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.     

Flower colour adaptation in a mimetic orchid

Although the tremendous variability in floral colour among angiosperms is often attributed to divergent selection by pollinators, it is usually difficult to preclude the possibility that floral colour shifts were driven by non-pollinator processes. Here, we examine the adaptive significance of flower colour in Disa ferruginea, a non-rewarding orchid that is thought to attract its butterfly pollinator by mimicking the flowers of sympatric nectar-producing species. Disa ferruginea has red flowers in the western part of its range and orange flowers in the eastern part--a colour shift that we hypothesized to be the outcome of selection for resemblance to different local nectar-producing plants. Using reciprocal translocations of red and orange phenotypes as well as arrays of artificial flowers, we found that the butterfly Aeropetes tulbaghia, the only pollinator of the orchid, preferred both the red phenotype and red artificial flowers in the west where its main nectar plant also has red flowers, and both the orange phenotype and orange artificial flowers in the east, where its main nectar plant has orange flowers. This phenotype by environment interaction demonstrates that the flower colour shift in D. ferruginea is adaptive and driven by local colour preference in its pollinator.     

Importance of colour in the reaction of passerine predators to aposematic prey: experiments with mutants of Pyrrhocoris apterus (Heteroptera)

Persistent questions concerning the warning coloration of unpalatable insects address whether the bright aposematic colour itself or its combination with a species-specific dark pattern is the key factor in their protection against insectivorous birds, and how chromatic polymorphism originates and is maintained in aposematics. In the present study, these questions were tested experimentally, using the birds Parus major , Parus caeruleus , Erithacus rubecula , and Sylvia atricapilla as predators, and chromatically polymorphic firebug Pyrrhocoris apterus : red wild form, white, yellow, and orange mutants (all four of them with the same black melanin pattern, the mutants differing in colour of pteridine pigments only) and the nonaposematic brown-painted wild form as prey. The results show that a specific colour is essential for the birds to recognize the specific aposematic prey; the melanin pattern is not sufficient. White mutants were no better protected than nonaposematic firebugs; red wild-type and orange mutants were equally well protected against all bird species; and the reaction of birds to yellow mutants was species-specific. An evolutionary scenario of 'recurrent recessive mutations' is formulated to explain the origin of colour polymorphism in some aposematics.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 143–153.     

Ontogenetic colour change signals sexual maturity in a non-territorial damselfly

Conspicuous colouration increases male reproductive success through female preferences and/or male–male competition. Despite the advantages of conspicuous colouration, inconspicuous male morphs can exist simultaneously in a population due to genetic diversity, condition dependence or developmental constraints. We are interested in explaining the male dichromatism in Xanthagrion erythroneurum damselflies. We reared these damselflies in outdoor insectaries under natural conditions and showed that this species undergoes ontogenetic colour changes. The younger males are yellow and change colour to red 6–7 days after their emergence. We took red and yellow male reflectance spectra and found that red males are brighter than yellow males. Next, we aimed to determine whether ontogenetic colour change signals sexual maturity with field observations and laboratory experiments. Our field observational data showed that red males are in higher abundance in the breeding territory, and they have a higher mating frequency than yellow males. We confirmed these field observations by enclosing a red and a yellow male with two females and found that yellow males do not mate in presence of red males. To determine whether colour change signals sexual maturity, we measured mating success of males before and after colour changes by enclosing a single male at different age (day 3-day 7) and colour (yellow, intermediate and red) with a single female in a mating cage. Males did not mate when yellow but the same male mated after it changed colour to red, suggesting the ontogenetic colour change signals sexual maturity in this species. Our study shows that male dichromatism can be age-dependent and ontogenetic colour change can signal age and sexual readiness in non-territorial insects.     

Shell colour variation in Bullia digitalis, a sand-dwelling, intertidal whelk (Gastropoda: Prosobranchia)

Bullia digitalis is an intertidal whelk that lives on sandy beaches in South Africa. It is highly variable in shell colour, with individuals varying from white to dark brown. This paper describes shell colour variation of B. digitalis at seven sites, along a 230 km coastline east of the Cape Peninsula. Seven colour forms were found: striped, violet, banded violet, banded brown, orange, pale yellow and white. These forms are probably genetically determined morphs. The striped form is the most common at all sites, constituting 53–62% of each sample. The violet is the second most common morph. Its frequencies are remarkably stable at 15–17%. The striped form blends well into the sandy environment and may therefore be of considerable cryptic value in concealing B. digitalis from predators. The violet form is highly conspicuous. Its stable frequency throughout the study area may represent a genetic balance that is not relevant to any visual advantages of the violet colour.     

