Ecological mechanisms for coexistence of colour polymorphism in a coral-reef fish: an experimental evaluation

The evolution of different colour morphs and how they are maintained in animal populations is poorly understood. We investigated the mechanisms maintaining yellow and brown morphs of a coral-reef fish, Pseudochromis fuscus, at Lizard Island, on the Great Barrier Reef. Histological examination of the gonads revealed that colour morphs were not sex-limited, therefore sexual selection does not appear to promote dichromatism in this species. The field distributions of the two colour morphs were spatially segregated, limiting the opportunity for negative frequency-dependent selection to operate. Our results support another ecological mechanism of coexistence. The yellow morph occurred in deeper areas, usually close to the reef edge, where there was a proportionally high cover of live branching corals. In contrast, the brown morph occurred in shallower areas, more distant from the reef edge, that were proportionally low in live branching corals. Within these habitats, each colour morph of P. fuscus displayed a close association with similar coloured damselfishes from the genus Pomacentrus. The yellow morph was associated with predominantly yellow damselfishes (P. moluccensis and P. amboinensis) and the brown morph with darker coloured species (P. adelus and P. chrysurus). Multiple-choice experiments in the laboratory revealed that: (1) each colour morph of P. fuscus preferentially selected habitat patches occupied by damselfishes with the same colouration; and (2) differences in microhabitat use between the two colour morphs of P. fuscus were due to the presence of different coloured damselfishes in these microhabitats. P. fuscus is a predator of newly recruited damselfishes and the striking resemblance between each morph of P. fuscus and the damselfish with which it was associated, suggests that aggressive mimicry may promote coexistence of P. fuscus colour morphs.Due to an error in the citation line, this revised PDF (published in December 2003) deviates from the printed version, and is the correct and authoritative version of the paper.     

Carotenoid-based colour polyphenism in a moth species: search for fitness correlates

Carotenoid‐based integumental coloration is often associated with individual performance in various animals. This is because the limited amount of the pigment has to be allocated to different vital functions. However, most of the evidence for the carotenoid‐based trade‐off comes from vertebrate studies, and it is unclear if this principle can be applied to insects. This possibility was investigated in Orgyia antiqua L. (Lepidoptera: Lymantriidae). The larvae of this species are polyphenic in their coloration, varying from a highly conspicuous combination of yellow hair tufts on black background to cryptic appearance with brown hair tufts. The conspicuous larvae are aposematic, advertising their aversive hairiness. The maintenance of different colour morphs in O. antiqua requires explanation, as an aposematic signal is expected to evolve towards monomorphism. Chromatographic analysis showed that the yellow coloration of the hair is based on the carotenoid pigment lutein (α‐carotene‐3,3’‐diol). The colour of hair tufts was dependent on their carotenoid content. This justifies an expectation of carotenoid‐based physiological trade‐offs between aposematic coloration and individual performance. To test this hypothesis, we monitored life histories of differently coloured larvae reared on various host plants, recording their body sizes, growth rates, and mortalities in each instar. There was a significant but relatively low heritability of tuft coloration, which allowed us to expect environmental effects. We found no phenotypic associations between hair tuft colour and performance indices in O. antiqua larvae, neither did the quality of host plant affect the frequency of colour morphs. However, the frequency of colour morphs differed between larval instars. Our results suggest that carotenoid‐mediated physiological trade‐offs are not involved in the maintenance of colour morphs in O. antiqua larvae, and factors other than individual condition should be responsible for the observed variability.     

Incipient reproductive isolation between two morphs of Drosophila elegans (Diptera: Drosophilidae)

Drosophila elegans is a flower-breeding species occurring in tropical and subtropical regions of Asia. Two morphs, brown and black, are known in this species. The brown morph is recorded from southern China, Philippines, Indonesia and New Guinea, while the black morph is from the Okinawa islands and Taiwan. The present crossing experiment suggests that the difference of body colour between them was due to alleles on a single locus or closely linked loci on an autosome; F₁ hybrids exhibited intermediate body colour. Female choice tests revealed asymmetrical premating isolation between the brown and black morphs; isolation indices ranged from 0.55 to 0.83 in the tests using females of the black morph (deviation from random mating was significant), but from — 0.03 to 0.50 in the tests using females of the brown morph (deviation from random mating was insignificant). However, body colour was not used as a criterion of mate choice by females. A weak and asymmetrical postmating isolation was also observed between the brown and black morphs; viability was lowered in F₂ progenies of crosses between females of the brown morph and males of the black morph. No premating or postmating isolation was observed between geographic strains of each morph. Under irradiation, body temperature was higher in the black morph than in the brown morph. On the other hand, no significant difference was observed in tolerance to cold, heat and desiccation between the brown and black morphs.     

