Colour Polymorphic Species Research Articles

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.

Selective use of multiple cues by males reflects a decision rule for sex discrimination in a sexually mimetic damselfly

Discriminating between the sexes when one sex resembles the members of the other sex may be challenging. When sexual mimicry imposes costs on signal receivers, receivers can minimize confusion by using nonmimetic cues that differ between the models and the mimics. We tested this hypothesis in a female-specific polymorphic damselfly Enallagma hageni, whose blue coloration of andromorphic females resembles that of males, whereas the heteromorphic females have a distinctive green colour. Both female morphs share an abdominal pattern that differs from the males'. We predicted that males selectively use both colour (the mimetic cue) and pattern (the nonmimetic cue) in sex recognition: they use the nonmimetic cue only when the encountered individual has the mimetic colour. We modified the abdominal pattern of males, andromorphs and heteromorphs to resemble that of the opposite sex, and recorded males' reactions to pattern-altered and control individuals both in an arena and in the field. Our results supported our hypothesis. We then derived and tested potential male decision rules based on the two visual cues for sex recognition. We presented focal males with unnatural, orange females possessing either a male or female abdominal pattern, and recorded the reactions of mate-searching males to individuals with a novel pink-painted phenotype. Males reacted sexually to orange- and pink-painted individuals regardless of the abdominal pattern. Collectively, our results support a male discrimination rule of ‘if not blue, then female’, providing insights into the origin of phenotypic novelty in colour-polymorphic species.

Sexually dimorphic melanin-based colour polymorphism, feather melanin content, and wing feather structure in the barn owl (Tyto alba)

Feathers confer protection against biophysical agents and determine flying ability. The geometry and arrangement of the barbs, together with the keratin and pigments deposited in the feathers, determine the mechanical stability of the vane, and its stiffness and resistance to abrasive agents. In colour-polymorphic species, individuals display alternative colour morphs, which can be associated with different foraging strategies. Each morph may therefore require specific flying abilities, and their feathers may be exposed to different abrasive agents. Feathers of differently coloured individuals may thus have a specific structure, and colour pigments may help resist abrasive agents and improve stiffness. We examined these predictions in the barn owl (Tyto alba), a species for which the ventral body side varies from white to dark reddish pheomelanic, and in the number and size of black spots located at the tip of the feathers. White and reddish birds show different foraging strategies, and the size of black feather spots is associated with several phenotypic attributes. We found that birds displaying a darker reddish coloration on the ventral body side deposit more melanin pigments in their remiges, which also have fewer barbs. This suggests that wear resistance increases with darkness, whereas feathers of lighter coloured birds may bend less easily. Accordingly, individuals displaying a lighter reddish coloration on the ventral body side, and those displaying larger black spots, displayed more black transverse bars on their remiges: as larger-spotted individuals are heavier and longer-winged birds also have more transverse bars, these bars may reduce feather bending when flying. We conclude that differently coloured individuals produce wing feathers of different strengths to adopt alternative behavioural and life history strategies. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 562‐573.

Visual habitat geometry predicts relative morph abundance in the colour-polymorphic ornate rainbowfish

During colour signalling in aquatic environments, the colour of the ambient light, the background against which signals are viewed and signal transmission through the environment can all have profound impacts on the efficacy of a given signal. In colour-polymorphic species, where alternative morphs persist owing to a balance in the natural and sexual selection for each, changes to the visual context can have large effects on the local success and relative abundance of competing phenotypes. The ornate rainbowfish, Rhadinocentrus ornatus, is composed of populations that vary in the relative frequency of red and blue individuals, and inhabit sites that vary in water transmittance from clear (white) to heavily tannin-stained (red-shifted). Using spectroradiometry, we measured the downwelling and sidewelling irradiance, bank radiance and water transmittance of 10 R. ornatus habitats. We found that the relative local abundance of each morph was predicted not by water transmittance but by chromatic differences between the vertical (downwelling light) and horizontal (bank colour) components of the habitat. This visual habitat geometry should increase contrast between the colour signal and background, with large potential to influence the strength of natural and sexual selection in this system.

