Artificial selection for food colour preferences

Colour is an important factor in food detection and acquisition by animals using visually based foraging. Colour can be used to identify the suitability of a food source or improve the efficiency of food detection, and can even be linked to mate choice. Food colour preferences are known to exist, but whether these preferences are heritable and how these preferences evolve is unknown. Using the freshwater fish Poecilia reticulata, we artificially selected for chase behaviour towards two different-coloured moving stimuli: red and blue spots. A response to selection was only seen for chase behaviours towards the red, with realized heritabilities ranging from 0.25 to 0.30. Despite intense selection, no significant chase response was recorded for the blue-selected lines. This lack of response may be due to the motion-detection mechanism in the guppy visual system and may have novel implications for the evolvability of responses to colour-related signals. The behavioural response to several colours after five generations of selection suggests that the colour opponency system of the fish may regulate the response to selection.     

How hollow melanosomes affect iridescent colour production in birds

Developmental constraints and trade-offs can limit diversity, but organisms have repeatedly evolved morphological innovations that overcome these limits by expanding the range and functionality of traits. Iridescent colours in birds are commonly produced by melanin-containing organelles (melanosomes) organized into nanostructured arrays within feather barbules. Variation in array type (e.g. multilayers and photonic crystals, PCs) is known to have remarkable effects on plumage colour, but the optical consequences of variation in melanosome shape remain poorly understood. Here, we used a combination of spectrophotometric, experimental and theoretical methods to test how melanosome hollowness—a morphological innovation largely restricted to birds—affects feather colour. Optical analyses of hexagonal close-packed arrays of hollow melanosomes in two species, wild turkeys (Meleagris gallopavo) and violet-backed starlings (Cinnyricinclus leucogaster), indicated that they function as two-dimensional PCs. Incorporation of a larger dataset and optical modelling showed that, compared with solid melanosomes, hollow melanosomes allow birds to produce distinct colours with the same energetically favourable, close-packed configurations. These data suggest that a morphological novelty has, at least in part, allowed birds to achieve their vast morphological and colour diversity.     

Evolution of female mating preferences in stalk-eyed flies

Sensory exploitation predicts that female mate preferences existbefore the evolution of exaggerated male ornaments. We testedthis prediction by estimating female preference functions, rematingintervals, and copulation durations for three species of stalk-eyedflies. Two species, Cyrtodiopsis whitei and C dalmanni, exhibitextreme sexual dimorphism in eye span, with eye stalks exceedingbody length in large males. In contrast, C quinqucguttata ofboth sexes possess short eye stalks. Maximum parsimony analysisof 437 basepairs of the 16S mitochondrial ribosomal RNA genefrom 6 Malaysian diopsids reveals that short, sexually monomorphiceye stalks are plesiomorphic in Cyrtodiopsis. Observations ofmultiple copulations by females in paired-choice mating chambersindicated that female C whitei and C. dalmanni exhibit relativepreferences for longer eye stalks such that preference intensityincreases linearly with the difference in eye stalk length betweenmales. Females from the sexually monomorphic species showedno detectable preference for male eye stalk length. Female matingpreferences of bodi sexually dimorphic species exhibited significantrepeatability, as expected if genetic variation underlies thepreference. In addition, female C whitei and C. dalmanni exhibitedshorter copulations, mated more frequently, and rejected fewermating attempts than female C quinqueguttata. Thus, opportunitiesfor sperm competition have increased with acquisition of femalepreferences. We conclude that female sensory bias for maleswith long eye span did not exist in a common ancestor to thesespecies. Instead, female preference and remating propensityeither coevolved with eye span dimorphism or evolved after maleeye stalks elongated.     

Sexual selection mediated by the thermoregulatory effects of male colour pattern in the ambush bug Phymata americana

Sexual dimorphism in coloration is a taxonomically widespread phenomenon often attributed to sexual selection on visual signals. However, the ambush bug Phymata americana exhibits sexual dimorphism in coloration that has no apparent signalling function. Here we provide evidence that colour pattern in this species influences male mating success indirectly through its effect on thermoregulation. We demonstrate, using experimental manipulation, that individuals with dark colour pattern achieve higher thoracic temperatures under illumination. We also show that dark colour pattern predicted mate-searching success but only under thermally challenging conditions (i.e. cool ambient temperature). As far as we are aware, this is the first study to provide evidence that sexual dimorphism can be accounted for by sexual selection on thermoregulatory performance.     