Comparative life history and parasitism of a new colour morph of the walnut aphid in California

1 The walnut aphid Chromaphis juglandicola is a yellow aphid. In 2003, however, a white colour morph was discovered in the Sacramento Valley of California. The colour dimorphism occurs between clone lines and, when white morphs are present, they occur in mixed colour morph colonies on the underside of walnut leaves. 2 Laboratory experiments were undertaken to evaluate the thermal requirements for development, adult longevity and progeny production of the two colour morphs. Host instar preference of Trioxys pallidus, a parasitoid responsible for the successful biological control of the walnut aphid in California, was examined separately for each colour morph, and host colour preference was investigated for the preferred instar. 3 No differences in thermal requirements for development, adult size or mean longevity were detected between yellow and white colour morphs. A small difference in early reproduction was detected: white colour morphs produced more progeny on each of the two first days of adult reproduction than yellow colour morphs. 4 Trioxys pallidus showed a slight preference for the fourth instar of the yellow morph over the second‐ and third‐, but equal preference for second, third and fourth instars of the white morph. When offered equal numbers of fourth instars of the two colour morphs, T. pallidus did not show any colour preference. 5 The differences in early aphid reproduction and host instar preference by T. pallidus were combined in a stage‐structured matrix model. Model analysis showed a greater potential for population growth of the white morph over the yellow morph, with early reproduction having a greater influence than host instar preference.     

Evidence for reproductive isolation between two colour morphs of cavity nesting honey bees (Apis) in south India

In south India there are two distinct colour morphs of cavity nesting honey bees: the yellow ‘Plain’ morph and the black ‘Hill’ morph which are collectively known as Apis cerana. We show that the Hill morph is associated with a widely distributed mitochondrial haplotype that is present throughout mainland populations of south east Asian A. cerana. In contrast, the Plain morph, which is apparently confined to low to moderate elevations in India and Sri Lanka, is associated with a unique mitochondrial haplotype that is not present in other cavity nesting honey bees. We further show that in a region of sympatry (Bangalore, Karnataka State) the drone mating flight times of the two colour morphs barely overlap. Combined, drone flight data and the complete separation of mitochondrial haplotypes suggest that the two morphs are reproductively isolated. The Plain morph is distinguished from the Hill morph by the first three abdominal tergites of the worker, which are completely yellow in the Plain morph, whereas in the Hill morph they are black or black with yellow patches. Although the two morphs are generally distinguishable in the field by overall colouration, microscopic examination of the first 3 abdominal tergites is preferred. Received 16 February 2006; revised 11 May 2006; accepted 23 May 2006.     

Body size influences differently the detectabilities of colour morphs of cryptic prey

Body size and coloration may contribute to variation in performance and fitness among individuals; for example, by influencing vulnerability to predators. Yet, the combined effect of size and colour pattern on susceptibility to visual predators has received little attention, particularly in camouflaged prey. In the colour polymorphic pygmy grasshopper Tetrix subulata (Linnaeus, 1758), females are larger than males, although there is a size overlap between sexes. In the present study, we investigated how body size and colour morph influenced detection of these grasshoppers, and whether differences in protective value among morphs change with size. We conducted a computer‐based experiment and compared how human ‘predators’ detected images of large, intermediate or small grasshoppers belonging to black, grey or striped colour morphs when embedded in photographs of natural grasshopper habitats. We found that time to detection increased with decreasing size, that differences in time to detection of the black, grey and striped morphs depended differently on body size, and that no single morph provided superior or inferior protection in all three size classes. By comparing morph frequencies in samples of male and female grasshoppers from natural populations, we also examined whether the joint effects of size and colour morph on detection could explain evolutionary dynamics in the wild. Morph frequency differences between sexes were largely in accordance with expectations from the results of the detection experiment. The results of the present study demonstrate that body size and colour morph can interactively influence detection of camouflaged prey. This may contribute to the morph frequency differences between male and female pygmy grasshoppers in the wild. Such interactive effects may also influence the dynamics of colour polymorphisms, and contribute to the evolution of ontogenetic colour change and sexual dichromatism. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 112–122.     

