Variation in the Visual Habitat May Mediate the Maintenance of Color Polymorphism in a Poeciliid Fish

The conspicuousness of animal signals is influenced by their contrast against the background. As such, signal conspicuousness will tend to vary in nature because habitats are composed of a mosaic of backgrounds. Variation in attractiveness could result in variation in conspecific mate choice and risk of predation, which, in turn, may create opportunities for balancing selection to maintain distinct polymorphisms. We quantified male coloration, the absorbance spectrum of visual pigments and the photic environment of Poecilia parae, a fish species with five distinct male color morphs: a drab (i.e., grey), a striped, and three colorful (i.e., blue, red and yellow) morphs. Then, using physiological models, we assessed how male color patterns can be perceived in their natural visual habitats by conspecific females and a common cichlid predator, Aequidens tetramerus. Our estimates of chromatic and luminance contrasts suggest that the three most colorful morphs were consistently the most conspicuous across all habitats. However, variation in the visual background resulted in variation in which morph was the most conspicuous to females at each locality. Likewise, the most colorful morphs were the most conspicuous morphs to cichlid predators. If females are able to discriminate between conspicuous prospective mates and those preferred males are also more vulnerable to predation, variable visual habitats could influence the direction and strength of natural and sexual selection, thereby allowing for the persistence of color polymorphisms in natural environments.     

Intrasexual competition among females and the stabilization of a conspicuous colour polymorphism in a Lake Victoria cichlid fish

The maintenance of colour polymorphisms within populations has been a long-standing interest in evolutionary ecology. African cichlid fish contain some of the most striking known cases of this phenomenon. Intrasexual selection can be negative frequency dependent when males bias aggression towards phenotypically similar rivals, stabilizing male colour polymorphisms. We propose that where females are territorial and competitive, aggression biases in females may also promote coexistence of female morphs. We studied a polymorphic population of the cichlid fish Neochromis omnicaeruleus from Lake Victoria, in which three distinct female colour morphs coexist: one plain brown and two blotched morphs. Using simulated intruder choice tests in the laboratory, we show that wild-caught females of each morph bias aggression towards females of their own morph, suggesting that females of all three morphs may have an advantage when their morph is locally the least abundant. This mechanism may contribute to the establishment and stabilization of colour polymorphisms. Next, by crossing the morphs, we generated sisters belonging to different colour morphs. We find no sign of aggression bias in these sisters, making pleiotropy unlikely to explain the association between colour and aggression bias in wild fish, which is maintained in the face of gene flow. We conclude that female-female aggression may be one important force for stabilizing colour polymorphism in cichlid fish.     

Variation in founder groups promotes establishment success in the wild

Environmental changes currently pose severe threats to biodiversity, and reintroductions and translocations are increasingly used to protect declining populations and species from extinction. Theory predicts that establishment success should be higher for more variable groups of dissimilar individuals. To test this 'diversity promotes establishment' hypothesis, we introduced colour polymorphic pygmy grasshoppers (Tetrix subulata) to different sites in the wild. The number of descendants found at the release sites the subsequent year increased with increasing number of colour morphs in the founder group, and variation in founder groups also positively affected colour morph diversity in the established populations. Since colour morphs differ in morphology, physiology, behaviour, reproductive life history and types of niche used, these findings demonstrate that variation among individuals in functionally important traits promotes establishment success under natural conditions, and further indicate that founder diversity may contribute to evolutionary rescue and increased population persistence.     

Color polymorphic lures target different visual channels in prey

Selection for signal efficacy in variable environments may favor color polymorphism, but little is known about this possibility outside of sexual systems. Here we used the color polymorphic orb‐web spider Gasteracantha fornicata, whose yellow‐ or white‐banded dorsal signal attracts dipteran prey, to test the hypothesis that morphs may be tuned to optimize either chromatic or achromatic conspicuousness in their visually noisy forest environments. We used data from extensive observations of naturally existing spiders and precise assessments of visual environments to model signal conspicuousness according to dipteran vision. Modeling supported a distinct bias in the chromatic (yellow morph) or achromatic (white morph) contrast presented by spiders at the times when they caught prey, as opposed to all other times at which they may be viewed. Hence, yellow spiders were most successful when their signal produced maximum color contrast against viewing backgrounds, whereas white spiders were most successful when they presented relatively greatest luminance contrast. Further modeling across a hypothetical range of lure variation confirmed that yellow versus white signals should, respectively, enhance chromatic versus achromatic conspicuousness to flies, in G. fornicata's visual environments. These findings suggest that color polymorphism may be adaptively maintained by selection for conspicuousness within different visual channels in receivers.     

