the environment in which individuals live. The aim of the present paper is to review the current theoretical and empirical knowledge of the evolution, maintenance and adaptive function of colour plumage traits for which the expression is mainly under genetic control. The finding that in many bird species the inheritance of colour morphs follows the laws of Mendel indicates that genetic colour polymorphism is frequent. Polymorphism may have evolved or be maintained because each colour morph facilitates the exploitation of alternative ecological niches as suggested by the observation that individuals are not randomly distributed among habitats with respect to coloration. Consistent with the hypothesis that different colour morphs are linked to alternative strategies is the finding that in a majority of species polymorphism is associated with reproductive parameters, and behavioural, life-history and physiological traits. Experimental studies showed that such covariations can have a genetic basis. These observations suggest that colour polymorphism has an adaptive function. Aviary and field experiments demonstrated that colour polymorphism is used as a criterion in mate-choice decisions and dominance interactions confirming the claim that conspecifics assess each other's colour morphs. The factors favouring the evolution and maintenance of genetic variation in coloration are reviewed, but empirical data are virtually lacking to assess their importance. Although current theory predicts that only condition-dependent traits can signal quality, the present review shows that genetically inherited morphs can reveal the same qualities. The study of genetic colour polymorphism will provide important and original insights on the adaptive function of conspicuous traits.     

Ecological and evolutionary consequences of the trophic polymorphism in Cichlasoma citrinellum (Pisces: Cichlidae)

The neotropical cichlid fish Cichlasoma citrinellum is polymorphic in the structure of its pharyngeal jaw apparatus and external morphology. The pharyngeal jaws are either gracile and bear slender, pointed teeth (papilliform) or robust with strong, rounded teeth (molariform). Molariform morphs have a ‘benthic’, and papilliform morphs a ‘limnetic’ body form. Furthermore, this species is also polychromatic, with yellow and black morphs. The molariform morphology of the pharyngeal jaw apparatus adapts the fish for cracking and feeding on snails. Based on analysis of stomach contents, 94% of the molariform morph ate snails whereas only 19%, of the papilliform morph did so. This result suggests that the morphs occupy different ecological niches. The morphology of the pharyngeal jaw apparatus does not correlate significantly with sex, but it does with body colouration (P<0.005). Cichlasoma citrinellum mate assortatively with their own colour; therefore a mating preference for colour may lead to genetic isolation of trophic morphs. The frequency of the molariform morph differs strikingly among populations of five Nicaraguan lakes and its abundance is correlated with the abundance of snails, the fishes' principal prey item. Among populations the frequency of molariform morphs decreases in the dry season. Morphology possibly changes reversibly within particular individuals between seasons. These results suggest that phenotypic plasticity and polymorphisms may be an adaptive characteristic of cichlid fishes. Patterns of intraspecific morphological variation match patterns of interspecific morphological diversification which suggests that universal developmental mechanisms canalize the possible expressions of morphology. The ability to respond morphologically to environmental shifts, in conjunction with genetically determined trophic polymorphisms and sexual selection via mate choice, could be the basis for speciation through intermediate stages of polymorphism of the impressive adaptive radiation of cichlid fishes.     

Common Wall Lizard Females (Podarcis muralis) do not Actively Choose Males Based on their Colour Morph

Identifying the processes that lead to the evolution and maintenance of links between colour morphs and behavioural strategies has implications for the evolution of reproductive isolation and sympatric speciation. Sexual selection may play a significant role in the evolution of colour pattern complexity in reptiles, particularly when there are fitness consequences associated with mating with males of different colour morphs. In this article, we explored if common wall lizard females (Podarcis muralis) actively select males according to their morph in a colour‐assortative pattern using a multiple‐choice experiment with both visual and chemical cues. We failed to identify female active mate choice, as females did not choose males based on male colouration or femoral pore secretions. Indeed, females equally entered the three preference compartments and spent nearly the same amount of time within them, irrespective of both colour and odour of males. Consequently, our results do not support the hypothesis that colour polymorphism in this species may be driven by colour‐assortative mating promoted by females. However, we cannot exclude the possibility that females may choose males according to their colour following a flexible choice strategy, nor the possibility that females actively discriminate among males according to qualities that are not directly related to morph‐specific strategies.     