Morph-specific and sex-specific temperature effects on morphology in the colour polymorphic damselfly Ischnura elegans

Colour polymorphic species with extensive ranges often exhibit large-scale geographic patterns of morph frequency variation. Because colour polymorphism is associated with correlated differences in multiple traits, such as thermal performance, a likely proximate explanation for such patterns is morph-specific responses to temperature variation. The colour polymorphic Blue-tailed damselfly Ischnura elegans exhibits large-scale geographic variation in morph frequencies, but the possibility that temperature is a proximate explanation for the latitudinal cline in morph frequencies has only ever been tested within a single developmental stage (egg survival and hatching time), where no difference between the morphs was found. I therefore carried out a temperature manipulation on larvae of I. elegans which I raised to maturity in the laboratory. I found that individuals exhibited incomplete compensatory growth after being exposed to cold temperatures, and that individuals which did not emerge successfully and those that experienced cold temperatures had more juvenile morphology in the last instar. In addition, there were sex-specific and morph-specific effects of temperature on adult morphology, such that sexual size dimorphism was increased when individuals experienced warm temperatures throughout the larval stage, and that cold temperatures tended to result in larger size of androchromes and their offspring compared to the other morphs. These results are generally consistent with the large-scale geographic variation in morph frequencies found in this species.

COLONIZATION HISTORY AND POPULATION GENETICS OF THE COLOR-POLYMORPHIC HAWAIIAN HAPPY-FACE SPIDER THERIDION GRALLATOR (ARANEAE, THERIDIIDAE)

Past geological and climatological processes shape extant biodiversity. In the Hawaiian Islands, these processes have provided the physical environment for a number of extensive adaptive radiations. Yet, single species that occur throughout the islands provide some of the best cases for understanding how species respond to the shifting dynamics of the islands in the context of colonization history and associated demographic and adaptive shifts. Here, we focus on the Hawaiian happy-face spider, a single color-polymorphic species, and use mitochondrial and nuclear allozyme markers to examine (1) how the mosaic formation of the landscape has dictated population structure, and (2) how cycles of expansion and contraction of the habitat matrix have been associated with demographic shifts, including a "quantum shift" in the genetic basis of the color polymorphism. The results show a marked structure among populations consistent with the age progression of the islands. The finding of low genetic diversity at the youngest site coupled with the very high diversity of haplotypes on the slightly older substrates that are highly dissected by recent volcanism suggests that the mosaic structure of the landscape may play an important role in allowing differentiation of the adaptive color polymorphism.

Polymorphic male color morphs visualized with steroids in monomorphic females: a tool for designing analysis of sex-limited trait inheritance

In diploid animals, males and females share most of the genome (except sex-specific elements, such as sex chromosome genes), yet despite sharing the underlying genes that hard-wire traits, males and females may differ in their phenotypes when traits are controlled by proximate mechanisms, such as hormones. In color polymorphic species where coloration is only expressed in one sex, the design of studies of the inheritance of color and coevolved morph-specific traits (e.g. territorial vs sneaker strategies, skewed energetic investment in territorial defense vs sperm production, etc.) is compromised as the expression of morph-coding genes is only visualized in one sex. Here, we circumvented this problem by first characterizing oxidative stress traits in both sexes and then using testosterone implants in females to expose their otherwise 'silent' coloration. Males of our model species are highly territorial and exhibit morph-specific levels of aggression, whereas females are non-territorial and display very low levels of aggression. Interestingly, reactive oxygen species levels were found to be morph specific regardless of sex, despite considerable differences in lifestyle. Males and females did differ remarkably, however, in superoxide levels depending on whether they sported a colored throat bib or not, a trait also used in male sexual signaling. Females with throat bibs had significantly lower levels of superoxide than females without a bib, which was not the case for males.

Colour polymorphism in the polychaete Harmothoe imbricata (Linnaeus, 1767)

We investigated whether the different colour morphs in Harmothoe imbricata constitute a single polymorphic species or if there are several species present. We sequenced the mitochondrial COI and the nuclear ITS1–5.8SrDNA–ITS2 region from 57 specimens representing 10 distinct colour morphs collected from Svalbard to the Swedish west coast. The resulting minimum spanning haplotype network based on mitochondrial COI unequivocally shows H. imbricata to be a single and colour polymorphic species, whereas variation in the ITS region was very limited.

