One cost of being gold: selective predation and implications for the maintenance of the Midas cichlid colour polymorphism (Perciformes: Cichlidae)

In the colour‐polymorphic Midas cichlid fish species complex (Amphilophus citrinellus spp.), gold morphs occur at much lower frequencies (< 10%) than dark individuals. This might be surprising because gold coloration is dominant and coded for by a single Mendelian locus. Furthermore, gold individuals are considered to be competitively advantaged over dark ones because they grow faster and win aggressive encounters more often compared to dark individuals of equal size. However, one might expect a cost of being gold in terms of natural selection as a result of predation. We tested whether the Jaguar cichlid (Parachromis managuensis), a major fish predator of Midas cichlids, preys differentially on colour variants of goldfish (Carassius auratus auratus), which were used as a proxy for Midas cichlids because of their similarity in colour. Size‐matched pairs of prey fish (gold and dark) were offered to the predator and the time until the fish were attacked was recorded. The gold morph was attacked first more often (approximately 70%) but not faster than the dark morph. This suggests that the predator perceives the gold individual first, and/or that the predator exhibits a preference or higher motivation to attack the gold prey fish. The increased risk of predation of gold prey fish suggests for the Midas cichlid system that being gold may carry significant costs in terms of natural selection as a result of its major piscivorous predator. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 350–358.     

Differential predation on colour morphs of the Midas cichlid, Cichlasoma citrinellum

Predation has often been invoked as a selective agent affecting colour patterns in a wide range of organisms, but data relating susceptibility to predation and objective measures of conspicuousness are rare. To investigate relative crypticity in free-swimming fishes, two colour morphs of the Midas cichlid were exposed to predation by largemouth bass, Micropterus salmoides. The two colour morphs, normal and amelanic golds, were viewed by predators in ponds against a uniform, natural background. Swimming pools, 4 m in diameter, were stocked with equal numbers of gold and normal juvenile Midas cichlids. Bass took a significantly higher proportion of normal-coloured fishes (69·2% of fish) than gold morphs overall, and in a significantly higher proportion of trials (68·8% of experiments). No differences were found between colour morphs in their behaviour or in the willingness of bass to attack either morph. The significance of these results are discussed in relation to the visual system of the predator and the relative conspicuousness of the prey colour patterns.     

Background matching ability and the maintenance of a colour polymorphism in the red devil cichlid

The evolution and maintenance of colour polymorphisms remains a topic of considerable research interest. One key mechanism thought to contribute to the coexistence of different colour morphs is a bias in how conspicuous they are to visual predators. Although individuals of many species camouflage themselves against their background to avoid predation, differently coloured individuals within a species may vary in their capacity to do so. However, to date, very few studies have explicitly investigated the ability of different colour morphs to plastically adjust their colouration to match their background. The red devil (Amphilophus labiatus) is a Neotropical cichlid fish with a stable colour polymorphism, with the gold morph being genetically dominant and having a myriad of documented advantages over the dark morph. However, gold individuals are much rarer, which may be related to their heightened conspicuousness to would‐be predators. Here, we tested the ability of differently coloured individuals to phenotypically adjust the shade of their body colour and patterns to match their background. In particular, we filmed dark, gold and mottled (a transitioning phase from dark to gold) individuals under an identical set‐up on light vs. dark‐coloured substrates. We found that, in contrast to individuals of the dark morph, gold and mottled individuals were less capable of matching their body colouration to their background. As a result, gold individuals appeared to be more conspicuous. These results suggest that a difference in background matching ability could play an important role in the maintenance of colour polymorphisms.     

Reproductive success and risk of predation in normal and melanistic colour morphs of the adder, Vipera berus

In a population of adders (Vipera berus) in Southwest Sweden, melanistic males were heavier than normal coloured males of the same length. Victory in male-male sexual combats was positively related to size. Higher risk of predation in the black morph was inferred from experiments showing a high predator attack rate on models of the black morph. Even the bright colour in newly moulted basking males of the normal morph gives cryptic protection. In females, melanism probably also affects body size and risk of predation by visually searching predators. The thermoregulatory influence of black colour, the reproductive success and the maintenance of two colour morphs in the population are discussed.     

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.     

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.     