Testing the role of coadapted genes versus bet-hedging for mating strategies in colour polymorphic pygmy grasshoppers

Recent investigations of mate choice indicate that the genetic effect of sires on offspring fitness may depend on the interaction between maternal and paternal genotypes and the environmental conditions experienced by the offspring. Alternative colour morphs of the pygmy grasshopper, Tetrix subulata , represent ecological strategies that differ in body size, life history, thermoregulatory behaviour, and habitat selection. The hypothesis that selection promotes behaviours maintaining coadapted gene complexes predicts individuals to mate assortatively with respect to colour morph. On the other hand, the bet-hedging hypothesis predicts that the temporal variability of the environment inhabited by these animals may select for disassortative mating behaviour resulting in heterogeneous offspring. To distinguish between these competing hypotheses, we investigated mating behaviours using dual-choice experiments. Our results were not in agreement with the prediction of assortative mating but suggest instead that matings were random with regard to colour morph. Polyandry was common, and females mated with the second male regardless of whether the first mating was assortative or disassortative. Polyandry also was equally frequent among females in triads in which the two males belonged to different colour morphs as in triads where both males belonged to the same colour morph. A field experiment confirmed that polyandry occurred also among free-ranging individuals, and uncovered variation in mating success among male colour morphs, probably due to indirect effects of coloration on activity or habitat use. The consequences of this random and polyandrous mating strategy for the evolutionary dynamics of the colour polymorphism remain to be explored.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 491–499.     

Maladaptive mate choice maintained by heterozygote advantage

Common buzzards (Buteo buteo) show a plumage polymorphism that appears to be maintained by heterozygote advantage and allows a maladaptive form of mate choice to persist. The light and dark morphs have a much lower fitness than the presumed heterozygous intermediate morph, but are replenished through Mendelian segregation in intermediate-intermediate pairs. Light and dark morphs could maximize their fitness by mating light with dark to produce all intermediate offspring, but instead choose partners of their own color, thereby producing broods of minimally fit homozygotes. Such maladaptive behavior argues forcefully against mate choice based on "good genes," and its persistence is best explained by heterozygote advantage maintaining the polymorphism coupled with nongenetic mate choice based on sexual imprinting. Modeling different patterns of mate choice shows that random mating and preference for own morph fit our data poorly, whereas preference for mother's morph yields a good fit.     

In the eye of the beholder: visual mate choice lateralization in a polymorphic songbird

Birds choose mates on the basis of colour, song and body size, but little is known about the mechanisms underlying these mating decisions. Reports that zebra finches prefer to view mates with the right eye during courtship, and that immediate early gene expression associated with courtship behaviour is lateralized in their left hemisphere suggest that visual mate choice itself may be lateralized. To test this hypothesis, we used the Gouldian finch, a polymorphic species in which individuals exhibit strong, adaptive visual preferences for mates of their own head colour. Black males were tested in a mate-choice apparatus under three eye conditions: left-monocular, right-monocular and binocular. We found that black male preference for black females is so strongly lateralized in the right-eye/left-hemisphere system that if the right eye is unavailable, males are unable to respond preferentially, not only to males and females of the same morph, but also to the strikingly dissimilar female morphs. Courtship singing is consistent with these lateralized mate preferences; more black males sing to black females when using their right eye than when using their left. Beauty, therefore, is in the right eye of the beholder for these songbirds, providing, to our knowledge, the first demonstration of visual mate choice lateralization.     

