A stable,genetically determined colour dimorphism in the dung beetle Aphodius depressus: patterns and mechanisms

1. Melanism – the occurrence of dark morphs – in insects has been attributed to differences in, among other things, thermoregulation and immune defence. Dark individuals are hypothesised to perform better in colder areas, and to exhibit stronger melanin‐based immune defence. 2. In the present study, the geographical distribution of two colour morphs in Aphodius depressus (Kugelann), its climatic correlates, and temporal stability was described. Underlying mechanisms were then targeted through experiments: the inheritance of colour through controlled crosses, heating rates by thermal imaging, physiological tolerance by critical thermal limits, and immune efficiency by melanisation of implants. 3. In A. depressus, colour appears inherited by simple Mendelian principles, with red dominating over black. The frequency of two colour morphs forms a large‐scale cline. In the South West of Finland, all individuals are black, whereas, in the North East, most are red. This pattern has remained constant over 13 years (1996–2008). 4. The geographical pattern was not attributable to thermoregulation: black morphs were more abundant in warmer rather than colder parts of the country. In experiments, we found no differences in the heating rate of the two morphs, or in their upper temperature maxima. Neither did the morphs differ in their response to artificial objects inserted in their haemolymph. 5. Overall, colour variation in A. depressus occurs as a stable, genetically determined dimorphism, governed by Mendelian inheritance. Yet, no support for prevailing theory of factors sustaining melanism was found. The reasons for colour polymorphism in insects may thus be complex, and should be sought on a case‐by‐case basis.     

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.     

Pro‐opiomelanocortin gene and melanin‐based colour polymorphism in a reptile

Colour polymorphism is widespread among vertebrates and plays important roles in prey–predator interactions, thermoregulation, social competition, and sexual selection. However, the genetic mechanisms involved in colour variation have been studied mainly in domestic mammals and birds, whereas information on wild animals remains scarce. Interestingly, the pro‐opiomelanocortin gene (POMC) gives rise to melanocortin hormones that trigger melanogenesis (by binding the melanocortin‐1‐receptor; Mc1r) and other physiological and behavioural functions (by binding the melanocortin receptors Mc1‐5rs). Owing to its pleiotropic effect, the POMC gene could therefore account for the numerous covariations between pigmentation and other phenotypic traits. We screened the POMC and Mc1r genes in 107 wild asp vipers (Vipera aspis) that can exhibit four discrete colour morphs (two unpatterned morphs: concolor or melanistic; two patterned morphs: blotched or lined) in a single population. Our study revealed a correlation between a single nucleotide polymorphism situated within the 3′‐untranslated region of the POMC gene and colour variation, whereas Mc1r was not found to be polymorphic. To the best of our knowledge, we disclose for the first time a relationship between a mutation at the POMC gene and coloration in a wild animal, as well as a correlation between a genetic marker and coloration in a snake species. Interestingly, similar mutations within the POMC 3′‐untranslated region are linked to human obesity and alcohol and drug dependence. Combined with our results, this suggests that the 3′‐untranslated region of the POMC gene may play a role in its regulation in distant vertebrates. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 160–168.     

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.     

Genetic and Ecological Characterisation of Colour Dimorphism in a Coral Reef Fish

Synopsis Many recognised species of coral reef fishes exhibit two or more colour variants, but it is unknown whether these represent genetically identical phenotypes, genetic polymorphisms or closely related species. We tested between these alternatives for two colour morphs of the coral reef fish, Pseudochromis fuscus, from Lizard Island (Great Barrier Reef). A molecular analysis using mtDNA did not detect any genetic differentiation between co-occurring ‘yellow’ and ‘brown’ colour morphs. A previous study proposed that these two colour morphs are aggressive mimics of yellow and brown damselfishes. Here, a manipulative field experiment was used to evaluate whether the colour dimorphism in P. fuscus is a phenotypic response to the presence of two different model species. Colonies of either yellow or brown damselfish species were established on different patch reefs, and each of the two different P. fuscus morphs was then placed on the different reefs. Contrary to expectations, all yellow individuals that stayed on the reefs changed to brown, regardless of the model species. No brown individuals changed to the yellow colouration. However, P. fuscus were more likely to emigrate from, or suffer higher mortality on, patch reefs where they were not matched with similarly coloured models. Clearly, yellow and brown P. fuscus are members of a single species with sufficient phenotypic plasticity to switch from yellow to brown colouration.     