Prey selection by wild birds can allow novel and conspicuous colour morphs to spread in prey populations

Conspicuous warning coloration helps to protect prey because it signals to potential predators that the prey is unprofitable. However, such signals only work once predators have come to associate the conspicuous colour with the unprofitability of the prey. The evolution of warning coloration is generally considered to be paradoxical, because it has traditionally been assumed that the first brightly coloured individuals would be at an immediate selective disadvantage because of their greater conspicuousness to predators that are naïve to the meaning of the signal. As a result, it has been difficult to understand how a novel conspicuous colour morph could ever avoid rapid extinction, and instead survive and spread in the population until predators have become educated about the signal. In the present study, we experimentally simulated the appearance of a single novel coloured mutant in small populations (20 individuals) of palatable artificial pastry "prey". The colour morph frequencies in each "generation" of prey (presented on successive days of a trial) were determined by the relative survival of the previous generation under predation by free-living birds. We found that the novel colour morphs regularly persisted and increased from a starting frequency of 1/20 to reach fixation (100%), despite being fully palatable, even when the novel morph was much more conspicuous against the background than the familiar morph. This was true for both green (not normally considered a warning colour) and red (a classic warning colour) novel morphs. Novel colours reached fixation significantly faster than could be accounted for by random drift, indicating differential predation in relation to prey colour by the birds. Our experiments show that the immediate demise of a fully palatable new prey morph is not an inevitable outcome of predator behaviour, because even very conspicuous prey can gain protection from conservative foragers, simply by being novel.     

Female‐limited colour polymorphism in the crab spider Synema globosum (Araneae: Thomisidae)

Conspicuous colour variation, caused by the influence of the environment on phenotype or by genetic differences among individuals, is frequently observed in nature. If genetic in origin, colour variation can facilitate the study of mechanisms that contribute to the maintenance of true polymorphisms. Here we describe, for the first time, the female‐limited colour polymorphism in the crab spider, Synema globosum. We looked for associations between life‐history traits and female colour morph, and identified potential agents of selection that could influence the maintenance of the polymorphism. Our results showed that the polymorphism is discrete and heritable, and that differences in colour among morphs are likely to be detectable by honeybees, birds, and conspecifics. We found limited evidence of differences among morphs in morphology and ecology, and found no differences in components of reproduction. Based on the lines of evidence obtained in this study, we suggest that selection exerted by prey, predators, and/or mates is likely to influence the maintenance of the polymorphism observed in S. globosum. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 368–383.     

Dietary conservatism may facilitate the initial evolution of aposematism

It has generally been assumed that warningly coloured organisms pay a cost associated with their increased visibility, because naïve predators notice and eat them. This cost is offset by their enhanced protection from educated predators who associate the colour pattern with unprofitability. However, some studies have suggested that avoidance of novel prey by avian predators ("dietary conservatism") can actually place novel colour morphs at a selective advantage over familiar ones, even when they are highly conspicuous. To test this idea, we experimentally simulated the appearance of a single novel-coloured mutant in small populations (20 individuals) of palatable artificial prey. The colour morph frequencies in each "generation" were determined by the relative survival of the previous generation under predation by birds. We used wild-caught European robins Erithacus rubecula foraging on pastry "prey" of different colours. The aim was to test whether prey selection by predators prevented or facilitated the novel colour morph persisting in the prey population over successive generations. We found that the novel colour morph quickly increased to fixation in 14/40 prey "populations", and at least once each in 8 of the 10 birds tested. Novel mutants of the classic aposematic colours (red and yellow) reached fixation most frequently, but even the green and blue novel morphs both increased to fixation in 2/40 trials. Novel colours reached fixation significantly faster than could be accounted for by drift, indicating active avoidance by the birds. These results suggest that a novel colour morph arising in a prey population can persist and increase under the selective pressure imposed by predators, even to the local exclusion of the original morph, despite being fully palatable. The consequences of this finding are discussed in relation to receiver psychology, the evolution of aposematism and the existence of polymorphism in Müllerian mimics.     

The interplay between multiple predators and prey colour divergence

Evolutionary divergence in the coloration of toxic prey is expected when geographic variation in predator composition and behavior favours shifts in prey conspicuousness. A fundamental prediction of predator‐driven colour divergence is that the local coloration should experience lower predation risk than novel prey phenotypes. The dorsal coloration of the granular poison frog varies gradually from populations of conspicuous bright red frogs to populations of dull green and relatively cryptic frogs. We conducted experiments with clay models in four populations to examine the geographic patterns of taxon‐specific predation. Birds avoided the local phenotype while lizards consistently selected for decreased conspicuousness and crab predation did not depend on frog coloration. Importantly, birds and lizards favoured low conspicuousness in populations where relatively cryptic green morphs have evolved. This study provides evidence for the interplay among distinct selective pressures, from multiple‐predator taxa, acting on the divergence in protective coloration of prey species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 580–589.