Eumelanin-based coloration and fitness parameters in birds: a meta-analysis

Although melanin is the most common pigment in animal integuments, the adaptive function of variation in melanin-based coloration remains poorly understood. The individual fitness returns associated with melanin pigments can be variable across species as these pigments can have physical and biological protective properties and genes involved in melanogenesis may vary in the intensity of pleiotropic effects. Moreover, dark and pale coloration can also enhance camouflage in alternative habitats and melanin-based coloration can be involved in social interactions. We investigated whether darker or paler individuals achieve a higher fitness in birds, a taxon wherein associations between melanin-based coloration and fitness parameters have been studied in a large number of species. A meta-analysis showed that the degree of melanin-based coloration was not significantly associated with laying date, clutch size, brood size, and survival across 26 species. Similar results were found when restricting the analyses to non-sexually dimorphic birds, colour polymorphic and monomorphic species, in passerines and non-passerines and in species for which inter-individual variation in melanism is due to colour intensity. However, eumelanic coloration was positively associated with clutch and brood size in sexually dimorphic species and those that vary in the size of black patches, respectively. Given that greater extent of melanin-based coloration was positively associated with reproductive parameters and survival in some species but negatively in other species, we conclude that in birds the sign and magnitude of selection exerted on melanin-based coloration is species- or trait-specific.

Does floral trait variability enhance reproductive success in deceptive orchids?

Unusually high intra-specific floral trait variability has often been described within deceptive orchid populations, as opposed to rewarding ones. Such variability is traditionally thought to have consequences on reproduction in this orchid group, i.e. phenotypically variable deceptive species may have a reproductive success advantage compared to those with a constant floral display. The proposed reason for this hypothetic pattern is that floral trait variability decreases pollinator avoidance learning in dealing with nectarless flowers, hence increasing their visitation rate. However, despite an intuitive and appealing hypothesis and a possible mechanism to explain it, the often-cited higher reproductive success induced by floral trait variability still remains unsupported. Here, we review the literature and consider eight studies that have experimentally or correlatively tested this hypothesis in deceptive orchids. In all these experiments, we have found no difference in average reproductive success between populations with high versus low flower trait variability, either in scent variable or colour polymorphic species. We discuss possible explanations for the lack of this pattern including the incapability of pollinators in perceiving the variability, the scarce relevance of polymorphic traits in the choice of species to forage on, or a different pollinator behaviour than the one proposed. We suggest that the high phenotypic variability is not likely to enhance deceptive orchids’ reproductive success, but is more likely to be a consequence of relaxed selection by pollinators. Nonetheless, information regarding orchid pollination strategy or pollinator cognitive abilities is often superficial, hence calling researchers for additional investigations that can contribute to a better understanding of this debated and yet unsupported hypothesis.

Colour phases of the eastern screech owl: a comparison of biomechanical variables of body contour feathers

Summary 1. Melanin is a ubiquitous pigment in the animal kingdom and has been reported to increase biological tissue strength. Melanin is responsible for many observed cases of colour polymorphism, or existence of two or more distinct plumage colours in one species (regardless of age, sex, or mass). Researchers have postulated that the relative concentration of melanin pigments deposited in feathers may function to strengthen feathers but colour polymorphic species have been ignored. Here, we investigate whether different morphs of a polymorphic bird species exhibit differential plumage strength. 2. While colour polymorphism is widespread in birds, there is no consensus on the adaptive significance of polymorphism or the maintenance of clinal variation in colour morphs. The eastern screech owl (Megascops asio) is a polymorphic species; individuals exhibit rufous, intermediate, or grey coloration that is likely caused by relative amounts or concentration of black or rufous melanin subtype (eumelanin and pheomelanin respectively). This species exhibits clinal variation in morph prevalence; the rufous morph predominates in humid deciduous forests while the grey morph is more common in dry or cold environments. 3. Here, we test the hypothesis that differences in feather strength may select for darker plumage in drier climates. First, we use reflectance spectrometry to objectively verify differences in colour morphs of the eastern screech owl. Second, we measure mechanical variables and morphology of dorsal feather barbs. 4. While reflectance spectrometry objectively separated the three colour morphs, we found no significant differences in the mechanical variables of plumage morphs. These results fail to demonstrate differences in plumage strength among eastern screech owl colour variants. 5. This conclusion rejects the hypothesis that melanin subtype affects the strength of body contour feathers in the eastern screech owl and may not factor in the maintenance of the observed clinal variation.