Clinal polymorphism variation in the Booted Eagle Hieraaetus pennatus: the influence of climate during the breeding season

ABSTRACT

Capsule: The existence of clinal variation in the colour polymorphism of the Booted Eagle Hieraaetus pennatus in its breeding area in the Palaearctic is probably caused by the influence of precipitation and the detectability of the two morphs in different light conditions.

Aims: To test whether Booted Eagles shows clinal variation in colour polymorphism along its breeding range in the Palaearctic and to test if there was selective or/and environmental pressure in the polymorphism throughout its breeding range in the Palaearctic and South Africa.

Methods: Published data were obtained on the proportion of colour morphs of seven study populations within the Palaearctic and South Africa, as well as those of 11 populations on the Iberian Peninsula, and the variation was examined in relation to longitude, latitude, and environmental and meteorological variables.

Results: There was a strong relationship between the proportion of the dark morph and longitude from west to east. In the Palaearctic and South Africa, there was a strong positive relationship between the proportion of the dark morph and the amount of rainfall during the period of chick growth.

Conclusion: There is clinal variation in colour polymorphism in the Booted Eagle. The variation is probably maintained by disruptive selection due to climatic factors such as rain and cloud cover, which influence the detectability of the different colour morphs to their prey.     

Variation in thermal sensitivity of performance among colour morphs of a pygmy grasshopper

Populations of pygmy grasshoppers, Tetrix subulata, display genetically coded discrete variation in colour pattern and there are differences among morphs in the capacity to achieve body heating. To determine whether colour morphs differ in thermal physiology, I assessed reaction distance and jumping performance of individuals belonging to different morphs at two different temperatures. Individuals allowed a potential predator to approach less closely and jumped longer distances at high than at low temperature. My analyses also uncovered variation among morphs in average reaction distance and jumping capacity, as well as in thermal sensitivity of these two traits. Matrix correlation analysis further revealed that pair-wise differences between morphs in thermal sensitivity of jumping performance (but not reaction distance) could be accurately predicted by differences in body temperatures preferred in a laboratory thermal gradient. These results support the view that morphology, behaviour and thermal physiology of ectotherms may evolve in concert. The relationship between reaction distance and jumping performance varied among colour morphs at high temperature, and the common within-morph relationship between these two traits deviated from the corresponding among-morph relationship. This suggests that the variation among morphs has partially arisen through active divergence, with selection having influenced both traits and modifications having occurred to different degrees in different morphs. My data further suggest that pale colour morphs, with a limited capacity to attain high body temperatures, may not necessarily be at a selective disadvantage, because their physiology may be adapted to lower body temperatures.     

Immune function, parasitization and extended phenotypes in colour polymorphic pygmy grasshoppers

Ecological and evolutionary consequences of host–parasite interactions have attracted considerable attention from evolutionary biologists. Previous studies have suggested that immune responsiveness may be genetically or developmentally linked with colour pattern, such that the evolution of animal colour patterns may be influenced by correlated responses to selection for parasite resistance. We studied interactions between the endoparasitic fly Leiophora innoxia (Meigen) (Diptera: Tachinidae) and its colour polymorphic pygmy grasshopper host Tetrix undulata (Sow.) (Orthoptera: Tetrigidae) to test for morph‐specific differences in parasitization and immune defence, and host‐induced variation in parasite phenotypes. Our results revealed that c. 2 and 30% of adult grasshoppers collected from the same natural population in two subsequent years, respectively were parasitized. Parasite prevalence was independent of host sex and colour morph. Pupae were larger if the parasite had developed in a female than in a male host, possibly reflecting host resource value or a physical constraint on larval growth imposed by host body size. Pupal size was also associated with host colour morph, with individuals that had developed in dark morphs being smaller at pupation compared to those that developed in paler morphs. However, immune defence, measured as the encapsulation response to a novel antigen, did not differ among individuals belonging to alternative colour morphs or sexes. Darker morphs warm up more quickly and prefer higher body temperatures than paler ones. Encapsulation was not influenced by maintenance temperature (15 vs. 30 °C), however, suggesting that indirect effects of coloration on parasite resistance mediated via differential body temperature are unlikely. The dependence of parasite body size on host colour morph may thus reflect plasticity of growth and development of the larvae in response to differential host body temperature, rather than variable host immune defence. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85 , 373–383.     