Frequency-dependent physiological trade-offs between competing colour morphs

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

Floral polymorphism and the fitness implications of attracting pollinating and florivorous insects

Background and Aims

Floral polymorphism is frequently attributed to pollinator-mediated selection. Multiple studies, however, have revealed the importance of non-pollinating visitors in floral evolution. Using the polymorphic annual daisy Ursinia calenduliflora, this study investigated the importance of different insect visitors, and their effects on fitness, in the maintenance of floral polymorphism.

Methods

The spatial structure of a discrete floral polymorphism was characterized based on the presence/absence of anthocyanin floret spots in U. calenduliflora. A 3-year observational study was then conducted in polymorphic populations to investigate differences in visitation rates of dominant visitors to floral morphs. Experiments were performed to explore the floral preference of male and female Megapalpus capensis (the dominant insect visitor) and their effectiveness as pollinators. Next, floral damage by antagonistic florivores and the reproductive success of the two floral morphs were surveyed in multiple populations and years.

Key Results

Floral polymorphism in U. calenduliflora was structured spatially, as were insect visitation patterns. Megapalpus capensis males were the dominant visitors and exhibited strong preference for the spotted morph in natural and experimental observations. While this may indicate potential fitness benefits for the spotted morph, female fitness did not differ between floral morphs. However, as M. capensis males are very efficient at exporting U. calenduliflora pollen, their preference may likely increase the reproductive fitness of the spotted morph through male fitness components. The spotted morph, however, also suffered significantly greater costs due to ovule predation by florivores than the spotless morph.

Conclusions

The results suggest that pollinators and florivores may potentially exert antagonistic selection that could contribute to the maintenance of floral polymorphism across the range of U. calenduliflora. The relative strength of selection imposed by each agent is potentially determined by insect community composition and abundance at each site, highlighting the importance of community context in the evolution of floral phenotypes.     

Evidence of post-pollination barriers among three colour morphs of the deceptive orchid Dactylorhiza sambucina (L.) Soó

Floral-colour polymorphism in rewardless orchids has been hypothesized to be maintained by means of naïve insects, which after visiting a flower without reward will tend to fly elsewhere, looking for a flower of a different colour. In this study, levels of male and female reproductive success were monitored in Southern Italy populations of the deceptive orchid Dactylorhiza sambucina, through field observations over 3 years. These populations were characterized by the presence of a rare pink morph which is sympatric with the more frequent yellow and red morphs. In addition, final plant fertility was evaluated through percentages of embryo-containing seeds produced in both natural conditions and hand-pollination experiments. Results showed that pollinator preferences were independent of the morph frequencies and thus do not promote the predicted negative frequency-dependent selection. Although yellow and pink morphs showed significantly higher male reproductive success (RS), we found comparable levels of female RS, which suggest that pollinator behaviour cannot be the main mechanism which maintains this polymorphism. Interestingly, we found different percentages of embryo-containing seeds in fruits set under natural conditions as well as in those obtained from experimental crosses. In particular, pink morph showed a very low intrinsic fertility. Moreover, fertility in intra- was higher than in inter-morph crosses. To our knowledge, this is the first study pointing out the occurrence in the orchid family of post-pollination reproductive barriers. Findings are discussed in light of present hypothesis on the evolution and maintenance of colour polymorphism in deceptive orchids and other angiosperms.     

