Balancing selection maintains cryptic colour morphs

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

Beyond morphs: Inter-individual colour variation despite strong genetic determinism of colour morphs in a wild bird

Categorizing individuals into discrete forms in colour polymorphic species can overlook more subtle patterns in coloration that can be of functional significance. Thus, quantifying inter-individual variation in these species at both within- and between-morph levels is critical to understand the evolution of colour polymorphisms. Here we present analyses of inter-individual colour variation in the Reunion grey white-eye (Zosterops borbonicus), a colour polymorphic wild bird endemic to the island of Reunion in which all highland populations contain two sympatric colour morphs, with birds showing predominantly grey or brown plumage, respectively. We first quantified colour variation across multiple body areas by using a continuous plumage colour score to assess variation in brown-grey coloration as well as smaller scale variation in light patches. To examine the possible causes of among-individual variation, we tested if colour variation in plumage component elements could be explained by genotypes at two markers near a major-effect locus previously related to back coloration in this species, and by other factors such as age, sex and body condition. Overall, grey-brown coloration was largely determined by genetic factors and was best described by three distinct clusters that were associated to genotypic classes (homozygotes and heterozygote), with no effect of age or sex, whereas variation in smaller light patches was primarily related to age and sex. Our results highlight the importance of characterizing subtle plumage variation beyond morph categories that are readily observable since multiple patterns of colour variation may be driven by different mechanisms, have different functions and will likely respond in different ways to selection.     

Frequency-dependent physiological trade-offs between competing colour morphs

Evolutionary theory suggests that alternative colour morphs (i.e. genetically controlled phenotypes) may derive similar fitness under frequency-dependent selection. Here we experimentally demonstrate opposing effects of frequency-dependent social environments on plasma hormone levels (testosterone and corticosterone) and immune function between red- and black-headed male morphs of the Gouldian finch (Erythrura gouldiae). Red-headed males are highly sensitive to changes in the social environment, especially towards the relative density of their own aggressive morph, exhibiting high stress responses and immunosuppression in socially competitive environments. In contrast, the non-aggressive black-headed males follow a more passive strategy that appears to buffer them against social stresses. The differential effect of hormones on aggressive behaviour and immune performance reinforces the contrasting behavioural strategies employed by these colour morphs, and highlights the importance of the social environment in determining the individual basis of behavioural and physiological responses.     

Recent speciation between sympatric Tanganyikan cichlid colour morphs

Lake Tanganyika, Africa's oldest lake, harbours an impressive diversity of cichlid fishes. Although diversification in its radiating groups is thought to have been initially rapid, cichlids from Lake Tanganyika show little evidence for ongoing speciation. In contrast, examples of recent divergence among sympatric colour morphs are well known in haplochromine cichlids from Lakes Malawi and Victoria. Here, we report genetic evidence for recent divergence between two sympatric Tanganyikan cichlid colour morphs. These Petrochromis morphs share mitochondrial haplotypes, yet microsatellite loci reveal that their sympatric populations form distinct genetic groups. Nuclear divergence between the two morphs is equivalent to that which arises geographically within one of the morphs over short distances and is substantially smaller than that among other sympatric species in this genus. These patterns suggest that these morphs diverged only recently, yet that barriers to gene flow exist which prevent extensive admixture despite their sympatric distribution. The morphs studied here provide an unusual example of active diversification in Lake Tanganyika's generally ancient cichlid fauna and enable comparisons of speciation processes between Lake Tanganyika and other African lakes.     

Greater mycorrhizal colonization of unisexual morphs than of hermaphroditic morphs of Jacaratia mexicana during flowering and fruiting in central Mexico

Different sexual morphs of dimorphic and trimorphic populations of plants have different demands for resources correlating with phenotypic and ecological dissimilarities among morphs. Few studies have investigated the variations in mycorrhizal symbiosis across the sexual morphs of trimorphic plant populations. Here, we report seasonal variations in the mycorrhizal colonization of the roots of female, male and hermaphroditic trees of Jacaratia mexicana under field conditions in central Mexico. Mycorrhizal colonization was low in the rainy season, when J. mexicana bears only leaves, but high in the dry season when it flowers and fruits. In the dry season, the mycorrhizal colonization of female and male trees was over twofold higher than that of the hermaphroditic trees, and all three morphs had low mycorrhizal colonization in the rainy season. The lack of seasonal variation in the mycorrhizal colonization of hermaphroditic trees, together with other available evidence, supports the idea that hermaphroditic trees of J. mexicana might have some physiological disadvantages compared with male and female trees.     