Phenotype-dependent mate choice and the influence of mixed-morph lineage on the reproductive success of a polymorphic and aposematic moth

Polymorphic warning signals in aposematic organisms are puzzling because efficient predator learning should select for the most efficient warning colouration. Yet, there are many examples of polymorphic and aposematic organisms in nature. Here, we investigated whether perceived trade-offs between natural and sexual selection, combined with different degrees of morph lineage admixture, can maintain polymorphic yellow and white hindwing colouration in aposematic wood tiger moth males (Arctia plantaginis). Prior research in the system suggests that yellow males have better warning colouration against predators, whereas white male morphs have higher mating success. We performed a mating experiment where females were offered four males: two white and two yellow. One male from each colour came from (purely) monomorphic lines (i.e. including the same paternal colour for multiple generations), whereas one male from each colour were from mixed-morph (or hybrid) lineages. We then assessed whether phenotype (colour), lineage, or an interaction between the two, best affected mating success. Our results showed that although white hindwing coloured males tended to have overall better reproductive success, this was mainly due to the significantly higher mating and hatching success of mixed-morph compared to pure-line individuals. Notably, this suggests the advantage of mixed-morph lineage is limited to white individuals, while on the contrary yellow mixed lineage moths have a disadvantage, i.e. the lowest mating success. The latter also suggests a cost to reproductive success in producing the more efficient against predators yellow warning colouration, even when those individuals recently descend from a white hindwing coloured lineage. Heterozygote, or hybrid advantage, even when confined to only one morph, has been shown to promote polymorphism in some systems, therefore, our results point at the need to further examine genetic architecture and the role of mixed-morph lineages in understanding the maintenance of polymorphisms in nature.     

Mate choice and the genetic basis for colour variation in a polymorphic dart frog: inferences from a wild pedigree

Understanding how reproductive barriers evolve during speciation remains an important question in evolution. Divergence in mating preferences may be a common first step in this process. The striking colour pattern diversity of strawberry dart frog (Dendrobates pumilio) populations has likely been shaped by sexual selection. Previous laboratory studies have shown that females attend to male coloration and prefer to court with males of their own colour, suggesting that divergent morphs may be reproductively isolated. To test this hypothesis, we used molecular data to estimate pedigree relationships from a polymorphic population. Whereas in the laboratory both red and yellow females preferred to court with males of their own phenotype, our pedigree shows a pattern of assortative mating only for red females. In the wild, yellow females appear to be less choosy about their mates, perhaps because they incur higher costs associated with searching than females of the more common red phenotype. We also used our pedigree to investigate the genetic basis for colour-pattern variation. The phenotype frequencies we observed were consistent with those expected if dorsal background coloration is controlled by a single locus, with complete dominance of red over yellow. Our results not only help clarify the role of sexual selection in reducing gene flow, but also shed light on the mechanisms underlying colour-pattern variation among sympatric colour morphs. The difference we observed between mating preferences measured under laboratory conditions and the pattern of mate choice observed in the wild highlight the importance of field studies for understanding behavioural reproductive isolation.     

Cryptic differences in colour among Müllerian mimics: how can the visual capacities of predators and prey shape the evolution of wing colours?

Antagonistic interactions between predators and prey often lead to co‐evolution. In the case of toxic prey, aposematic colours act as warning signals for predators and play a protective role. Evolutionary convergence in colour patterns among toxic prey evolves due to positive density‐dependent selection and the benefits of mutual resemblance in spreading the mortality cost of educating predators over a larger prey assemblage. Comimetic species evolve highly similar colour patterns, but such convergence may interfere with intraspecific signalling and recognition in the prey community, especially for species involved in polymorphic mimicry. Using spectrophotometry measures, we investigated the variation in wing coloration among comimetic butterflies from distantly related lineages. We focused on seven morphs of the polymorphic species Heliconius numata and the seven corresponding comimetic species from the genus Melinaea. Significant differences in the yellow, orange and black patches of the wing were detected between genera. Perceptions of these cryptic differences by bird and butterfly observers were then estimated using models of animal vision based on physiological data. Our results showed that the most strikingly perceived differences were obtained for the contrast of yellow against a black background. The capacity to discriminate between comimetic genera based on this colour contrast was also evaluated to be higher for butterflies than for birds, suggesting that this variation in colour, likely undetectable to birds, might be used by butterflies for distinguishing mating partners without losing the benefits of mimicry. The evolution of wing colour in mimetic butterflies might thus be shaped by the opposite selective pressures exerted by predation and species recognition.     