The potential for selection on pollen colour dimorphisms in Nigella degenii: morph-specific differences in pollinator visitation, fertilisation success and siring ability

Two subspecies of Nigella degenii (Ranunculaceae) possess a dimorphism in pollen colour and vary extensively in frequency of the two morphs in natural populations. Here we investigate the role of selection on pollen colour during the pollination phase in the two subspecies and its potential contribution to the maintenance of this colour variation. In a combination of common garden experiments and field observations, we obtained data on pollinator visitation rates and explored the effect of pollen colour on fertilisation success and siring ability under conditions of low vs. high pollen competition. In experimental gardens, naïve pollinators responded differently to plants with different pollen colour, but the favoured morph varied between dates and locations, and colour morphs were not visited in a frequency-dependent manner. Donor plants with dark pollen had a reproductive advantage (higher seed set) in single-donor pollinations, but the realised siring ability (measured by progeny morph ratio) was highly variable between different two-donor crosses with no general bias towards the light or dark morph. Therefore, although the dark pollen type appears to have a general selective advantage in terms of fertilisation success, our data are also consistent with a scenario involving the maintenance of both colour morphs, particularly under conditions of high pollen competition, a variable genetic background and/or spatial or temporal variation in the pollinator fauna.     

Differential predation on the two colour morphs of Nicaraguan Crater lake Midas cichlid fish: implications for the maintenance of its gold‐dark polymorphism

Predation can play an important role in the evolution and maintenance of prey colour polymorphisms. Several factors are known to affect predator choice, including the prey's relative abundance and conspicuousness. In polymorphic prey species, predators often target the most common or most visible morphs. To test if predator choice can explain why in Midas cichlid fish the more visible (gold) morph is also more rare than the inconspicuous dark morph, we conducted predation experiments using two differently coloured wax models in Nicaraguan crater lakes. Contrary to expectations, we observed an overall higher attack rate on the much more abundant, yet less conspicuous dark models, and propose frequency‐dependent predation as a potential explanation for this result. Interestingly, the attack rate differed between different types of predators. While avian predators were biased towards the abundant and less colourful dark morphs, fish predators did not show a strong bias. However, the relative attack rate of fish predators seemed to vary with the clarity of the water, as attack rates on gold models went up as water clarity decreased. The relative differential predation rates on different morphs might impact the relative abundance of both colour morphs and thus explain the maintenance of the colour polymorphism. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 123–131.     

Testing the role of coadapted genes versus bet-hedging for mating strategies in colour polymorphic pygmy grasshoppers

Recent investigations of mate choice indicate that the genetic effect of sires on offspring fitness may depend on the interaction between maternal and paternal genotypes and the environmental conditions experienced by the offspring. Alternative colour morphs of the pygmy grasshopper, Tetrix subulata , represent ecological strategies that differ in body size, life history, thermoregulatory behaviour, and habitat selection. The hypothesis that selection promotes behaviours maintaining coadapted gene complexes predicts individuals to mate assortatively with respect to colour morph. On the other hand, the bet-hedging hypothesis predicts that the temporal variability of the environment inhabited by these animals may select for disassortative mating behaviour resulting in heterogeneous offspring. To distinguish between these competing hypotheses, we investigated mating behaviours using dual-choice experiments. Our results were not in agreement with the prediction of assortative mating but suggest instead that matings were random with regard to colour morph. Polyandry was common, and females mated with the second male regardless of whether the first mating was assortative or disassortative. Polyandry also was equally frequent among females in triads in which the two males belonged to different colour morphs as in triads where both males belonged to the same colour morph. A field experiment confirmed that polyandry occurred also among free-ranging individuals, and uncovered variation in mating success among male colour morphs, probably due to indirect effects of coloration on activity or habitat use. The consequences of this random and polyandrous mating strategy for the evolutionary dynamics of the colour polymorphism remain to be explored.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 491–499.     