Experimental evidence that extra-pair mating drives asymmetrical introgression of a sexual trait

Theory suggests that traits under positive selection may introgress asymmetrically across a hybrid zone, potentially driven by sexual selection. Two subspecies of the red-backed fairy-wren (Malurus melanocephalus) differ primarily in a sexual signal used in mate choice—red versus orange male back plumage colour—but phylogeographic analyses suggest asymmetrical introgression of red plumage into the genetic background of the orange subspecies. We hypothesized that this asymmetrical introgression may be facilitated by sexual selection if red males have a mating advantage over orange males. We tested this hypothesis with correlational data and a plumage manipulation experiment where we reddened the back plumage of a subset of orange males to mimic males of the red subspecies. There was no correlational evidence of a mating advantage to naturally redder males in this population. Experimentally reddened males sired a similar amount of within-pair young and lost paternity at the same rate as orange males, but they sired significantly more extra-pair young, leading to substantially higher total reproductive success. Thus, we conclude that sexual selection via extra-pair mating is a likely mechanism responsible for the asymmetrical introgression of plumage colour in this system, and is potentially driven by a sensory bias for the red plumage signal.     

Condition-dependent expression of red colour differs between stickleback species

Sexual isolation may arise when male mating traits and female preferences differ between species. Such divergence in mating traits is likely to occur when the strength or targets of sexual selection differ. Therefore, by comparing the traits under sexual selection in closely related species and the nature of preference for those traits, we can gain insight into when sexual selection contributes to sexual isolation and how it does so. Collecting these data is no easy undertaking. To simplify this comparison, I use the presence and extent of condition dependence in traits to determine whether directional sexual selection is acting on them. Condition dependence thus serves as a signature of sexual selection. I investigate differences in sexual selection on red nuptial colour in limnetic-benthic species pairs of three-spined sticklebacks. I evaluate condition dependence by comparing the strength of the relationship between colour and condition, and the magnitude of variance in red nuptial colour to other colour traits and to nonsexual traits. I find that limnetic males have strong condition-dependent expression of red nuptial colour whereas benthic males have at most weak condition-dependent expression. Ancestral anadromous males show no condition dependence. This suggests that colour is under strong directional sexual selection only in limnetics and that this is the derived state. Moreover, I find that the strength of female preference for red is related to the extent of condition dependence. The extent of condition dependence is also associated with the importance of colour differences to mate recognition. These results show that differences between these species in the action of sexual selection underlie their sexual isolation.     

Interaction between female mating preferences and predation may explain the maintenance of rare males in the pentamorphic fish Poecilia parae

Variation in mating preferences coupled with selective predation may allow for the maintenance of alternative mating strategies. Males of the South American live‐bearing fish Poecilia parae fall in one of five discrete morphs: red, yellow, blue, stripe‐coloured tail (parae) and female mimic (immaculata). Field surveys indicate that the red and yellow morphs are the rarest and that their rarity is consistent across years. We explored the role of variable female mating preference and selective predation by visual predators in explaining the rarity of red and yellow males, and more generally, the maintenance of this extreme colour polymorphism. We presented wild‐caught P. parae females and Aequidens tetramerus, the most common cichlid predator, with the five male colour morphs in separate trials to determine mating and prey preferences, respectively. We found that a large proportion of females shared a strong preference for the rare carotenoid‐based red and yellow males, but a distinct group also preferred the blue and parae morphs. The cichlid predator strongly preferred red and yellow males as prey. Together, these results suggest that the interaction between premating sexual selection favouring and predation acting against the red and yellow morphs may explain their rarity in the wild. The trade‐off between sexual and natural selection, accompanied by variation in female mating preferences, may therefore facilitate the maintenance of the striking colour polymorphism in P. parae.     