Pollen colour morphs take different paths to fitness

Colour phenotypes are often involved in communication and are thus under selection by species interactions. However, selection may also act on colour through correlated traits or alternative functions of biochemical pigments. Such forms of selection are instrumental in maintaining petal colour diversity in plants. Pollen colour also varies markedly, but the maintenance of this variation is little understood. In Campanula americana, pollen ranges from white to dark purple, with darker morphs garnering more pollinator visits and exhibiting elevated pollen performance under heat stress. Here, we generate an F2 population segregating for pollen colour and measure correlations with floral traits, pollen attributes and plant‐level traits related to fitness. We determine the pigment biochemistry of colour variants and evaluate maternal and paternal fitness of light and dark morphs by crossing within and between morphs. Pollen colour was largely uncorrelated with floral traits (petal colour, size, nectar traits) suggesting it can evolve independently. Darker pollen grains were larger and had higher anthocyanin content (cyanidin and peonidin) which may explain why they outperform light pollen under heat stress. Overall, pollen‐related fitness metrics were greater for dark pollen, and dark pollen sires generated seeds with higher germination potential. Conversely, light pollen plants produce 61% more flowers than dark, and 18% more seeds per fruit, suggesting a seed production advantage. Results indicate that light and dark morphs may achieve fitness through different means—dark morphs appear to have a pollen advantage whereas light morphs have an ovule advantage—helping to explain the maintenance of pollen colour variation.     

Competition between cyanogenic and acyanogenic morphs of Trifolium repens

Summary To investigate the cost of the dimorphic cyanogenic system in Trifolium repens L., genotypes of the cyanogenic (T_c) and acyanogenic (T_a) morphs were grown in mixtures over a range of ratios and in pure stands at two levels of total density (low in a first experiment, high in a second experiment). The principles of the competition analysis employed were those related to the inverse linear model response. The morphs were compared using two interaction indices, the substitution rate and the relative resource total (RRT). The relative fitness of the two morphs, i.e. biomass and number of flowers per plant, suggests that the T_a morph has a competitive advantage over the T_c morph.     

Differences in shell properties between morphs of Littoraria pallescens

Differences between the shells of the dark and the yellow morphs of the leaf-inhabiting mangrove snail Littoraria pallescens (Philippi) have been examined. In the samples studied yellows are less heavy than darks, which agrees with earlier findings that they are thinner and more easily broken. In both morphs there is a decrease in variance of shell shape between small-shelled and large-shelled individuals, and in both size classes yellows are less variable in shell shape than darks. The interpretation of these differences in relation to stabilizing selection is discussed. It is concluded that they are not simply consequences of the normal growth process but indicate the direct action of natural selection.     

Fitness of insularia morphs of the peppered moth Biston betularia

In recent years the industrial melanic carbonaria morph in the moth Biston betularia (L.) has decreased rapidly in frequency in Britain as air pollution has decreased. The intermediate melanic insularia has shown a variable response. We have estimated the fitness of insularia, compared with the other two morphs, for several data sets. As a rule its fitness lies between that of carbonaria and typical, but nearer to typical and sometimes very close to it. The intermediate position is expected if fitness relates directly to phenotype. The results suggest that insularia may continue polymorphic while carbonaria is likely to disappear. The past high frequency of insularia in South Wales may have been due to an initial increase in insularia frequency before carbonaria reached the region. Differences in dynamics of frequency change in insularia and carbonaria are evidence against induction, which has sometimes been invoked to explain the spread of melanism in this species.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 359–366.     

Heating properties of morphs of the mangrove snail Littoraria pallescens

The rate of heating and the temperature attained after 10 and 20 min have been examined for shells of the yellow, dark and orange morphs of the mangrove leaf snail Littoraria pallescens. Under the experimental conditions used, heating from 20 to 40C took 5–10 min and thereafter the temperature remained roughly constant for up to 20 min. This represents temperature conditions which the animals are likely to experience in the wild. Large shells heat more slowly than small ones and reach lower temperatures. At around 40C yellows are on average 1.5C cooler than the dark morph, and orange individuals lie between. This difference could account for the observed difference between morphs in their choice of preferred leaf surface. Besides differing in colour, yellows are thinner and less heavy than dark shells, which probably contributes to the fact that they arc less robust.     

Ontogeny of sexual dimorphism and phenotypic integration in heritable morphs

In this study we investigated the developmental basis of adult phenotypes in a non-model organism, a polymorphic damselfly (Ischnura elegans) with three female colour morphs. This polymorphic species presents an ideal opportunity to study intraspecific variation in growth trajectories, morphological variation in size and shape during the course of ontogeny, and to relate these juvenile differences to the phenotypic differences of the discrete adult phenotypes; the two sexes and the three female morphs. We raised larvae of different families in individual enclosures in the laboratory, and traced morphological changes during the course of ontogeny. We used principal components analysis to examine the effects of Sex, Maternal morph, and Own morph on body size and body shape. We also investigated the larval fitness consequences of variation in size and shape by relating these factors to emergence success. Females grew faster than males and were larger as adults, and there was sexual dimorphism in body shape in both larval and adult stages. There were also significant effects of both maternal morph and own morph on growth rate and body shape in the larval stage. There were significant differences in body shape, but not body size, between the adult female morphs, indicating phenotypic integration between colour, melanin patterning, and body shape. Individuals that emerged successfully grew faster and had different body shape in the larval stage, indicating internal (non-ecological) selection on larval morphology. Overall, morphological differences between individuals at the larval stage carried over to the adult stage. Thus, selection in the larval stage can potentially result in correlated responses in adult phenotypes and vice versa.     