Frequency distribution and environmental correlates of plumage polymorphism in the grey fantail Rhipidura fuliginosa

Abstract

The grey fantail (Rhipidura fuliginosa) in New Zealand displays a striking plumage polymorphism. Some individuals are coloured almost entirely black (the “black morph"), while other individuals sport a contrasting brown and white plumage (the “pied morph"). The adaptive significance of plumage polymorphism in this species is unknown. We mapped the relative distribution and frequency of each morph across the entire South Island range of the fantail, and correlated the frequency of the morphs with a variety of ecological variables. The black morph comprised <5% of individuals across the South Island and, contrary to previous observations, was least frequent at the southern extremes of its range. From historical records, the frequency of the black morph also appears to have declined, although we cannot rule out a bias in reporting rates of the black morph in the literature. The relative frequency of the two morphs was not related to vegetation type, annual rainfall, altitude, or mean annual temperature. Although we could not identify an environmental variable that might explain the distribution of the two morphs over the South Island, changes in the relative abundance of each morph suggest a dynamic process that warrants further long‐term study.     

Colour-associated foraging success and population genetic structure in a sit-and-wait predator Nephila maculata (Araneae: Tetragnathidae)

Giant wood spiders, Nephila maculata (Fabricius 1793), typically have a greenish cephalothorax and a dark abdomen decorated with striking yellow bands and spots. However, in Taiwan and neighbouring coastal islands we also found some morphologically indistinguishable individuals that were totally dark. As insects are attracted to ultraviolet (UV) light, we compared the UV reflectance property and insect-catching ability of the two morphs to see whether variation in colour affected foraging success. We also examined the population genetic structure to estimate indirectly the level of gene flow between these two colour morphs. Body surface UV reflection rate was measured from six areas of the spider with a spectrometer. To compare the insect-catching ability of different morphs, we recorded the spiders' body colour, orb size and insect-interception rates. The typical morph of N. maculata reflected significantly more UV in four of the six areas examined and caught significantly more insects than the melanic morph. We estimated population genetic structure by allozyme electrophoresis, using 20 loci from 17 enzymes. The population differentiation index (F_ST) derived from all eight polymorphic loci was 0.023, indicating a minimum level of genetic differentiation. These results indicate that the two morphs ofN. maculata may be members of an interbreeding population, and melanics have lower foraging success because of a lower body surface reflectance.     

Influence of shell colour on the mortality rate of the land snail Arianta arbustorum under different microclimatic regimes

The mortality of phenotypic shell colour morphs and age classes of the snail Arianta arbustorum in several microclimatic conditions was recorded. An analysis of variance was performed on five factors: adaptation temperature, relative humidity, shell colour, age class and test temperature. There were no significant differences in the mortality between different adaptation temperatures or relative humidities, but the interaction of these two factors was highly significant. There were significant differences in mortality rate between test temperature and age class. The mortality of the brown morph was higher than the yellow one at all adaptation temperatures (overall, P < 0.05). There were no significant differences between the mortality rates of the two morphs at different relative humidities. The mortality of the brown morph was higher than that of the yellow at six out of seven test temperatures. Juvenile snails survived significantly better than adults at all test temperatures.     

Colour morph related performance in the meadow grasshopper Chorthippus parallelus (Orthoptera,Acrididae)

Abstract 1. Polymorphism has been described for a number of herbivorous insects, but little is known about whether differences in body colour cause fitness differences. In Chorthippus parallelus, three main colour morphs occur, namely brown, green, and dorsally striped. 2. The present study examined colour morph abundances and morph‐related differences in body size, oviposition rate, and offspring numbers in females of C. parallelus collected in 15 montane grasslands. The study also examined the effect of plant species richness, composition, community productivity, and solar radiation on colour morph frequency and fitness. 3. The relative frequencies of the three colour morphs was 31.7% (brown), 33.1% (green), and 35.2% (dorsally striped), but the morphs were not evenly distributed across the 15 sites. 4. There was no effect of the habitat variables on the distribution of the green and the striped morph in the study sites, however 80% of the variation in the abundances of the brown morph was explained by plant species richness and composition. 5. Grasshopper size was equal among the morphs. Brown females laid significantly more egg pods than the green and dorsally striped morphs. There were no significant differences in offspring numbers among the colour morphs. 6. Body colour in C. parallelus seems to be a fitness‐relevant trait, raising the question of the evolutionary maintenance of polymorphism.     

