Habitat heterogeneity, predation and gene flow: colour polymorphism in the isopod, Idotea baltica

The colour polymorphic isopod Idotea baltica inhabits the brown alga Fucus vesiculosus which is often colonised by the white epizoite Electra crustulenta (Bryozoa). In an experiment the predation risk for the different colour morphs of I. baltica was highly dependent on background colouration. Morph frequencies and Electra density varied substantially among 10 collecting sites but correlated poorly with each other, suggesting that local selection for cryptic colouration may be counteracted by gene flow. Indeed, estimates based on four polymorphic allozymes suggested rate of gene flow to be high. These results support the hypothesis that locally varying selection for cryptic colouration counteracted by gene flow contributes to the maintenance of colour polymorphism in I. baltica. The visual differences between the microhabitats and the differential microhabitat use between males and females seem to result in different patterns of selection on males and females for cryptic colouration. Also this is likely to play an important role for the polymorphism.     

Shell colour polymorphism associated with substrate colour in the intertidal snail Littorina saxatilis Olivi (Prosobranchia: Littorinidae)

Littorina saxatilis Olivi (1792), the rough winkle, is highly polymorphic in shell colour. Shell colour frequencies were studied at six locations in south-western Wales, U.K., each at a geological contact between red sandstone and grey limestone or volcanic rock. At each site shell colour frequencies were determined in samples from the contact zone and on red or grey rock on either side. Highly significant associations were found between shell colour frequencies and substrate colour. Grey shells were always more common on grey rock than on red rock, and brown shells were usually more common on red than on grey rock, suggesting selection for cryptic colouration. Shell colour frequency differences were also found between replicate samples taken only 5 m apart from the same kind of rock, and between samples from the same kind of rock at the six study sites. These latter differences suggest that selection for camouflage is not the only factor involved in maintaining shell colour polymorphism in this species.     

Spots and stripes: ecology and colour pattern evolution in butterflyfishes

The incredible diversity of colour patterns in coral reef fishes has intrigued biologists for centuries. Yet, despite the many proposed explanations for this diversity in coloration, definitive tests of the role of ecological factors in shaping the evolution of particular colour pattern traits are absent. Patterns such as spots and eyespots (spots surrounded by concentric rings of contrasting colour) have often been assumed to function for predator defence by mimicking predators'' enemies'' eyes, deflecting attacks or intimidating predators, but the evolutionary processes underlying these functions have never been addressed. Striped body patterns have been suggested to serve for both social communication and predator defence, but the impact of ecological constraints remains unclear. We conducted the first comparative analysis of colour pattern diversity in butterflyfishes (Family: Chaetodontidae), fishes with conspicuous spots, eyespots and wide variation in coloration. Using a dated molecular phylogeny of 95 species (approx. 75% of the family), we tested whether spots and eyespots have evolved characteristics that are consistent with their proposed defensive function and whether the presence of spots and body stripes is linked with species'' body length, dietary complexity, habitat diversity or social behaviour. Contrary to our expectations, spots and eyespots appeared relatively recently in butterflyfish evolution and are highly evolutionarily labile, suggesting that they are unlikely to have played an important part in the evolutionary history of the group. Striped body patterns showed correlated evolution with a number of ecological factors including habitat type, sociality and dietary complexity. Our findings question the prevailing view that eyespots are an evolutionary response to predation pressure, providing a valuable counter example to the role of these markings as revealed in other taxa.     

Shell colour polymorphism in a mangrove snail Littorina sp. (Prosobranchia: Littorinidae)

Shell colour polymorphism was examined in populations of a mangrove snail Littorina sp. in Queensland, Australia. Three morphs were recognized, yellow, red and brown, and morph frequencies varied both between widely spaced populations and between islands less than 1 km apart. Morph frequencies also varied with time of year. There was a relationship between shell colour and position on the tree, with yellow snails more often occurring amongst the foliage and brown snails more often on trunks and branches. In some populations yellow snails appeared to survive better than the other morphs, while in other populations there was no difference. The evidence for the maintenance of the polymorphism by natural selection is discussed.     