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.     

Geographic variation in the colour/ pattern polymorphism of British Philaenus spumarius (L) (Homoptera: Aphrophoridae) populations *

Geographic variation in the frequency of colour/pattern morphs of Philaenus spumarius is described at 48 localities in England and Wales. The sites have been divided into four broad environmental categories, two urban and two rural. There is a distinction between the urban and rural groupings in the relative proportions of the colour morphs; in urban localities there is a higher combined frequency of the eight ‘melanic’ morphs. Differences also exist between locality groupings, and between the sexes, in the relative frequencies of the eight morphs within the ‘melanic’ phenotypic category. Morphs limited to the female sex in some other parts of the species range occur among males in British populations. It is suggested that the different dominance hierarchy between the sexes which exists in Fennoscandian populations may not be characteristic of British populations.     

Sympatric colour polymorphisms associated with nonrandom gene flow in cichlid fish of Lake Victoria

Colour polymorphisms have fascinated evolutionary ecologists for a long time. Yet, knowledge on the mechanisms that allow their persistence is restricted to a handful of well‐studied cases. We studied two species of Lake Victoria cichlid fish, Neochromis omnicaeruleus and Neochromis greenwoodi, exhibiting very similar sex‐linked colour polymorphisms. The ecology and behaviour of one of these species is well studied, with colour‐based mating and aggression preferences. Here, we ask whether the selection potentially resulting from female and male mating preferences and aggression biases reduces gene flow between the colour morphs and permits differentiation in traits other than colour. Over the past 14 years, the frequencies of colour morphs have somewhat oscillated, but there is no evidence for directional change, suggesting the colour polymorphism is persistent on an ecological timescale. We find limited evidence of eco‐morphological differentiation between sympatric ancestral (plain) and derived (blotched) colour morphs. We also find significantly nonrandom genotypic assignment and an excess of linkage disequilibrium in the plain morph, which together with previous information on mating preferences suggests nonrandom mating between colour morphs. This, together with negative frequency‐dependent sexual selection, found in previous studies, may facilitate maintenance of these polymorphisms in sympatry.     

Phylogeography of the poison frog Mantella viridis (Amphibia: Mantellidae) reveals chromatic and genetic differentiation across ecotones in northern Madagascar

Mantella viridis is a threatened poison frog species endemic to the ecologically very heterogeneous northern region of Madagascar. The existence of several colour morphs within M. viridis and its very low genetic differentiation to the allopatrically distributed Mantella ebenaui raise questions about the processes driving the differentiation between these poison frog populations and about their taxonomic status. Using a DNA fragment of 476 nucleotides of the mitochondrial cytochrome b gene from 240 individuals of this species complex, we investigated the genetic variability of all known colour morphs of M. viridis, sampling this species throughout its known range, as well as several populations of M. ebenaui. Our genetic results confirm that M. viridis and M. ebenaui are closely related but reveal that no haplotype sharing occurs between these two taxa. Further, our molecular analyses provided evidence for barriers to gene flow among some of the colour morphs. Estimates of overlap of bioclimatic envelopes as assessed by ecological niche modelling also suggest a distinct bioclimatic niche of some of the lineages studied.     