Variable discrimination and asymmetric preferences in laboratory tests of reproductive isolation between cichlid colour morphs

Mating behaviour affects reproductive isolation and phenotypic differentiation. In Lake Tanganyika, the cichlid fish Tropheus moorii diversified into numerous, currently allopatric colour variants. Allopatric isolation is periodically interrupted by dispersal and secondary contact during lake level fluctuations, making long‐term differentiation partly dependent on assortative mating. Laboratory experiments with two moderately distinct morphs revealed assortative female preferences in one (Nakaku), but random mate choice in the other morph (Mbita). No discrimination was apparent between two subtly differentiated morphs (Chimba and Moliro). Tested against each other in a previous study, the highly distinct Moliro and Nakaku exhibited strong assortative preferences. The correlation between colour pattern similarity and mate discrimination suggests that allopatry and philopatric behaviour are less crucial for the maintenance of differentiation between highly distinct morphs than for more similar morphs. Interestingly, the asymmetric isolation in one pair of morphs is congruent with a pattern of unidirectional mitochondrial introgression between populations.     

Mimicry and the evolution of premating isolation in Heliconius melpomene Linnaeus

Ecological divergence can cause speciation if adaptive traits have pleiotropic effects on mate choice. In Heliconius butterflies, mimetic patterns play a role in mate detection between sister species, as well as signalling to predators. Here we show that male butterflies from four recently diverged parapatric populations of Heliconius melpomene are more likely to approach and court their own colour patterns as compared with those of other races. A few exceptions, where males were more attracted to patterns other than their own, suggest that some mimetic patterns are sub-optimal in mate choice. Genotype frequencies in hybrid zones between races of H. melpomene suggest that mating is random, so reinforcement is unlikely to have played a role in intra-specific divergence. In summary, co-evolved divergence of colour pattern and mate preference occurs rapidly and is likely the first step in Heliconius speciation.     

Differential predation on sexes affects colour polymorphism of the isopod Idotea baltica (Pallas)

Variable selection, including spatio-temporal variation, frequency-dependent selection and differential selection due to habitat choice, may maintain polymorphism in heterogeneous environments. We studied predation as a selective agent on colour polymorphism of the aquatic isopod I baltica. Variable predation on this species can arise from at least three sources. First, apostatic selection was studied by testing the formation of preferences on colour morphs in the perch, a common predator of I baltica. Such acquired preferences should induce apostatic selection. While our results indicate some acquired preferences, there was significant heterogeneity in the behaviour of predator individuals. Second, temporal variation in selection can arise due to habitat shift from the green algae juvenile habitat to the bladderwrack adult habitat, and the consequent change in the crypsis of the morphs. Different crypsis between sexes probably promoted high predation mortality among females in the juvenile habitat. The high rate of male mortality during the breeding period, on the other hand, was presumably due to their high mate-searching activity. Third, the sex-dependent habitat choice of I baltica leads to sexual differences in the susceptibility of morphs to predation. Predators preferred the white-spotted morph over the uniform one in males but not in females, supporting the 'dimorphic niche' hypothesis as an explanation of sexual differences in morph frequencies. Finally, no evidence was found that the colouration patterns were under sexual selection. We therefore conclude diat variable predation is the most promising explanation for the maintenance of polymorphism in I. baltica.     

Experimental manipulation reveals differential effects of colour pattern on survival in male and female pygmy grasshoppers

Populations of pygmy grasshoppers, Tetrix subulata, exhibit genetically coded discontinuous variation in colour pattern. To determine whether the dynamics of this polymorphism is likely to be affected by selective processes, rather than by stochastic events, we experimentally manipulated colour patterns of free-ranging grasshoppers and then calculated and controlled for differences in capture probabilities between categories of individuals before estimating and testing for differences in survival using mark–recapture data and program SURGE . We found that paint treatment had a significant effect on survival, and that the relationship between colour pattern and survival was different in males and females. Our analyses also revealed significant differences between sexes in relative frequencies of natural colour morphs, body size, activity pattern, dispersal distance and microhabitat use. These findings accord with the hypothesis that colour pattern and behaviour jointly determine susceptibility to visual predators. Our data enable us to reject the null-hypothesis that colour pattern is a selectively neutral character and that the polymorphism is maintained solely by stochastic processes, such as random genetic drift and founder events. Indeed, the effect of dorsal coloration on survival, together with associations between colour pattern and many biologically important traits (body size, behaviour, thermal capacity, physiology and reproductive performance), suggests that colour pattern is likely to significantly influence individual fitness, and that the polymorphism must be maintained by some active process, such as spatially variable selection in combination with gene flow. The possible role of colour polymorphism as an intermediate stage in the evolution of sexual dichromatism in animals is discussed.     

