Gold Morphs Research Articles

The role of rare morph advantage and conspicuousness in the stable gold-dark colour polymorphism of a crater lake Midas cichlid fish.

Genetically based stable colour polymorphisms provide a unique opportunity to study the evolutionary processes that preserve genetic variability in the wild. Different mechanisms are proposed to promote the stability of polymorphisms, but only few empirical examples have been documented, resulting in an incomplete understanding of these mechanisms. A remarkable genetically determined stable colour polymorphism is found in the Nicaraguan Midas cichlid species complex (Amphilophus cf. citrinellus). All Midas cichlids start their life with a dark-grey coloration (dark morph), but individuals carrying the dominant "gold" allele (c. 10%) lose their melanophores later in life, revealing the underlying orange coloration (gold morph). How this polymorphism is maintained remains unclear. Two main hypotheses have been proposed, both suggesting differential predation upon colour morphs as the proximate mechanism. One predicts that the conspicuous gold morph is more likely to be preyed upon, but this disadvantage is balanced by their competitive dominance over the dark morph. The second hypothesis suggests a rare morph advantage where the rarer gold morph experiences less predation. Empirical evidence for either of these mechanisms is still circumstantial and inconclusive. We conducted two field experiments in a Nicaraguan crater lake using wax models simulating both morphs to determine predation pressure upon Midas cichlid colour morphs. First, we tested the interaction of coloration and depth on attack rate. Second, we tested the interaction of fish size and coloration. We contrasted the pattern of attacks from these experiments to the predicted predation patterns from the hypotheses proposed to explain the colour polymorphism's stability. Large models imitating colour morphs were attacked at similar rates irrespectively of their position in the water column. Yet, attacks upon small models resembling juveniles were directed mainly towards dark models. This resulted in a significant size-by-colour interaction. We suggest that gold Midas cichlids experience a rare morph advantage as juveniles when individuals of this morph are extremely uncommon. But this effect is reduced or disappears among adults, where gold individuals are relatively more common. Thus, the interaction of rare morph advantage and conspicuousness, rather than either of those factors alone, is a likely mechanism resulting in the stability of the colour polymorphism in Midas cichlids.

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.

Genetic Control of Color Polymorphism in the Stag Beetle Cyclommatus metallifer Boisduval (Coleoptera: Lucanidae)

Abstract We describe the genetic control of body color polymorphism in the metallic stag beetle, Cyclommatus metallifer Boisduval. As with many species of sexually dimorphic stag beetles, male C. metallifer exhibit condition-dependent exaggerated growth of mandibles. Another characteristic of this species is that two body colors have been described from both wild and captive bred populations. The two body colors are a commonly observed gold and a more rare black. We performed a simple Mendelian cross of individuals from families that produced only gold offspring to individuals from families that produced only blue-black offspring. All of the F1 hybrid progeny between these two pure gold families and pure black families exhibited the gold body color. The F2 progeny resulting from the crossing of F1 hybrids exhibited a 3:1 gold to black ratio. The backcross of the F1 hybrid to the gold morph resulted in 1:0 gold to black ratio. The backcross of the F1 hybrid to the black morph resulted in progeny with a 1:1...

All that glitters is not gold: different anti-predatory behavior of two color morphs of goldfish (Carassius auratus)

The foraging behavioral responses of individuals from two color morphs of the common goldfish (Carassius auratus) to a foraging predator, the little egret (Egretta garzetta) were tested in two artificial theaters, each containing three fish ponds. Each pond contained two distinct microhabitats for the fish: 1. A safe microhabitat: a sheltered area under an opaque cover at the center of the pool providing a refuge but no food. 2. A risky microhabitat: the rest of the pool area, where the fish could feed but were exposed to predation by egrets. This experimental design forced the goldfish to trade off food and safety, and to manage risk via time allocation to each microhabitat. The foraging behavioral responses of the gold variant and the bronze variant goldfish, one morph at a time, were quantified. In the presence of an egret, bronze morph fish spent significantly more time out of cover and more fish emerged from under the cover at any given time than did the gold morph fish. Despite the greater exposure of bronze morph fish, they were captured significantly less often by the egrets. These findings strongly suggest that differently colored fish may perceive predation risk differently, trade off food and safety differently, and may have different susceptibility to predators. Our results show that color variation in goldfish may affect both foraging behavior and anti-predatory behavior.