Preference for Male Traits Differ in Two Female Morphs of the Tree Lizard,Urosaurus ornatus

Non-random female mating preferences may contribute to the maintenance of phenotypic variation in color polymorphic species. However, the effect of female preference depends on the types of male traits used as signals by receptive females. If preference signals derive from discrete male traits (i.e., morph-specific), female preferences may rapidly fix to a morph. However, female preference signals may also include condition-dependent male traits. In this scenario, female preference may differ depending on the social context (i.e., male morph availability). Male tree lizards (Urosaurus ornatus) exhibit a dewlap color polymorphism that covaries with mating behavior. Blue morph males are aggressive and defend territories, yellow males are less aggressive and defend smaller territories, and orange males are typically nomadic. Female U. ornatus are also polymorphic in dewlap color, but the covariation between dewlap color and female behavior is unknown. We performed an experiment to determine how female mate choice depends on the visual and chemical signals produced by males. We also tested whether female morphs differ in their preferences for these signals. Female preferences involved both male dewlap color and size of the ventral color patch. However, the female morphs responded to these signals differently and depended on the choice between the types of male morphs. Our experiment revealed that females may be capable of distinguishing among the male morphs using chemical signals alone. Yellow females exhibit preferences based on both chemical and visual signals, which may be a strategy to avoid ultra-dominant males. In contrast, orange females may prefer dominant males. We conclude that female U. ornatus morphs differ in mating behavior. Our findings also provide evidence for a chemical polymorphism among male lizards in femoral pore secretions.     

Red and white Chinook salmon: genetic divergence and mate choice

Chinook salmon (Oncorhynchus tshawytscha) exhibit extreme differences in coloration of skin, eggs and flesh due to genetic polymorphisms affecting carotenoid deposition, where colour can range from white to bright red. A sympatric population of red and white Chinook salmon occurs in the Quesnel River, British Columbia, where frequencies of each phenotype are relatively equal. In our study, we examined evolutionary mechanisms responsible for the maintenance of the morphs, where we first tested whether morphs were reproductively isolated using microsatellite genotyping, and second, using breeding trials in seminatural spawning channels, we tested whether colour assortative mate choice could be operating to maintain the polymorphism in nature. Next, given extreme difference in carotenoid assimilation and the importance of carotenoids to immune function, we examined mate choice and selection between colour morphs at immune genes (major histocompatibility complex genes: MHC I‐A1 and MHC II‐B1). In our study, red and white individuals were found to interbreed, and under seminatural conditions, some degree of colour assortative mate choice (71% of matings) was observed. We found significant genetic differences at both MHC genes between morphs, but no evidence of MHC II‐B1‐based mate choice. White individuals were more heterozygous at MHC II‐B1 compared with red individuals, and morphs showed significant allele frequency differences at MHC I‐A1. Although colour assortative mate choice is likely not a primary mechanism maintaining the polymorphisms in the population, our results suggest that selection is operating differentially at immune genes in red and white Chinook salmon, possibly due to differences in carotenoid utilization.     

Morph‐dependent fitness and directional change of morph frequencies over time in a Dutch population of Common buzzards Buteo buteo

How genetic polymorphisms are maintained in a population is a key question in evolutionary ecology. Previous work on a plumage colour polymorphism in the common buzzard Buteo buteo suggested heterozygote advantage as the mechanism maintaining the co‐existence of three morphs (light, intermediate and dark). We took advantage of 20 years of life‐history data collected in a Dutch population to replicate earlier studies on the relationship between colour morph and fitness in this species. We examined differences between morphs in adult apparent survival, breeding success, annual number of fledglings produced and cumulative reproductive success. We found that cumulative reproductive success differed among morphs, with the intermediate morph having highest fitness. We also found assortative mating for colour morph, whereby assortative pairs were more likely to produce offspring and had longer‐lasting pair bonds than disassortative pairs. Over the 20‐year study period, the proportion of individuals with an intermediate morph increased. This apparent evolutionary change did not just arise from selection on individual phenotypes, but also from fitness benefits of assortative mating. The increased frequency of intermediates might also be due to immigration or drift. We hypothesize that genetic variation is maintained through spatial variation in selection pressures. Further studies should investigate morph‐dependent dispersal behaviour and habitat choice.     