Morph‐dependent fitness and directional change of morph frequencies over time in a Dutch population of Common buzzards Buteo buteo

How genetic polymorphisms are maintained in a population is a key question in evolutionary ecology. Previous work on a plumage colour polymorphism in the common buzzard Buteo buteo suggested heterozygote advantage as the mechanism maintaining the co‐existence of three morphs (light, intermediate and dark). We took advantage of 20 years of life‐history data collected in a Dutch population to replicate earlier studies on the relationship between colour morph and fitness in this species. We examined differences between morphs in adult apparent survival, breeding success, annual number of fledglings produced and cumulative reproductive success. We found that cumulative reproductive success differed among morphs, with the intermediate morph having highest fitness. We also found assortative mating for colour morph, whereby assortative pairs were more likely to produce offspring and had longer‐lasting pair bonds than disassortative pairs. Over the 20‐year study period, the proportion of individuals with an intermediate morph increased. This apparent evolutionary change did not just arise from selection on individual phenotypes, but also from fitness benefits of assortative mating. The increased frequency of intermediates might also be due to immigration or drift. We hypothesize that genetic variation is maintained through spatial variation in selection pressures. Further studies should investigate morph‐dependent dispersal behaviour and habitat choice.     

Fluctuating selection by water level on gynoecium colour polymorphism in an aquatic plant

Background and Aims

It has been proposed that variation in pollinator preferences or a fluctuating environment can act to maintain flower colour polymorphism. These two hypotheses were tested in an aquatic monocot Butomus umbellatus (Butomaceae) with a pink or white gynoecium in the field population.

Methods

Pollinator visitation was compared in experimental arrays of equivalent flowering cymes from both colour morphs. Seed set was compared between inter- and intramorph pollination under different water levels to test the effect of fluctuating environment on seed fertility.

Key Results

Overall, the major pollinator groups did not discriminate between colour morphs. Compared with the white morph, seed production in the pink morph under intermorph, intramorph and open pollination treatments was significantly higher when the water level was low but not when it was high. Precipitation in July was correlated with yearly seed production in the pink morph but not in the white morph.

Conclusions

The results indicated that the two colour morphs differed in their tolerance to water level. Our study on this aquatic plant provides additional evidence to support the hypothesis that flower colour polymorphism can be preserved by environmental heterogeneity.     

Common Wall Lizard Females (Podarcis muralis) do not Actively Choose Males Based on their Colour Morph

Identifying the processes that lead to the evolution and maintenance of links between colour morphs and behavioural strategies has implications for the evolution of reproductive isolation and sympatric speciation. Sexual selection may play a significant role in the evolution of colour pattern complexity in reptiles, particularly when there are fitness consequences associated with mating with males of different colour morphs. In this article, we explored if common wall lizard females (Podarcis muralis) actively select males according to their morph in a colour‐assortative pattern using a multiple‐choice experiment with both visual and chemical cues. We failed to identify female active mate choice, as females did not choose males based on male colouration or femoral pore secretions. Indeed, females equally entered the three preference compartments and spent nearly the same amount of time within them, irrespective of both colour and odour of males. Consequently, our results do not support the hypothesis that colour polymorphism in this species may be driven by colour‐assortative mating promoted by females. However, we cannot exclude the possibility that females may choose males according to their colour following a flexible choice strategy, nor the possibility that females actively discriminate among males according to qualities that are not directly related to morph‐specific strategies.     

Differential foraging success across a light level spectrum explains the maintenance and spatial structure of colour morphs in a polymorphic bird

Detectability of different colour morphs under varying light conditions has been proposed as an important driver in the maintenance of colour polymorphism via disruptive selection. To date, no studies have tested whether different morphs have selective advantages under differing light conditions. We tested this hypothesis in the black sparrowhawk, a polymorphic raptor exhibiting a discrete white and dark morph, and found that prey provisioning rates differ between the morphs depending on light condition. Dark morphs delivered more prey in lower light conditions, while white morphs provided more prey in brighter conditions. We found support for the role of breeding season light level in explaining the clinal pattern of variation in morph ratio across the species range throughout South Africa. Our results provide the first empirical evidence supporting the hypothesis that polymorphism in a species, and the spatial structuring of morphs across its distribution, may be driven by differential selective advantage via improved crypsis, under varying light conditions.     