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.

Genetic, Comparative Genomic, and Expression Analyses of the Mc1r Locus in the Polychromatic Midas Cichlid Fish (Teleostei, Cichlidae Amphilophus sp.) Species Group

Natural populations of the Midas cichlid species in several different crater lakes in Nicaragua exhibit a conspicuous color polymorphism. Most individuals are dark and the remaining have a gold coloration. The color morphs mate assortatively and sympatric population differentiation has been shown based on neutral molecular data. We investigated the color polymorphism using segregation analysis and a candidate gene approach. The segregation patterns observed in a mapping cross between a gold and a dark individual were consistent with a single dominant gene as a cause of the gold phenotype. This suggests that a simple genetic architecture underlies some of the speciation events in the Midas cichlids. We compared the expression levels of several candidate color genes Mc1r, Ednrb1, Slc45a2, and Tfap1a between the color morphs. Mc1r was found to be up regulated in the gold morph. Given its widespread association in color evolution and role on melanin synthesis, the Mc1r locus was further investigated using sequences derived from a genomic library. Comparative analysis revealed conserved synteny in relation to the majority of teleosts and highlighted several previously unidentified conserved non-coding elements (CNEs) in the upstream and downstream regions in the vicinity of Mc1r. The identification of the CNEs regions allowed the comparison of sequences from gold and dark specimens of natural populations. No polymorphisms were found between in the population sample and Mc1r showed no linkage to the gold phenotype in the mapping cross, demonstrating that it is not causally related to the color polymorphism in the Midas cichlid.

Testing the Carotenoid Trade‐Off Hypothesis in the Polychromatic Midas Cichlid, Amphilophus citrinellus

Many animals use carotenoid pigments derived from their diet for coloration and immunity. The carotenoid trade-off hypothesis predicts that, under conditions of carotenoid scarcity, individuals may be forced to allocate limited carotenoids to either coloration or immunity. In polychromatic species, the pattern of allocation may differ among individuals. We tested the carotenoid trade-off hypothesis in the Midas cichlid, Amphilophus citrinellus, a species with two ontogenetic color morphs, barred and gold, the latter of which is the result of carotenoid expression. We performed a diet-supplementation experiment in which cichlids of both color morphs were assigned to one of two diet treatments that differed only in carotenoid content (beta-carotene, lutein, and zeaxanthin). We measured integument color using spectrometry, quantified carotenoid concentrations in tissue and plasma, and assessed innate immunity using lysozyme activity and alternative complement pathway assays. In both color morphs, dietary carotenoid supplementation elevated plasma carotenoid circulation but failed to affect skin coloration. Consistent with observable differences in integument coloration, we found that gold fish sequestered more carotenoids in skin tissue than barred fish, but barred fish had higher concentrations of carotenoids in plasma than gold fish. Neither measure of innate immunity differed between gold and barred fish, or as a function of dietary carotenoid supplementation. Lysozyme activity, but not complement activity, was strongly affected by body condition. Our data show that a diet low in carotenoids is sufficient to maintain both coloration and innate immunity in Midas cichlids. Our data also suggest that the developmental transition from the barred to gold morph is not accompanied by a decrease in innate immunity in this species.

COLOR ASSORTATIVE MATING CONTRIBUTES TO SYMPATRIC DIVERGENCE OF NEOTROPICAL CICHLID FISH

It is still debated vigorously whether sexual selection can result in speciation without physical barriers to gene flow. In this study, we used field data and molecular methods to investigate the gold-normal color polymorphism in two endemic cichlid fish species of crater lake Xiloá, Nicaragua. We found significant assortative mating by color in both Amphilophus xiloaensis and A. sagittae. Focusing on A. xiloaensis, microsatellite allele frequencies, an assignment test, and model-based cluster analysis demonstrates significant and clear genetic differentiation (F(ST)= 0.03) between gold and normal individuals in sympatry. In addition, we find genetic differentiation between all three sympatric and ecologically distinct Midas cichlid species of Lake Xiloá, A. amarillo, A. sagittae, and A. xiloaensis (F(ST)= 0.03 - 0.19), and clear genetic isolation of these species from their closest relative (A. citrinellus) in the neighboring great lake Managua. The A. xiloaensis gold morph is genetically more distinct from the lake's other two Midas cichlid species than is A. xiloaensis-normal. Thus, we have identified sexual isolation based on color that is evident in population genetics and mate choice. Our results suggest that sexual selection through color assortative mating may play an important role in incipient sympatric speciation in Midas cichlids of Nicaragua.