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.     

Influence of previous experience on the mate selection of two colour morphs of the convict cichlid, Cichlasoma nigrofasciatum (Pisces,Cichlidae)

In a pilot test, individuals of two colour morphs of Cichlasoma nigrofasciatum showed colour preferences in their schooling behaviour according to previous experience. Two further experiments were undertaken to investigate if such experientially induced preferences could reflect on the choice of mate. In one experiment white males who had been reared differently with regard to the colour morph of parents and siblings were given females of the different colour morphs (white and normal) to choose from, the females being successively removed after pairing to induce further choices. In this test, however, the males predominantly chose normal females, probably because of dominance relationships among the females, which masked a possible colour preference. Instead, a free choice test was devised, where 74 white and 74 normal fishes were allowed to pair off freely in a large tank. Here, a statistically significant sexual preference for the previously experienced colour morph was found. These results, as well as the possible evolutionary consequences, are discussed.     

Female mate-choice behavior and sympatric speciation

Many models have investigated how the process of speciation may occur in sympatry. In these models, individuals are either asexual or mate choice is determined by very simple rules. Females, for example, may be assumed either to compare their phenotype to that of a potential mate, preferring to mate with similar males (phenotype matching), or to possess preference genes that determine which male phenotype they prefer. These rules often do not reflect the mate-choice rules found in empirical studies. In this paper, we compare these two modes of female choice with various types of sexual imprinting. We examine the efficacy of different mate-choice behavior in causing divergence in male traits under simple deterministic one-locus population genetic models as well as under polygenic, individual-based simulations based on the models of Dieckmann and Doebeli (1999). We find that the inheritance mechanism of mate choice can have a large effect on the ease of sympatric speciation. When females imprint on their mothers, the result of the model is similar to phenotype matching, where speciation can occur fairly easily. When females imprint on their fathers or imprint obliquely, speciation becomes considerably less likely. Finally, when females rely on preference genes, male trait evolution occurs easily, but the correlation between trait and preference can be weak, and interpreting these results as speciation may be suspect.     

Reversible frequency-dependent switches in male mate choice

Current sexual-selection theories predict that mating should occur preferentially with the highest-quality partner, and assume that for distinguishing among potential mates the choosy sex applies an internal representation of the characteristics of the desired mate, i.e. a template. Binary choice experiments were performed to test male mate choice between two different female colour morphs in the damselfly Ischnura elegans. Choice experiments were conducted before and after an habituation period, during which males were exposed to only one female colour morph. Given the choice between the two female morphs, males did exhibit a choice for the most recently experienced female morph. This is the first evidence for a reversible switch in mate choice in a frequency-dependent way. In contrast with previous studies on mate choice, template formation in male I. elegans seems not to be based on quality. Switching mate choice in a frequency-dependent manner, choosing the most common morph, probably allows males to minimize their search efforts and to maximize fitness.     

Dynamics of colour polymorphism in a changing environment: fire melanism and then what?

Studies of whether disturbance events are associated with the changing genetic compositions of natural populations may provide insights into the importance of local selection events in maintaining diversity, and might inform plans for the conservation and protection of that diversity. We examined the dynamics of a colour pattern polymorphism in a natural population of pygmy grasshoppers Tetrix subulata (Orthoptera: Tetrigidae) inhabiting a previously burnt clear-cut area. Data on morph frequencies for wild-caught and captive-reared individuals indicated that the initial dominance of black phenotypes following the fire event was followed by an increased diversity of the polymorphism. This was manifested as the appearance of a novel morph, a decreased incidence of the black morph, and a more even distribution of individuals across alternative morphs following the recurrence of vegetation. We also found that the colour patterns of captive-reared individuals resembled those of their parents and that the degree of within-clutch diversity increased between generations. Our comparisons of morph frequencies across generations and between environments within generations point to a genetic determination of colour pattern, and indicate that the polymorphism is influenced more strongly by selection than by plasticity or migration.     