Genome mapping of the orange blotch colour pattern in cichlid fishes

The dramatic variation of cichlid fish colour pattern is thought to function in mate choice, evolve by sexual selection, and contribute to explosive speciation. Here, we combine linkage mapping and population genetic analyses to identify a single region of the cichlid genome responsible for the orange blotch (OB) colour phenotype. In each analysis, OB is tightly linked to the c-ski1 gene. Additionally, we use comparative mapping information from the Takifugu rubripes and human genomes to suggest positional candidate loci for OB. Our work should engender a more comprehensive understanding of the molecular ecology of OB and its role in cichlid speciation. Moreover, we have assembled the components of a method to focus upon the genetic basis of evolutionarily and ecologically significant phenotypes.     

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.     

Hybridization and contemporary evolution in an introduced cichlid fish from Lake Malawi National Park

Rapidly evolving systems offer the chance to observe genetic and phenotypic change in real time. We exploit a well-characterized introduction of cichlid fish into Lake Malawi National Park to document a short history of habitat colonization and the evolution of genes and colour pattern. In the early 1960s, a fish exporter introduced individuals of Cynotilapia afra to a single site (Mitande Point) of Thumbi West Island and, as late as 1983, the species was confined to this location. In 2001, C. afra had colonized the entire perimeter of Thumbi West. In July of that year, we sampled C. afra individuals from six sites around the island and scored variation in dorsal fin colour as well as allelic diversity at six microsatellite loci. We found that, in two decades, C. afra had diverged into genetically distinct, phenotypically different northern and southern populations. We observed a high proportion of hybrids between the introduced C. afra and the native Metriaclima zebra on the southern coast of Thumbi West, and speculate that hybridization is facilitated by low water clarity at these windward sites. The short history of C. afra at Thumbi West is a microcosm of contemporary evolutionary divergence and may provide the opportunity to study the process from start to finish in genetic detail.     

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.     

Natural levels of colour polymorphism reduce performance of visual predators searching for camouflaged prey

Polymorphism, the coexistence of two or more variants within a population, has served as a classic model system to address questions about the evolution and maintenance of intraspecific variation. It has been hypothesized that a natural level of colour polymorphism may impair the search efficiency of visually orientated predators. To test this polymorphism protects hypothesis, we asked human participants to search for images of natural black, striped or grey Tetrix subulata grasshopper colour morphs presented against photographs of their natural habitat on computer screens. Fewer grasshoppers were detected when morphs were presented in mixed than in uniform sequences. All three morphs benefited to comparable degrees, in terms of reduced detection, from being presented in polymorphic sequences. Our findings demonstrate that natural levels of polymorphic variation can impede the efficiency of visually orientated predators and increase survival of prey. This protective effect supports the limited attention hypothesis, explains why predators develop ‘search images’, may account for the spread and establishment of novel colour variants, and contributes to maintenance of polymorphisms. © 2014 The Authors. Biological Journal of the Linnean Society published by John Wiley & Sons Ltd on behalf of The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 546–555.     

Colour pattern and inhibition of aggression in the cichlid fish Astronotus ocellatus

Oscars Astronotus ocellatus defeated in combat often undergo a colour pattern change in which the normal olive-green to brown body coloration darkens to near black, interrupted with irregular white barring. Dummy oscars were used in two complementary tests which showed that the dark-and-banded colour pattern inhibits aggression in conspecifics under two different experimental designs and with two different subject groups.     