Sexual-Selection Models for Exaggerated Traits are Useful but Constraining

SYNOPSIS. Science is driven by productive hypotheses and technology, but these may sometimes limit the questions posed. For instance, Fisherian runaway sexual selection and related hypotheses have helped us understand the evolution of exaggerated visual sexual dimorphism. Species with indistinguishable sexes, however, may use different behavioral mechanisms when pairing and thus possess different adaptations. In the monomorphic Midas cichlid ( Amphilophus citrinellum ), females chose large aggressive males in a restrained situation, as sexual selection predicts, but males did not choose. The nuchal hump of males swells coincidently with pair formation. However, overly large humps were shunned by females while the normal— size hump facilitated sex recognition. This species is polychromatic, and pairs mate assortatively by color in Nicaragua. Some have suggested the Midas cichlid might therefore show how sexual selection produces explosive speciation of cichlids in Africa. All females, however, are biased toward normal—color males. The color of gold morphs modulates aggressive responses of the other fish. All else equal, the benefit to gold in a fight equals 15% more weight than the opponent. Pair formation succeeds best when the typically smaller female of a pair is relatively more aggressive than the male. The pair combination, gold male with normal female, is difficult to produce; making the female the same size as the male removes the disability. Pair formation is a negotiated process in which the male tests the aggressiveness of the female relative to self. That puts the behavioral mechanisms of the male and female in conflict.

Large body size in the pygmy swordtail Xiphophorus pygmaeus

Fishes in the genus Xiphophorus (swordtails and platyfishes) are well known for the influence of the pituitary (P) locus on variation of male size at maturity both within and among species. We report the discovery of large male size ( >29 mm SL) in several populations of the swordtail X. pygmaeus, a species previously thought to consist of only small males (<29 mm SL). Large size is geographically restricted, and average male size varies significantly by site and year sampled in a pattern suggesting a recent origin and slow spreading of the large male phenotype. However, large male size is not strongly patternally inherited in this species, as it is in its two closest relatives, X. nigrensis and X. multilineatus, showing that large size does not result from the same genetic (P locus) mechanism. Large X. pygmaeus males do not court, can exhibit the gold morph, do not possess swords and have slender body shape. In these traits they resemble small conspecific males and small males of X. nigrensis and X. multilineatus rather than large males of these latter two species. This shows that correlations between morphological and behavioural traits that occur in X. nigrensis and X. multilineatus are absent in X. pygmaeus.

Large body size in the pygmy swordtail Xiphophorus pygmaeus

Fishes in the genus Xiphophorus (swordtails and platyfishes) are well known for the influence of the pituitary ( P) locus on variation of male size at maturity both within and among species. We report the discovery of large male size ( >29 mm SL) in several populations of the swordtail X. pygmaeus, a species previously thought to consist of only small males (<29 mm SL). Large size is geographically restricted, and average male size varies significantly by site and year sampled in a pattern suggesting a recent origin and slow spreading of the large male phenotype. However, large male size is not strongly patternally inherited in this species, as it is in its two closest relatives, X. nigrensis and X. multilineatus, showing that large size does not result from the same genetic ( P locus) mechanism. Large X. pygmaeus males do not court, can exhibit the gold morph, do not possess swords and have slender body shape. In these traits they resemble small conspecific males and small males of X. nigrensis and X. multilineatus rather than large males of these latter two species. This shows that correlations between morphological and behavioural traits that occur in X. nigrensis and X. multilineatus are absent in X. pygmaeus.