Correlated evolution of colour pattern and body size in polymorphic pygmy grasshoppers, Tetrix undulata

Theory posits that selection on functionally interrelated characters will promote physical and genetic integration resulting in evolution of favourable trait-value combinations. The pygmy grasshopper Tetrix undulata (Orthoptera: Tetrigidae) displays a genetically encoded polymorphism for colour pattern. Colour morphs differ in several traits, including behaviours, thermal biology and body size. To examine if these size differences may reflect phenotypic plasticity of growth and development in response to temperature we used a split brood-design and reared hatchlings from mothers belonging to different morphs in different thermal environments (warm or cold) until maturity. We found that time to maturity was longer in the cold compared with the warm treatment. In the warm (but not in the cold) treatment time to maturity also varied among individuals born to mothers belonging to different colour morphs. Although low temperature and long development time are normally accompanied by increased body size in ectotherms, our results revealed no difference in size at maturity between individuals reared in the two temperature treatments. There was also an increase (not a decrease) in adult body size with shortened time to maturity across families within each treatment. Taken together, this suggests that body size is canalized against environmental perturbations, and that early maturation does not necessarily trade off against a size-mediated decrease in fecundity. Heritability of body size was moderate in magnitude. Moreover, body size at maturity varied among individuals belonging to different morphs and was influenced also by maternal colour morph, suggesting that a genetic correlation exists between colour pattern and body size. These findings suggest that different characters have evolved in concert and that the various colour morphs represent different evolutionary strategies, i.e., alternative peaks in a multi-modal adaptive landscape.     

Colour biases in territorial aggression in a Neotropical cichlid fish

Discrete colour morphs have provided important insights into the evolution of phenotypic diversity. One of the mechanisms that can help to explain coexistence of ecologically similar colour morphs and incipient species is (colour) biased aggression, which has the potential to promote continued existence of the morphs in a frequency-dependent manner. I addressed colour biases in territorial aggression in a field-based study on a Neotropical cichlid fish species, Amphilophus sagittae, which has two ecologically indistinguishable colour morphs that mate assortatively. I found that A. sagittae, in particular females, were more aggressive towards models of their own colour than those mimicking colours of the other morph. Such a behavioural pattern should result in a selection regime that benefits the rarer morph, and hence could help explain how novel, rare phenotypes may avoid competitive exclusion.     

Balancing selection maintains cryptic colour morphs

Animals display incredibly diverse colour patterns, a testament to evolution's endless innovation in shaping life. In many species, the interplay between males and females in the pursuit of mates has driven the evolution of a myriad of colour forms, from the flashy peacock tail feathers to the tiniest colour markings in damselflies. In others, colour provides crypsis by allowing to blend into the background and to escape the eyes of predators. While the obvious benefits of this dazzling diversity for reproduction and survival seem straightforward, its maintenance is not. Theory predicts that genetic drift and various forms of selection reduce variation over time, making the persistence of colour variants over generations a puzzle. In this issue of Molecular Ecology, Lindtke et al. ( 2017 ) study the cryptic colour morphs of Timema cristinae walking sticks to shed light on the genetic architecture and mechanisms that allow colour polymorphism maintenance over long timescales. By combining genome‐wide data with phenotyping information from natural populations, they were able to map the green and melanistic colour to one genomic region with highly reduced effective recombination rate between two main chromosomal variants, consistent with an inversion polymorphism. These two main chromosomal variants showed geographically widespread heterozygote excess, and genomic signatures consistent with long‐term balancing selection. A younger chromosomal variant was detected for the third morph, the green‐striped colour morphs, in the same genomic regions as the melanistic and the green‐unstriped morphs. Together, these results suggest that the genetic architecture of cryptic T. cristinae morphs is caused by nonrecombining genomic blocks that have been maintained over extended time periods by balancing selection making this study one of the few available empirical examples documenting that balancing selection of various forms may play an important role in maintaining adaptive genetic variation in nature.     