Frequency-dependent selection by pollinators: mechanisms and consequences with regard to behaviour of bumblebees Bombus terrestris (L.) (Hymenoptera: Apidae)

Bombus terrestris , a typical pollinating insect species, was offered artificial flowers of two different corolla colours with the same sucrose solution reward in an array. Common colours were significantly preferred, and the strength of the frequency-dependent response increased as a result of learning. There were also frequency-independent biases towards blue flowers, probably because blue flowers appeared more conspicuous to bumblebees than yellow flowers, and the degree of preference for blue was greater when flowers had low nectar rewards. Flower-to-flower movements by individual bumblebees between flowers were non-random, were biased to movements within the same flower colour, and were also dependent on morph frequency. The mechanisms governing flower selection in bumblebees are discussed. Pollinators foraging similarly in a natural situation would induce positive frequency-dependent selection, assortative mating, and directional selection on different corolla colour morphs of the plant population being visited, resulting in stabilizing selection for a single flower colour.     

Assortative preferences and discrimination by females against hybrid male song in the grasshoppers Chorthippus brunneus and Chorthippus jacobsi (Orthoptera: Acrididae)

The grasshoppers Chorthippus brunneus and Chorthippus jacobsi are highly differentiated for male mating signals, and form a mosaic hybrid zone in northern Spain. At some sites within this zone, many hybrids are observed. At others, few hybrids are observed. Such bimodal sites may reflect recent contacts between parental genotypes, or local variation in levels of assortative mating or selection against hybrids. Playback of 12 parental and F1 male songs to 296 parental and hybrid females revealed positive assortative preferences in C. brunneus and C. jacobsi females, supporting a direct role of male mating signals in female choice. However, all female genotypic classes showed reduced responsiveness to F1 male songs. Such sexual selection against hybrids is consistent with the narrow cline width observed in the field for song characters relative to morphology. These results have implications for the genetic structure of the hybrid zone and for models of speciation by reinforcement.     

No evidence for general condition-dependence of structural plumage colour in blue tits: an experiment

Condition-dependence is a central but contentious tenet of evolutionary theories on the maintenance of ornamental traits, and this is particularly true for structural plumage colour. By providing diets of different nutritional quality to moulting male and female blue tits, we experimentally manipulated general condition within the natural range, avoiding deprivation or stressful treatments. We measured reflectance of the structural-coloured UV/blue crown, a sexually selected trait in males, and the white cheek, a nonpigmented structural colour, directly after moult and again during the following spring mating season. We employed a variety of colour indices, based on spectral shape and avian visual models but, despite significant variation in condition and coloration, found no evidence for condition-dependence of UV/blue or white plumage colour during either season. These and previously published results suggest that structural colour might be sensitive to stress, rather than reduced body condition, during moult.     

Wild birds prefer the familiar morph when feeding on pastry-filled shells of the landsnail Cepaea hortensis (Müll.)

Colour polymorphisms in prey could be maintained if predators concentrate on common morphs and confer a selective advantage on rare morphs. We describe experiments to test whether wild birds feed on pastry-stuffed shells of Cepaea hortensis in a manner that might lead to such apostatic selection. The birds were first given a 'pre-training' choice test of a shell population with equal numbers of yellow unbandeds and yellow five-bandeds; they were then trained on one morph alone, given a second choice test, trained on the other morph and, finally, given a third choice test. The birds preferred five-bandeds in five of the six pre-training tests. In all six experiments the first training session increased the birds' preferences for the morph that was familiar. The results were less clear-cut when selection during pre-training was compared with selection after the second training session. However, a comparison between selection after each of the two training sessions showed that in all six experiments the results were in the direction predicted from the hypothesis that familiar morphs are preferred. This set of experiments is one of the few in which behaviour which could lead to apostatic selection has been tested with morphs that differ in pattern. The findings support the idea that polymorphism in Cepaea could be maintained by apostatic selection.