Polychromatic Midas Cichlids Respond To Dummy Opponents: Color, Contrast and Context

Dummies allow the analysis of the effects of striking visual traits free of the confounding variation and interaction seen in live stimuli. In the Midas cichlid ('Cichlasoma' citrinellum), gold morphs (G) dominate normal (N) ones, apparently because an all-gold fish is a 'supernormal releaser' of fear. Although in other fish a dummy that looks like a territory holder or a dominant individual usually evokes the most aggressive response, we wondered whether the gold color was special and would depress aggressiveness. If so, when shown four differently colored passive dummies, gold ones would be approached and attacked least. The other three colors, all naturally occurring, were gray, white and black. Based on earlier, indirect evidence, we predicted that the N and G subjects would not differ in their responses, nor would males and females. We found that gold dummies were attacked at the highest rate, not the lowest, but all dummies were approached about equally. G and N subjects did not differ, nor did males and females based on attack rates. Females, however, spent more time close to the dummies than did males, possibly prospecting for a mate. To 'calibrate' the responses, we then presented to male subjects dummies colored gold, gray, and two novel colors, green and blue. The dummies were attacked from most to least in that order. The novel colors produced greater differences in responses than did colors normally found in the Midas cichlid. Other tests using dummies altered the position of the gold patch that is normally found on the throat, eye color, eye position, proportion of body colored gold, and species-typical markings; a patch of gold covering just the face was particularly evocative. The response to G may depend on whether the encounter is symmetrical or asymmetrical. Gold and gray dummies that threatened back were alternated with passive ones of the same color. Reactive gold and gray dummies were attacked at the highest rates and about equally; they were approached less than were the passive dummies, however. The results of testing with dummies can produce contrary results depending on whether the dummy is reactive or passive, and on the color of the background.

Unsuspected cryptic polymorphism in the polychromatic Midas cichlid

The Midas cichlid (Cichlasoma citrinellum) of Nicaragua shows stable polychromatism in that a consistent, small proportion of the fish in nature lose their melanophores and thereby become gold-coloured. Before metamorphosis, all fish look alike. We asked whether the pre-transformed offspring of gold and normal morphs might differ in their morphological and physiological responses to white and to black backgrounds despite looking the same. More chromatophores developed in all juveniles exposed for two weeks to a black than to a white background. When moved from one background to the other, the fish adjusted to white faster than to black. Most importantly, genetically normal fish (N) colour-matched quicker than genetically gold fish (G) irrespective of the direction of change. Adjustment in G was also more variable, indicating poorer control. A parallel pattern was recorded photometrically in melanophores of excised scales: aggregation of pigment was faster than dispersion. And pigment in the melanophores of N aggregated and dispersed swifter than did those of G. Therefore, pre-metamorphosed juvenile G could be more vulnerable to predation than are juvenile N. This reveals a possible source of selection against the offspring of gold morphs before they become gold-coloured.

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.

Unmasking affiliative behavior among juvenile Midas cichlids (Cichlasoma citrinellum).

Adults of the Midas cichlid (Cichlasoma citrinellum) are predominantly normal-colored (N) morphs, although 8% in nature are gold (G) morphs. They tend to mate assortatively by color; that behavior may be influenced by prior experience with parents or siblings or by their own color. A previous experiment indicated that juveniles respond according to a rule that they avoid and behave defensively toward G juveniles and that they consort with and behave aggressively toward N juveniles (Barlow & Siri, 1987). The fear-provoking effect of G may have interfered with more subtle aspects of choice because the 4 treatment fish in each group reacted through the glass barrier to the approach of the subject. In the present experiment such feedback was eliminated by using one-way mirrors. N juveniles reared by normal parents (N X N) differentiated between N and G treatment fish only in that they attacked significantly more toward G; thus their behavior was contrary to that predicted by the fear-provoking effect of gold. The notable effect among juveniles reared by G parents (G X G) was that N spent more time with N and avoided G treatment fish, in keeping with the fear-provoking effect of gold. The results are discussed in terms of the differences in experiences between juveniles reared N X N, all of which were themselves N, and those reared G X G, consisting of both color morphs. Despite the differences in the two experiments, the main conclusion remains in place: Affiliative responses of juveniles, as measured in these tests, do not predict choice of mate among adults.

Do gold Midas cichlid fish win fights because of their color, or because they lack normal coloration?