A colour and size dimorphism in the green swordtail (population Jalapa): female mate choice,male–male competition,and male mating strategies

Two types of males are present in the Jalapa population of Xiphophorus helleri: Males with a black or dark brownish mid-lateral stripe ("black males") mature earlier and are smaller than males with a red or brownish mid-lateral stripe ("red males"). We tested the hypothesis that the colour patterns of red males may be regarded as ornaments, which evolved as the result of inter- and/or intrasexual selection. As predicted, in choice tests females exhibited a strong preference for red versus black males. Furthermore, in competition experiments red males became dominant over black males with no exception, both when body size was equal and even when red males were 3–5 mm smaller than black males. However, contrary to our prediction, sneak–chase behaviour in black males was not detected, and courtship displays occurred at similar rates in both morphs. Red males are always heterozygous, with one allele for red and another for black colouration. This genetic constraint potentially prevents the extinction of the black morph. Possibly, the colour patterns of red males are functioning as indicators of heterozygosity. According to the "heterozygosity theory of mate choice", the female's preference for red males may be adaptive.     

Fruit colour polymorphism in Acacia ligulata: seed and seedling performance, clinal patterns, and chemical variation

Fruit colour polymorphisms are widespread in nature, but their ecological and evolutionary dynamics remain poorly understood. Here we examine Acacia ligulata, a shrub of the Australian arid zone which exhibits a red/orange/yellow aril colour polymorphism. We asked whether the polymorphism had a genetic basis; whether selection acted differentially on morphs during the seed and seedling stages; whether geographic variation in morph frequencies was correlated with environmental factors; and whether morphs differed in physical or chemical characteristics that might influence selection on them. When grown to maturity in a common greenhouse environment, maternal families of seeds showed phenotypic patterns consistent with biparental genetic control of the polymorphism. In contrast to other fruit-colour polymorphic species, progeny of A. ligulata morphs did not vary in rates of seedling emergence or survival in a common garden. Sampling along a 580 km transect revealed clinal variation in morph frequencies. Frequencies of the yellow morph decreased, and frequencies of the red morph increased, across a gradient of decreasing temperature and increasing rainfall. Morphs did not differ in seed mass, aril mass, or in profiles of fatty acids and flavonoids in either arils or seeds. However, morphs showed consistent differences in carotenoid profiles' and elemental content of arils, suggesting that selection by avian and insect seed dispersers, seed predators and herbivores should be investigated. These patterns indicate that both abiotic and biotic factors may contribute to selection on the A. ligulata polymorphism. This revised version was published online in August 2006 with corrections to the Cover Date.     

Discrete genetic variation in mate choice and a condition-dependent preference function in the side-blotched lizard: implications for the formation and maintenance of coadapted gene complexes

Variation in female preference functions, both genotypic andphenotypic, has been largely ignored in the literature, despiteits implications to the maintenance of genetic variation inpopulations and the resolution of the "Lek paradox." Polymorphicpopulations, such as in the side-blotched lizard, provide idealstudy systems for its investigation, especially in the contextof incipient processes of sympatric speciation. Females of theside blotch lizard exist in 2 genetically distinct morphs, yellowthroated and orange throated, that experience disruptive selectionfor life history traits. Males express 3 throat color morphs,blue, orange, and yellow, that exhibit alternative strategiesin intrasexual competition. We experimentally tested for femalepreference in triadic mate choice trials to identify the presenceof discrete genetic and condition-dependent variation in femalepreference function. We found that females did in fact showgenetic variation in preference for males but that females alsooperate a multicondition preference function dependent uponthe genotype of the female and her state (number of clutcheslaid). Females exhibited positive assortative mating prior tothe first clutch. However, prior to later clutches, orange femalesswitched choice, preferring yellow males. These findings arediscussed in relation to the maintenance of coadapted gene complexeswithin populations and the prevention of divergent directionalselection (population bifurcation) by condition-dependent variationin mate choice.