Clinal colour variation within a panmictic population of tree squirrels,Tamiasciurus douglasii (Rodentia: Sciuridae), across an ecological gradient

Local adaptation occurs when a population in a heterogeneous environment experiences divergent ecological selection but only if selection is stronger than the homogenizing effects of gene flow. The forest environments of Oregon vary along a physical and biotic gradient from a wet, closed‐canopy forest near the coast to a drier open‐canopy forest eastward across the Cascade Mountains. The present study explores patterns of local adaptation in Douglas squirrels (Tamiasciurus douglasii) in relation to these transitions in forest structure and ecology. We test for the presence of morphological clines in relation to gene flow and, more specifically, whether any such character clines correspond with environmental clines. We sampled animals at six locations (10 specimens each) and evaluated environmental parameters across a 240‐km west‐to‐east transect. Population structure analysis of 18 microsatellite loci indicates a single, panmictic squirrel population across the entire transect. Coalescent‐based estimates show bidirectional gene flow at similar west–east intensities between squirrels in coastal and interior forests. Of the four skull traits examined, none shows a significant clinal transition. By contrast, ventral fur colour shows a strong clinal transition, from deep‐orange in coastal forest to whitish–yellow in the interior forest. This pattern of phenotypic divergence coincides with the gradient in tree‐canopy cover. Ventral fur colour of T. douglasii exemplifies a gradation of continuous phenotypic variation maintained despite ongoing gene flow in a panmictic population. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 536–546.     

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.     

Suitability of different fluorescent powders for mass-marking the Chrysomelid, Diabrotica virgifera virgifera LeConte

Abstract:  The Western Corn Rootworm, Diabrotica virgifera virgifera LeConte (Col., Chrysomelidae), is an invasive alien pest of maize, Zea mays , in Europe. The suitability of 14 fluorescent powders for mass-marking the adults was studied in laboratory and in field cages. The visual discrimination between remaining spots of each colour on the beetles was investigated under ultraviolet (UV) light, as well as their retention time and the influences of those colours on the beetle survival and flight take-off response. The two best recognizable orange colours (i.e. of Radiant Colour and of Fiesta Colours Swada) were proposed for field experiments in first priority, followed by an orange and a yellow (both Magruder Colour), another yellow (Fiesta) and a pink (Radiant), as all did not affect beetle survival and flight take-off response and were recognizable under UV light for at least 10 days in the field. In contrast, the colours yellow and green (Radiant), red and blue (Magruder), yellow (Ciba Geigy) and pink (Fiesta) were unsuitable, because they either quickly disappeared from the beetles or adversely affected beetle survival or flight take-off response. For mass releases with differently marked beetles, only the use of a single orange colour together with a single yellow colour or the use of a pink colour together with a yellow colour can be used since few spots can clearly be discriminated from each other under UV light.     

Does colour polymorphism enhance survival of prey populations?

That colour polymorphism may protect prey populations from predation is an old but rarely tested hypothesis. We examine whether colour polymorphic populations of prey exposed to avian predators in an ecologically valid visual context were exposed to increased extinction risk compared with monomorphic populations. We made 2976 artificial pastry prey, resembling Lepidoptera larvae, in four different colours and presented them in 124 monomorphic and 124 tetramorphic populations on tree trunks and branches such that they would be exposed to predation by free-living birds, and monitored their ‘survival’. Among monomorphic populations, there was a significant effect of prey coloration on survival, confirming that coloration influenced susceptibility to visually oriented predators. Survival of polymorphic populations was inferior to that of monomorphic green populations, but did not differ significantly from monomorphic brown, yellow or red populations. Differences in survival within polymorphic populations paralleled those seen among monomorphic populations; the red morph most frequently went extinct first and the green morph most frequently survived the longest. Our findings do not support the traditional protective polymorphism hypothesis and are in conflict with those of earlier studies. As a possible explanation to our findings, we offer a competing ‘giveaway cue’ hypothesis: that polymorphic populations may include one morph that attracts the attention of predators and that polymorphic populations therefore may suffer increased predation compared with some monomorphic populations.     