Gold morphs (G) of the polychromatic Midas cichlid, Cichlasoma citrinellum, dominate those of normal coloration (N). The adults vary greatly in weight because they continue to grow after reaching sexual maturity; relative weight is an important determinant of dominance. The first objective here was to characterize dominance in relation to color and to relative size by staging a large number of encounters between fish of various weights. Logistic curves were fitted to the data to analyze the relationship between relative size and winning. The baseline curves for N vs N and G vs G (Fig. 1, Table 1) did not differ (Table 2). The shape of the curve for N vs G also was not different from that of the baseline curves. But the curve for N vs G was shifted such that N must weigh 116% of G for the probability of winning to be 0.50.

A Comparison of Feeding, Spacing, and Aggression in Color Morphs of the Midas Cichlid. Ii. After 24 Hours Without Food

We set out to test three hypotheses: (1) Gold Effect - the coloration of the gold morph confers an advantage in hostile interactions because that color inhibits aggression. (2) Habituation Effect - fish habituate to gold fish if they are encountered frequently. (3) Dominance-Generalization Effect - the color of the dominant fish is learned, and small fish who share that color receive some protection from attacks. The basic experiment consisted of one large juvenile dominating a feeder which was approached by small fish, 3 golds and 3 normals. In the treatment, the feeder was removed for 24 hr then replaced 20 min before recording; this was done to see if the Gold Effect would prevail over the Habituation Effect under conditions of forced competition. Contrary to expectations, the large fish attacked the small golds more than the small normals. However, their attacks could have been evoked by the attacks or feeding behavior of the small fish. The small fish themselves showed both the Gold and Dominance-Generalization Effects. And, as predicted, the Gold Effect prevailed over the Habituation Effect after being deprived of food; but the same thing happened in the control situation, apparently due to the stimulation of revealing concealed worms when their feeder was simply lifted and immediately replaced. The small golds appeared to feed more often than the small normals, but the difference was not significant. However, the small golds gained significantly more weight than did the small normals. Thus the small golds benefited more from their aggressive advantage over the small normals than they lost by being attacked more by the large dominant fish.

Seasonality in habitat selection by the gold color morph of Cichlasoma citrinellum and its relevance to sympatric speciation in the family Cichlidae

Cichlasoma citrinellum is a polymorphic species whose individual coloration varies from the dark grey markings typical of the species to yellow, orange, and red. In Lake Jiloa, Nicaragua the depth distribution of these latter, nongrey, golden morphs shows dramatic seasonal variation. In the height of the dry season in February over 50% of the gold morphs occur above 9 m, but as the breeding season approaches they migrate deeper such that less than 7% of the gold population occurs above 9 m at the onset of the breeding season. During the rainy season when breeding occurs most of the gold morphs occur below 15 m. It appears that gold morphs ‘voluntarily’ move into deeper water to breed rather than being aggressively forced deeper by larger, territorial grey morphs as was implied in an earlier paper (McKaye & Barlow 1976). Since the morphs of this species assortatively mate and select different habitats in which to breed, future sympatric splitting of this species is possible. Likely examples of sympatric speciation and of incipient speciation in the family Cichlidae are discussed.

Colour and levels of aggression in the midas cichlid

Previous work established that gold morphs of the Midas cichlid ( Cichlasoma citrinellum) dominate normal ones of about the same size. Left unresolved, however, was whether the gold morphs dominate because they are inherently more aggressive or because the gold colour inhibits aggression. The issue was clarified here by comparing levels of aggression within groups of golds only, normals only, and golds plus normals. At first the groups of golds were the least aggressive. But 2 days later the levels of aggression in the other groups fell to about that of the golds. We conclude therefore that the gold colour inhibits attack, but that this effect is only discernible in groups when they are establishing inter-individual relationships disappearing when the groups stabilize. We suggest that gold coloration inhibits attacking by stimulating fear responses.

Predicting and assessing dominance from size and coloration in the polychromatic midas cichlid

To test whether gold morphs dominate normal ones, twelve groups were observed, each consisting of three golds and three normals paired by weight. Golds dominated comparable normals. Smaller golds also profited from sharing the colour of the dominant fish. Contest and approach declined across days, but attack and yield remained high. Standard deviation of rank was progressively greater with higher rank, but uncertainty of rank plotted as an inverted U. Behaviours important in dominance showed high dependence on type of fish but low dependence on day; these behaviours also had more variation attributable to the coloration factor. From a set of stated criteria, dominance is deemed best assessed here by an index: (attacks) ļo (yields + attacks); contesting (threat) is actually misleading.