Reflectance spectra and mating patterns support intraspecific mimicry in the colour polymorphic damselfly <Emphasis Type="Italic">Ischnura elegans</Emphasis>

Coexistence of female colour morphs in animal populations is often considered the result of sexual conflict, where polymorphic females benefit from reduced male sexual harassment. Mate-searching males easily detect suitable partners when only one type of female is present, but become challenged when multiple female morphs coexist, which may result in frequency-dependent mate preferences. Intriguingly, in damselflies, one female morph often closely resembles the conspecific male in body coloration, which has lead to hypotheses regarding intra-specific male-mimicry. However, few studies have quantitatively evaluated the correspondence between colour reflectance spectra from males and male-like females, relying instead on qualitative visual assessments of coloration. Using colour analyses of reflectance spectra, we compared characteristics of the body coloration of ontogenetic male and female colour morphs of the damselfly Ischnura elegans. In addition, we evaluated whether males appear to (1) discriminate between immature and mature female colour morphs, and (2) whether male-like females experience reduced male mating attention and low mating frequencies as predicted from male-mimicry. Spectral reflectance data show that immature female morphs differ substantially in coloration from mature individuals. Mating frequencies were much lower for immature than mature female morphs. For the male-like female morph, measures of colour were statistically indistinguishable from that of both immature and mature conspecific males. Mating frequencies of male-like females were lower than those of other mature female morphs under field and experimental conditions. Together, our results indicate that males may use the observed spectral differences in mate choice decisions. Furthermore, male-like females may be regarded as functional mimics that have reduced attractiveness and lowered rates of sexual harassment by mate-searching males.     

Female Colour Polymorphism: Gender and the Eye of the Beholder in Damselflies

Damselflies provide a classic example of female colour polymorphism. Usually, one female morph resembles the blue male colour (andromorph) while one, or more, female morphs are seen as typically female (gynomorph). Damselfly species fall in two distinct groups with respect to recent developments in mimicry theory: in some species females are perfect, they match male colouration and black patterning, and in other species they are supposed to be imperfect mimics, only matching male colouration. However, the underlying assumption of one female morph looking male-like is mostly based on human vision. Therefore we investigated the black patterning and colour of the three female morphs in Coenagrion puella, an imperfect mimic, using image analysis. In C. puella the blue female morph is perceived as male-like. We found that the black patterning of such females cannot be distinguished from the other female morphs, and is clearly different from males. Furthermore, the blue colour of andromorph females differs from the blue colour of males. Intriguingly, however, the red content did not differ between blue males and females.     

Greater cuticular melanism is not associated with greater immunogenic response in adults of the polymorphic mountain stone weta, Hemideina maori

Abstract.  1. Greater immune function is associated with the high-density melanic phase of polyphenic insects, appearing to compensate for density-dependent increases in susceptibility to parasites and/or pathogens. Other types of discrete variation in cuticular colour occur in insects (which may or may not be associated with melanin pigmentation), but whether this variation is predictive of immune ability has not been investigated.
2. In the mountain stone weta Hemideina maori , a black morph and yellow banded morph occur. These morphs are not seasonally polyphenic and have discrete haplotype genetic markers. Black individuals are typically found at lower local densities than yellow individuals, contrary to relations between cuticular melanism and density seen in polyphenic insects.
3. Yellow males and females had greater melanotic encapsulation responses upon immune challenge than did black males and females, but these differences were not associated with differences in temperature selection between morphs. Morph differences in melanotic encapsulation responses were somewhat related to differences between morphs in haemocyte concentrations.
4. These results indicate that a common form of immune expression is not heightened with dark coloration in the mountain stone weta. Thus, earlier findings of greater immunity associated with darker cuticles in phase polyphenic insects cannot be extended to insects with other forms of discrete colour variation. These findings will help in elucidating causes and consequences of such colour polymorphism, which is widespread in several insect orders.     

Intraspecific variation of flower colour and its distribution within a sea lavender, Limonium wrightii (Plumbaginaceae), in the northwestern Pacific Islands

Differentiation of flower colour is thought to be one of the most important factors promoting plant speciation. We describe the intraspecific variation of flower colour and its distribution in Limonium wrightii. We conducted a survey on 36 islands in the northwestern Pacific and discriminated six morphs of flower colour variation. Two flower colour morphs, pink and yellow, were most frequently observed, and their geographical distributions were basically allopatric. These two morphs were in contact in a narrow zone on Okinoerabu Island, located in the middle region of the Ryukyu Archipelago. In addition, orange, white, and ivory flower morphs were also found in this zone. The geographical distribution of pink and yellow morphs showed a “leapfrog” pattern; the distribution of pink flowers was divided into two areas, intercalated by the distribution of the yellow flower morph. The orange morph may have resulted from hybridization between the pink and yellow flower morphs.     