The evolution of male nuptial colour in a sexually dimorphic group of fishes (Percidae: Etheostomatinae)

To test hypotheses explaining variation in elaborate male colouration across closely related species groups, ancestral‐state reconstructions and tests of phylogenetic signal and correlated evolution were used to examine the evolution of male body and fin colouration in a group of sexually dichromatic stream fishes known as darters (Percidae: Etheostomatinae). The presence or absence of red–orange and blue–green male colour traits were scored across six body regions in 99 darter species using a recently estimated amplified fragment length polymorphism (AFLP) phylogeny for comparative analyses. Ancestral‐state reconstructions infer the most recent common ancestor of darters to lack red–orange colour and possess blue–green colour on different body regions, suggesting variation between species is due to independent gains of red–orange and losses of blue–green. Colour traits exhibit substantial phylogenetic signal and are highly correlated across body regions. Comparative analyses were repeated using an alternative phylogenetic hypothesis based on one mitochondrial and two nuclear genes, yielding similar results to analyses based on the AFLP phylogeny. Red–orange colouration in darters appears to be derived; whereas, blue–green appears to be ancestral, which suggests that different selection mechanisms may be acting on these two colour classes in darters.     

Plant scents modify innate colour preference in foraging swallowtail butterflies

Flower-visiting insects exhibit innate preferences for particular colours. A previous study demonstrated that naive Papilio xuthus females prefer yellow and red, whereas males are more attracted to blue. Here, we demonstrate that the innate colour preference can be modified by olfactory stimuli in a sexually dimorphic manner. Naive P. xuthus were presented with four coloured discs: blue, green, yellow and red. The innate colour preference (i.e. the colour first landed on) of the majority of individuals was blue. When scent from essential oils of either orange flower or lily was introduced to the room, females’ tendency to select the red disc increased. Scents of lavender and flowering potted Hibiscus rosa-sinensis, however, were less effective. Interestingly, the odour of the non-flowering larval host plant, Citrus unshiu, shifted the preference to green in females. In males, however, all plant scents were less effective than in females, such that blue was always the most favoured colour. These observations indicate that interactions between visual and olfactory cues play a more prominent role in females.     

EVIDENCE FOR BATESIAN MIMICRY IN A POLYMORPHIC HOVERFLY

Palatable Batesian mimics are avoided by predators because they resemble noxious or defended species. The striking resemblance of many hoverflies to noxious Hymenoptera is a “textbook” example of Batesian mimicry, but evidence that selection by predators has shaped the evolution of hoverfly patterns is weak. We looked for geographical and temporal trends in frequencies of morphs of the polymorphic hoverfly Volucella bombylans that would support the hypothesis that these morphs are Batesian mimics of different bumblebee species. The frequency of the black and yellow hoverfly morph was significantly positively related to the frequency of black and yellow bumblebees across 52 sites. Similarly, the frequency of the red‐tailed hoverfly morph was positively related to the frequency of red‐tailed bumblebees. However, the frequencies of hoverfly morphs were positively spatially autocorrelated, and after controlling for this, only one of the two common hoverfly morphs showed a significant positive relationship with its putative model. We conclude that the distribution of V. bombylans morphs probably reflects geographical variation in selection by predators resulting from differences in the frequencies of noxious bumblebee species.     

Convergence and divergence in lizard colour polymorphisms

Colour polymorphic species are model systems for examining the evolutionary processes that generate and maintain discrete phenotypic variation in natural populations. Lizards have repeatedly evolved strikingly similar polymorphic sexual signals in distantly related lineages, providing an opportunity to examine convergence and divergence in colour polymorphism, correlated traits and associated evolutionary processes. Herein, we synthesise the extensive literature on lizard colour polymorphisms in both sexes, including recent advances in understanding of the underlying biochemical, cellular and genetic mechanisms, and correlated behavioural, physiological and life-history traits. Male throat, head or ventral colour morphs generally consist of red/orange, yellow and white/blue morphs, and sometimes mixed morphs with combinations of two colours. Despite these convergent phenotypes, there is marked divergence in correlated behavioural, physiological and life-history traits. We discuss the need for coherence in morph classification, particularly in relation to ‘mixed’ morphs. We highlight future research directions such as the genetic basis of convergent phenotypes and the role of environmental variation in the maintenance of polymorphism. Research in this very active field promises to continue to provide novel insights with broad significance to evolutionary biologists.     