Hybridization and the inheritance of female colour polymorphism in two ischnurid damselflies (Odonata: Coenagrionidae)

Female‐limited polychromatism is frequent in many species of Odonata. Ischnura elegans has three colour morphs: one male‐like coloured (androchrome) and two additional gynochrome brown morphs (infuscans and rufescens‐obsoleta morphs). A total of 19 progenies obtained from once‐mated females were reared in the laboratory in three generations. Results indicate that the colour morphs are controlled by the same genetic system as previously described for I. graellsii, i.e. an autosomal locus with female‐limited expression and with three alleles with a hierarchy of dominance (p^a > pⁱ > p°). Five interspecific crossings between female I. graellsii and male I. elegans, five crossings between hybrid females and male I. elegans and one crossing between female I. graellsii and a hybrid male further confirmed that the genetic system is the same in both species. A survey of morph frequencies in north‐west Spain revealed that I. elegans shows high variability in androchrome frequency (4–91%) between nearby populations, whereas in I. graellsii androchromes never are the majority morph (5–40%). The highest androchrome frequency in I. graellsii was found in populations closest to a locality where both species have hybridized, and that now has the highest androchrome frequency of I. elegans. We hypothesize that I. elegans genes have been incorporated into the genome of I. graellsii resulting in increased androchrome frequency in the latter species. Low androchrome frequency in I. elegans seems also related to the influence of I. graellsii genes. Therefore, we suggest that hybridization between both taxa is contributing to the temporal maintenance of contrasting androchrome frequencies in nearby populations. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85 , 471–481.     

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.     

Cardiovascular system in larval zebrafish responds to developmental hypoxia in a family specific manner

Background

In eastern North America two common colour morphs exist in most populations of redback salamanders (Plethodon cinereus). Previous studies have indicated that the different morphs may be adapted to different thermal niches and the morphological variation has been linked to standard metabolic rate at 15°C in one population of P. cinereus. It has therefore been hypothesized that a correlated response to selection on metabolic rate across thermal niches maintains the colour polymorphism in P. cinereus. This study tests that hypothesis.

Results

We found that the two colour morphs do sometimes differ in their maintenance metabolic rate (MMR) profiles, but that the pattern is not consistent across populations or seasons. We also found that when MMR profiles differ between morphs those differences do not indicate that distinct niches exist. Field censuses showed that the two colour morphs are sometimes found at different substrate temperatures and that this difference is also dependent on census location and season.

Conclusion

While these morphs sometimes differ in their maintenance energy expenditures, the differences in MMR profile in this study are not consistent with maintenance of the polymorphism via a simple correlated response to selection across multiple niches. When present, differences in MMR profile do not indicate the existence of multiple thermal niches that consistently mirror colour polymorphism. We suggest that while a relationship between colour morph and thermal niche selection appears to exist it is neither simple nor consistent.     

Odour and colour polymorphism in the food-deceptive orchid Dactylorhiza romana

The food deceptive orchid, Dactylorhiza romana (Sebastiani) Soó exhibits a colour polymorphism with yellow, red, and intermediate orange morphs. In this study we tested if floral odour differed among the three distinct colour morphs. We identified 23 odour compounds in D. romana, and all of them occurred in the three colour morphs. Monoterpenes dominated the floral scent. On the basis of Euclidean distances of relative amounts of compounds, yellow morphs were closer to each other than to orange or red morphs. Differentiation of the morphs was mainly due to linalool and benzaldehyde. Linalool occurred in low relative amounts in the yellow morphs, but in high amounts in some of the red individuals, whereas benzaldehyde occurred in higher relative amounts in yellow morphs. Linalool and benzaldehyde are known to be important signal-substances in plant-insect communication, however, it remains to be shown whether insects can discriminate between flower morphs on the basis of the here shown odour differences.     

Sexual selection and non-random mating for shell colour in a natural population of the marine snailLittorina mariae (Gastropoda: Prosobranchia)

In order to estimate the three independent components of mating behaviour, sexual selection in females, sexual selection in males and mating pattern, we studied the distribution of shell colour morphs among mating pairs and between copulating and non-copulating snails in four subsamples of a natural population ofL. mariae. The colour of the shell, the sex and a qualitative estimate of age was recorded for every snail. We found sexual selection acting against one of the two commonest colours (yellow) among the young females. However, in males none of the eight shell colour morphs was favoured during matings. Male sexual choice or differences in female sexual activity may cause the sexual fitness disadvantage of yellow females. Moreover, individuals of different colour morphs did not mate at random, rather dissasortatively. A behavioural choice among shell colour morphs or a non-random microdistribution of the morphs may cause the departure from random mating in this population.     

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.