The genetic architecture of male colour differences between a sympatric Lake Malawi cichlid species pair

The genetic basis of traits involved in reproductive isolation is a key parameter in models of sympatric speciation by sexual selection, a potential mechanism driving the explosive radiation of East African cichlids. Analysis of hybrid crosses between two sympatric Lake Malawi cichlid species, representing the extremes of the extant colour distribution, generated Castle-Wright estimates of four to seven loci controlling colour differences. Segregation patterns deviated from a purely additive model with a significant contribution from dominance, and possibly also epistasis. Evidence was found for a strong influence of autosomal loci. As departures from simple additive variation could effect the operation of models of sympatric speciation, dominance and epistasis should not be neglected.     

Background choice as an anti-predator strategy: the roles of background matching and visual complexity in the habitat choice of the least killifish

Because background matching improves concealment, prey animals have traditionally been expected to prefer parts of the habitat that match their visual appearance. However, empirical support for this is scarce. Moreover, this idea has recently been challenged by an alternative hypothesis: visual complexity of the background impedes prey detection, and hence prey could instead prefer complex parts of the habitat. We used the least killifish to test, with and without predation threat, for the importance of the visual similarity between the fish and the background, and the level of visual complexity of the background. We observed their choice between backgrounds patterned with elements based on the longitudinal black stripe of the fish. Predation risk was important under some circumstances, and induced a preference for a background of matching horizontal stripes compared with mismatching vertical stripes. Interestingly, females under predation threat showed a preference for a complex background of randomly oriented and overlapping stripes compared with matching stripes, whereas males did not discriminate between these two. Additionally, males showed a preference for matching stripes compared with complex shapes, whereas females did not discriminate between these backgrounds. We conclude that matching is important in the choice for safe habitat, but some aspects of visual complexity may override or act together with background matching.     

Evidence of disassortative mating in a Tanganyikan cichlid fish and its role in the maintenance of intrapopulation dimorphism

Morphological dimorphism in the mouth-opening direction ('lefty' versus 'righty') has been documented in several fish species. It has been suggested that this deflection is heritable in a Mendelian one-locus, two-allele fashion. Several population models have demonstrated that lateral dimorphism is maintained by negative frequency-dependent selection, resulting from interactions between predator and prey species. However, other mechanisms for the maintenance of lateral dimorphism have not yet been tested. Here, we found that the scale-eating cichlid fish Perissodus microlepis exhibited disassortative mating, in which reproductive pairings between lefties and righties occurred at higher than expected frequency (p<0.001). A previous study reported that a lefty-righty pairing produces a 1:1 ratio of lefty:righty young, suggesting that disassortative mating contributes to the maintenance of lateral dimorphism. A combination of disassortative mating and negative frequency-dependent selection may stabilize lateral dimorphism more than would a single mechanism.     

Evolution of colour patterns in East African cichlid fish

African cichlid fishes have undergone outbursts of explosive speciation in several lakes, accompanied by rapid radiations in coloration and ecology. Little is known about the evolutionary forces that triggered these events but a hypothesis, published by Wallace Dominey in 1984, has figured prominently. It states that the evolution of colour patterns is driven by sexual selection and that these colour patterns are important in interspecific mate choice, a combination which holds the potential for rapid speciation. Here we present phylogenetic analyses that describe major events in colour evolution and test predictions yielded by Dominey's hypothesis. We assembled information on stripe patterns and the presence or absence of nuptial coloration from more than 700 cichlid species representing more than 90 taxa for which molecular phylogenetic hypotheses were available. We show that sexual selection is most likely the selection force that made male nuptial coloration arise and evolve quickly. In contrast, stripe patterns, though phylogenetically not conserved either, are constrained ecologically. The evolution of vertical bar patterns is associated with structurally complex habitats, such as rocky substrates or vegetation. The evolution of a horizontal stripe is associated with a piscivorous feeding mode. Horizontal stripes are also associated with shoaling behaviour. Strength of sexual selection, measured in terms of the mating system (weak in monogamous, strong in promiscuous species), has no detectable effects on stripe pattern evolution. In promiscuous species the frequency of difference between sister species in nuptial hue is higher than in pair bonding and harem forming species, but the frequency of difference in stripe pattern is lower. We argue that differences between the two components of coloration in their exposure to natural selection explain their very different evolutionary behaviour. Finally, we suggest that habitat-mediated selection upon chromomotor flexibility, a special form of phenotypic plasticity found in the river-dwelling outgroups of the lake-dwelling cichlids, explains the rapid and recurrent ecology-associated radiation of stripe patterns in lake environments, a new hypothesis that yields experimentally testable predictions.     