Territory acquisition in a polymorphic lizard: An experimental approach

Males of the colour polymorphic Australian painted dragon lizard Ctenophorus pictus occur in red or yellow head colouration. In a previous experiment, we showed that red is associated with a higher probability of winning staged contests for resources (females or space) and that manipulation of male colouration by painting males in the opposing morph changed the dynamics of staged interactions by prolonging them 30‐fold. Thus, colour is linked to behavioural differences between males and is involved in information transfer between competing males. This inherent red dominance could result in yellow males being marginalized to poorer quality territories in terms of access to females, food, perch sites or shade. With an experiment in the wild, we test to what extent this prediction is upheld, and how colour manipulation affects morph‐specific success in territory acquisition when male body size, territory quality and emergence time from hibernation are controlled through manipulation or randomization. There was no significant effect of colour category per se, although on average red males remained closer to the release sites (our proxy for territory acquisition ability) than yellow males and artificially altered morphs moved the furthest away. There was a significant interaction effect between colour category and experimental release position, which may be linked to differences in how exposed (or not) these positions were and morph‐specific ability to cope with such exposure (e.g. ‘boldness’). Our data show that territory acquisition success is not merely a function of competitive ability but a composite outcome of a suite of factors, including signal perception.     

Fruit colour polymorphism in Acacia ligulata: seed and seedling performance, clinal patterns, and chemical variation

Fruit colour polymorphisms are widespread in nature, but their ecological and evolutionary dynamics remain poorly understood. Here we examine Acacia ligulata, a shrub of the Australian arid zone which exhibits a red/orange/yellow aril colour polymorphism. We asked whether the polymorphism had a genetic basis; whether selection acted differentially on morphs during the seed and seedling stages; whether geographic variation in morph frequencies was correlated with environmental factors; and whether morphs differed in physical or chemical characteristics that might influence selection on them. When grown to maturity in a common greenhouse environment, maternal families of seeds showed phenotypic patterns consistent with biparental genetic control of the polymorphism. In contrast to other fruit-colour polymorphic species, progeny of A. ligulata morphs did not vary in rates of seedling emergence or survival in a common garden. Sampling along a 580 km transect revealed clinal variation in morph frequencies. Frequencies of the yellow morph decreased, and frequencies of the red morph increased, across a gradient of decreasing temperature and increasing rainfall. Morphs did not differ in seed mass, aril mass, or in profiles of fatty acids and flavonoids in either arils or seeds. However, morphs showed consistent differences in carotenoid profiles' and elemental content of arils, suggesting that selection by avian and insect seed dispersers, seed predators and herbivores should be investigated. These patterns indicate that both abiotic and biotic factors may contribute to selection on the A. ligulata polymorphism. This revised version was published online in August 2006 with corrections to the Cover Date.     

Frequency-dependent reproductive success in female common lizards: a real-life hawk–dove–bully game?

Alternative strategies are characterised by context-dependent fitness payoffs, which means that their fitness depends on the frequency and the nature of their interactions with one or more strategies. The analysis of the variation of the fitness of each strategy in different social environments can elucidate the evolutionary dynamics played by the strategies. In the common lizard, three female colour types (yellow, orange and mixed) are associated with alternative reaction norms in reproduction and social behaviour that signal alternative strategies. To clarify the nature of colour-specific interactions and their influence on female fitness, we analysed the response of female reproductive success to an experimental manipulation of colour frequencies in natural populations. We found that juvenile body condition at birth for all colour types was negatively affected by the local frequency of yellow females. In addition, we found that mixed females had higher clutch hatching success in the populations where orange females were frequent. These results prove that female reproduction is sensitive to the social environment, and are consistent with a scenario of a hawk–dove–bully game, in which yellow females are aggressive hawks, orange females non-aggressive doves, and mixed females have a context-dependent bully strategy. In this system, the plastic bully strategy would confer a reproductive advantage to putative heterozygotes in some social environments, which could allow the maintenance of the system through context-dependent overdominance effects.     

Too big for his boots: Are social costs keeping condition‐dependent status signalling honest in an Australian lizard?

Australian painted dragon lizards Ctenophorus pictus occur in three head colours (red, orange and yellow) that differ in their level of aggression (reds being most aggressive), hormone profile (reds having higher testosterone levels) and in their frequency in our study population over time. They are also polymorphic in bib colour; some males have a bright yellow area under the chin, while others lack this coloured area entirely. We show that red males with a bib are in better body condition than red males that lack a bib. This contrasts sharply to yellow males, in which males with a bib are in poorer condition than yellow males that lack a bib. Our analysis also shows that following exposure to a high percentage of red (more aggressive) neighbours, all males suffer a reduction in body condition, and importantly, males with a bib (regardless of their head colour) suffer a more severe loss of body condition than males that lack a bib. Finally, this condition loss is significantly higher for yellow bibbed males than for red bibbed males, suggesting that the cost of sporting a bib may be higher for them. Orange males showed a non‐significant difference in condition between bib morphs. Our analysis also shows that bibbed yellow males (the morph with lower body condition), but no other morph category, declined significantly in their frequency between 2 years.