Phylogeography of colour polymorphism in the coral reef fish Pseudochromis fuscus, from Papua New Guinea and the Great Barrier Reef

Body colour has played a significant role in the evolution of coral reef fishes, but the phylogenetic level at which colour variation is expressed and the evolutionary processes driving the development and persistence of different colour patterns are often poorly understood. The aim of this study was to examine the genetic relationships between multiple colour morphs of Pseudochromis fuscus (family Pseudochromidae), both within and among geographic locations. Pseudochromis fuscus is currently described as a single species, but exhibits at least six discrete colour morphs throughout its range. In this study, P. fuscus from Papua New Guinea (PNG) and the Great Barrier Reef (GBR), Australia, formed three genetically distinct clades based on mitochondrial DNA (control region) sequence data: (1) yellow and brown morphs from the GBR and southern PNG, as well as an orange morph from southern PNG; (2) a pink morph from southern PNG; and (3) all three morphs (pink, orange and grey) found in Kimbe Bay, northern PNG. The three groups showed deep levels of divergence (d=14.6–25.4%), suggesting that P. fuscus is a complex of polychromatic species, rather than a single widespread species with many different colour morphs. Population genetic analyses indicate that the three clades have experienced unique evolutionary histories, possibly from differential effects of sea level fluctuations, barriers to gene flow and historical biogeography.     

Threshold determination for olfactory receptors of the spiny lobster

The shallow water caridean shrimps Heptacarpus pictus and H. paludicola are polymorphic in colour pattern. Populations of these species collected over colour‐variable substrates showed the greatest degree of coloration in terms of the proportion of individuals displaying a distinct colour pattern. The frequencies of H. Pictus colour morphs varied significantly between most sampling periods. Apostatic selection by fish predators is suggested as one hypothesis which could explain these changes in morph frequency.

Experiments with Heptacarpus pictus on rapid colour change showed that, although some pigment migration did occur in the chromatosomes studied, the macroscopic appearance of the colour patterns was not altered when shrimps were shifted from black to white backgrounds or vice versa. The results of background choice experiments with H. pictus suggest that these shrimp do not seek out colour backgrounds that would seem to be a matching background in a concealing coloration. This behaviour is consistent with the morphology of the colour patterns which appears to be a disruptive coloration rather than a concealing coloration that closely matches a particular substrate.     

Biased predation could promote convergence yet maintain diversity within Müllerian mimicry rings of Oreina leaf beetles

Müllerian mimicry is a classic example of adaptation, yet Müller's original theory does not account for the diversity often observed in mimicry rings. Here, we aimed to assess how well classical Müllerian mimicry can account for the colour polymorphism found in chemically defended Oreina leaf beetles by using field data and laboratory assays of predator behaviour. We also evaluated the hypothesis that thermoregulation can explain diversity between Oreina mimicry rings. We found that frequencies of each colour morph were positively correlated among species, a critical prediction of Müllerian mimicry. Predators learned to associate colour with chemical defences. Learned avoidance of the green morph of one species protected green morphs of another species. Avoidance of blue morphs was completely generalized to green morphs, but surprisingly, avoidance of green morphs was less generalized to blue morphs. This asymmetrical generalization should favour green morphs: indeed, green morphs persist in blue communities, whereas blue morphs are entirely excluded from green communities. We did not find a correlation between elevation and coloration, rejecting thermoregulation as an explanation for diversity between mimicry rings. Biased predation could explain within‐community diversity in warning coloration, providing a solution to a long‐standing puzzle. We propose testable hypotheses for why asymmetric generalization occurs, and how predators maintain the predominance of blue morphs in a community, despite asymmetric generalization.     

Dorsal pattern polymorphism in female Iberian wall lizards: differences in morphology,dorsal coloration,immune response,and reproductive investment

Sex‐specific colour polymorphisms have been extensively documented in many different taxa. When polymorphism in colour pattern is restricted to females, the condition is known as female‐limited pattern polymorphism (FPP), which has been less commonly addressed in vertebrates. FPP is present in several lizard species, although most research on lizards has focused on carotenoid‐ and pteridine‐based coloration and not on melanin‐based polymorphisms. In the present study, we focus on Iberian wall lizards, Podarcis hispanicus, where two female melanin‐based dorsal patterns can be clearly distinguished: striped and reticulated‐blotched. We indirectly tested the hypothesis that selection acts differentially among P. hispanicus female morphs to create alternative morph‐specific phenotypic optima at different levels by investigating whether morphs differ in fitness proxies. We specifically examined whether the two female dorsal pattern morphs differed in adult morphology, dorsal coloration, immune response, reproductive investment, and growth. We did not find a relationship between melanin‐based coloration and hatchling growth and immune response, despite a correlation between these traits possibly being expected as a result of pleiotropy in the melanocortin system. However, our results show that female dorsal morphs in P. hispanicus differ in terms of adult morphology, dorsal coloration, and reproductive investment. Reticulated‐blotched P. hispanicus females had deeper heads and longer femora, less melanin, and more brownish coloration, and also had larger and heavier hatchlings than striped females.