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

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

A single mitochondrial haplotype and nuclear genetic differentiation in sympatric colour morphs of a riverine cichlid fish

Some of the diversity of lacustrine cichlid fishes has been ascribed to sympatric divergence, whereas diversification in rivers is generally driven by vicariance and geographic isolation. In the riverine Pseudocrenilabrus philander species complex, several morphologically highly distinct populations are restricted to particular river systems, sinkholes and springs in southern Africa. One of these populations consists of a prevalent yellow morph in sympatry with a less frequent blue morph, and no individuals bear intermediate phenotypes. Genetic variation in microsatellites and AFLP markers was very low in both morphs and one single mtDNA haplotype was fixed in all samples, indicating a very young evolutionary age and small effective population size. Nevertheless, the nuclear markers detected low but significant differentiation between the two morphs. The data suggest recent and perhaps sympatric divergence in the riverine habitat.     

Expression levels of the tetratricopeptide repeat protein gene ttc39b covary with carotenoid-based skin colour in cichlid fish

Carotenoid pigments play a major role in animal body colouration, generating strong interest in the genes involved in the metabolic processes that lead from their dietary uptake to their storage in the integument. Here, we used RNA sequencing (RNA-Seq) to test for differentially expressed genes in a taxonomically replicated design using three pairs of related cichlid fish taxa from the genera Tropheus and Aulonocara. Within each pair, taxa differed in terms of red and yellow body colouration, and high‐performance liquid chromatography (HPLC) analyses of skin extracts revealed different carotenoid profiles and concentrations across the studied taxa. Five genes were differentially expressed in all three yellow–red skin contrasts (dhrsx, nlrc3, tcaf2, urah and ttc39b), but only the tetratricopeptide repeat protein-coding gene ttc39b, whose gene product is linked to mammalian lipid metabolism, was consistently expressed more highly in the red skin samples. The RNA-Seq results were confirmed by quantitative PCR. We propose ttc39b as a compelling candidate gene for variation in animal carotenoid colouration. Since differential expression of ttc39b was correlated with the presence/absence of yellow carotenoids in a previous study, we suggest that ttc39b is more likely associated with the concentration of total carotenoids than with the metabolic formation of red carotenoids.     

An experimental test of the role of predators in the maintenance of a genetically based polymorphism

Polymorphisms provide one of the most useful tools for understanding the maintenance of genetic and phenotypic variation in nature. We have previously described a genetically based polymorphism in dorsal patterning that is expressed by female brown anole lizards, Anolis sagrei, which occur in Bar, Diamond and intermediate Diamond-Bar morphs. Previous studies of island populations in The Bahamas support a role for selection in maintaining the polymorphism, but the agents responsible for this selection remain unclear. We tested two main hypotheses regarding the importance of predation as a selective agent that maintains the polymorphism within populations. First, we tested whether correlational selection favours different combinations of morph, locomotor performance and escape behaviour by measuring morph-specific natural selection on sprint speed, running endurance and the propensity of females to either 'freeze' or 'run' in response to attempted capture. Morphs did not differ in any of these traits, nor did correlational selection consistently favour any particular combinations of morph and antipredator behaviour. Second, we experimentally excluded bird and snake predators from two entire island populations, allowed these predators access to two additional islands and then measured subsequent differences in natural selection on morphs in each population. Predators reduced the survival of Bar and Diamond females, but not of genetically intermediate Diamond-Bar females. These results provide limited evidence that predation may play a role in maintaining this polymorphism, although the functional traits that could account for differential susceptibility to predation remain unclear.