Phenotype-specific feeding behaviour of two arctic charr Salvelinus alpinus morphs

The feeding performance of two morphs of a trophically polymorphic fish, the arctic charr Salvelinus alpinus, feeding on zooplankton, was studied in the laboratory. Limnetic morphs, with a fusiform body, terminal mouth, short pectoral fins, and relatively long and dense gill rakers, fed at significantly higher rates on Daphnia and Cyclops than did benthic morphs. The benthic morphs were characterized by a chunky body form, subterminal mouth, long pectoral fins, and relatively short and spaced-out gill rakers. The limnetic morphs attacked the prey at significantly higher rates and were more successful in capture. Benthic morphs were more reluctant to start feeding on zooplankton and reaction time was longer than in limnetic morphs. In the absence as well as presence of zooplankton food, the position of the two morphs in the aquaria differed markedly. The results agree with dietary differences found in field-collected fish. The limnetic morphs consume zooplankton, whereas benthic morphs specialize on Lymnaea gastropods. The results suggest that benthic morphs are phenotypically inferior at using the pelagic food niche. This implies that the current role of competitive or predatory interactions in segregating the morphs may be minor.     

Extensive genetic differentiation between recently evolved sympatric Arctic charr morphs

The availability of diverse ecological niches can promote adaptation of trophic specializations and related traits, as has been repeatedly observed in evolutionary radiations of freshwater fish. The role of genetics, environment, and history in ecologically driven divergence and adaptation, can be studied on adaptive radiations or populations showing ecological polymorphism. Salmonids, especially the Salvelinus genus, are renowned for both phenotypic diversity and polymorphism. Arctic charr (Salvelinus alpinus) invaded Icelandic streams during the glacial retreat (about 10,000 years ago) and exhibits many instances of sympatric polymorphism. Particularly, well studied are the four morphs in Lake Þingvallavatn in Iceland. The small benthic (SB), large benthic (LB), planktivorous (PL), and piscivorous (PI) charr differ in many regards, including size, form, and life history traits. To investigate relatedness and genomic differentiation between morphs, we identified variable sites from RNA‐sequencing data from three of those morphs and verified 22 variants in population samples. The data reveal genetic differences between the morphs, with the two benthic morphs being more similar and the PL‐charr more genetically different. The markers with high differentiation map to all linkage groups, suggesting ancient and pervasive genetic separation of these three morphs. Furthermore, GO analyses suggest differences in collagen metabolism, odontogenesis, and sensory systems between PL‐charr and the benthic morphs. Genotyping in population samples from all four morphs confirms the genetic separation and indicates that the PI‐charr are less genetically distinct than the other three morphs. The genetic separation of the other three morphs indicates certain degree of reproductive isolation. The extent of gene flow between the morphs and the nature of reproductive barriers between them remain to be elucidated.     

Alarm pheromone mediates production of winged dispersal morphs in aphids

The aphid alarm pheromone ( E )- β -farnesene (EBF) is the major example of defence communication in the insect world. Released when aphids are attacked by predators such as ladybirds or lacewing larvae, aphid alarm pheromone causes behavioural reactions such as walking or dropping off the host plant. In this paper, we show that the exposure to alarm pheromone also induces aphids to give birth to winged dispersal morphs that leave their host plants. We first demonstrate that the alarm pheromone is the only volatile compound emitted from aphid colonies under predator attack and that emission is proportional to predator activity. We then show that artificial alarm pheromone induces groups of aphids but not single individuals to produce a higher proportion of winged morphs among their offspring. Furthermore, aphids react more strongly to the frequency of pheromone release than the amount of pheromone delivered. We suggest that EBF leads to a 'pseudo crowding' effect whereby alarm pheromone perception causes increased walking behaviour in aphids resulting in an increase in the number of physical contacts between individuals, similar to what happens when aphids are crowded. As many plants also produce EBF, our finding suggests that aphids could be manipulated by plants into leaving their hosts, but they also show that the context-dependence of EBF-induced wing formation may hinder such an exploitation of intraspecific signalling by plants.     

Social competition, corticosterone and survival in female lizard morphs

We examined the selective consequences of variation in behaviour and endocrine physiology in two female throat-colour morphs of the lizard, Uta stansburiana in the wild. Female morphs differed in home-range distribution patterns and corticosterone levels in relation to the density and frequency of their female neighbours. Levels of plasma corticosterone of yellow-throated females increased with increased density of both morphs. In contrast, orange-throated females had reduced levels of corticosterone in response to increased density of orange females. Additionally, females with lower corticosterone survived poorly, suggesting that social interactions and high local densities of orange females may be potentially costly for orange females. These results are consistent with decreased fitness effects and suppression of immune function previously reported for orange female morphs surrounded by more orange neighbours. These correlations, in conjunction with previous work in this system, indicate that corticosterone is likely to be an important physiological mechanism regulating female fitness in nature.