Territorial male color predicts agonistic behavior of conspecifics in a color polymorphic species

Male cichlid fish, Astatotilapia burtoni, live in a lek-like social system in shore pools of Lake Tanganyika, Africa, as one of two distinct social phenotypes: territorial (T) males that comprise approximately 10‐30% of the population and nonterritorial (NT) males that make up the rest. T males are brightly colored either blue or yellow with chromatic body patterns and are larger, reproductively capable, and defend territories containing a food resource used to entice females to spawn with them. NT males are camouflage colored, smaller, have regressed gonads, and shoal with females. Importantly, males shift between these social states depending on their success in aggressive encounters. It is not known whether there is a difference between yellow and blue T morphs. Here we asked whether T males preferentially defend their territory against a male of the same or opposite color. T males observed in social groups had agonistic interactions predominantly with neighboring T males of the opposite color, and yellow morphs initiated significantly more aggressive interactions. When agonistic preference was tested experimentally, T males had significantly more agonistic interactions toward males of the opposite color, and yellow T males became territorial in the majority of those interactions. Taken together, these results suggest that male coloration is an important social signal among neighboring T males in this species and support the hypothesis that T males differentially direct agonistic behavior depending on the color of neighboring males. Key words: aggression, polymorphism, social signal, territorial. [Behav Ecol]

Sexual selection in genetic colour-polymorphic species: a review of experimental studies and perspectives

Sexual selection theory has primarily focussed on the role of mating preferences for the best individuals in the evolution of condition-dependent ornaments, traits that signal absolute quality. Because the most suitable mate for one individual is not always the best for others, however, we argue that non-directional mate choice can promote the evolution of alternative morphs that are not condition-dependent in their expression (i.e. genetic polymorphism). We list the different mate-choice rules (i.e. all individuals have the same preference; preference depends on the chooser’s morph; individuals mate preferentially with conspecifics displaying an uncommon or the most frequent morph) and review experimental studies that investigated mate choice in natural populations of colour-polymorphic animals. Our review emphasises that although the experimental data support the idea that sexual selection plays an important role in the evolution of genetic colour polymorphism in many different ways, little is known about the adaptive value of each mate-choice strategy and about their implication in the evolutionary stability of colour polymorphism. One way of solving this problem is to determine the adaptive function of colour morphs, a worthwhile objective, because better understanding of mate-choice rules in polymorphic species should provide important insights into sexual-selection processes and, in turn, into the maintenance of genetic variation.

Oxygen consumption in offspring tawny owls Strix aluco is associated with colour morph of foster mother

In several colour polymorphic species, morphs differ in thermoregulation either because dark and pale surfaces absorb solar radiation to a different extent and/or because morphs differ in key metabolic processes. Morph-specific thermoregulation may potentially account for the observation that differently coloured individuals are frequently not randomly distributed among habitats, and differ in many respects, including behaviour, morphology, survival and reproductive success. In a wild population of the colour polymorphic tawny owl Strix aluco, a recent cross-fostering experiment showed that offspring raised and born from red mothers were heavier than those from grey mothers. In the present study, we tested in the same individuals whether these morph-specific offspring growth patterns were associated with a difference in metabolic rate between offspring of red and grey mothers. For this purpose, we measured nestling oxygen consumption under two different temperatures (laboratory measurements: 4 and 20°C), and examined the relationships between these data sets and the colour morph of foster and biological mothers. After controlling for nestling body mass, oxygen consumption at 20°C was greater in foster offspring raised by grey foster mothers. No relationship was found between nestling oxygen consumption and coloration of their biological mother. Therefore, our study indicates that in our experiment offspring raised by grey foster mothers showed not only a lower body mass than offspring raised by red foster mothers, but also consumed more oxygen under warm temperature. This further indicates that rearing conditions in nests of grey mothers were more stressful than in nests of red mothers.

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.