Effects of local density and flower colour polymorphism on pollination and reproduction in the rewardless orchid Dactylorhiza sambucina (L.) Soò

The rewardless orchid Dactylorhiza sambucina shows a stable flower colour polymorphism, with both yellow- and red-flowered morphs growing sympatrically. Pollination biology and breeding system were investigated to examine the effects of density of plants, colour polymorphism, inflorescence dimension, and flower position within inflorescence on male and female reproductive success in three natural populations of D. sambucina. There were significant differences among sites in the number of pollinia removed and in fruit set per inflorescence. Number of removed pollinia and capsule production in D. sambucina were independent from flower and inflorescence size or flower position. As a whole, the red morphs showed the highest number of capsules produced, while the yellow morphs had the greatest male success. The relative male and female reproductive success were independent from plant density but were significantly correlated with the yellow morph frequency at the population level. Overall, our findings show that the contribution to the total reproductive success deriving from the two colour morphs does not conform with the predictions of negative frequency-dependent selection.     

Skewed male reproductive success and pollen transfer in a small fragmented population of the heterodichogamous tree <Emphasis Type="Italic">Machilus thunbergii</Emphasis>

Heterodichogamy is defined as the presence of two flower morphs that exhibit the male and female functions at different times among individuals within a population. Heterodichogamy is regarded as an adaptation to promote outcrossing through enhanced inter-morph mating, together with a 1:1 morph ratio. However, in highly fragmented populations, the morph ratio may be more likely to be biased by stochastic events. In such a situation, individuals of a minority morph within a population are expected to have higher reproductive success than those of a majority morph, which may suffer from pollen shortages of the minority morph. In this paper, we evaluated mating patterns and male reproductive success in a highly fragmented population of Machilus thunbergii, a putative heterodichogamous evergreen laurel tree. Results of paternity analysis indicated that the selfing rate was not clearly different between the two morphs. In contrast, the proportion of intra-morph mating was higher in the majority-morph (MM) mother trees than in the minority-morph (MF) mother trees. Bayesian estimated male reproductive success indicated that male reproductive success was higher in minority-morph (MF) than in majority-morph (MM) mother trees. These findings indicate that (1) the majority morph mothers, suffering a shortage of the opposite morph pollen, could partly compensate for the reduced reproductive success by intra-morph mating rather than by selfing, and (2) negative-frequency dependent selection may be involved in the maintenance of the two morphs.     

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.     

The evolution, maintenance and adaptive function of genetic colour polymorphism in birds

The hypothesis that ornaments can honestly signal quality only if their expression is condition-dependent has dominated the study of the evolution and function of colour traits. Much less interest has been devoted to the adaptive function of colour traits for which the expression is not, or is to a low extent, sensitive to body condition and the environment in which individuals live. The aim of the present paper is to review the current theoretical and empirical knowledge of the evolution, maintenance and adaptive function of colour plumage traits for which the expression is mainly under genetic control. The finding that in many bird species the inheritance of colour morphs follows the laws of Mendel indicates that genetic colour polymorphism is frequent. Polymorphism may have evolved or be maintained because each colour morph facilitates the exploitation of alternative ecological niches as suggested by the observation that individuals are not randomly distributed among habitats with respect to coloration. Consistent with the hypothesis that different colour morphs are linked to alternative strategies is the finding that in a majority of species polymorphism is associated with reproductive parameters, and behavioural, life-history and physiological traits. Experimental studies showed that such covariations can have a genetic basis. These observations suggest that colour polymorphism has an adaptive function. Aviary and field experiments demonstrated that colour polymorphism is used as a criterion in mate-choice decisions and dominance interactions confirming the claim that conspecifics assess each other's colour morphs. The factors favouring the evolution and maintenance of genetic variation in coloration are reviewed, but empirical data are virtually lacking to assess their importance. Although current theory predicts that only condition-dependent traits can signal quality, the present review shows that genetically inherited morphs can reveal the same qualities. The study of genetic colour polymorphism will provide important and original insights on the adaptive function of conspicuous traits.     

Is the colour dimorphism inDactylorhiza sambucina maintained by differential seed viability instead of frequency-dependent selection?

The European rewardless, bee-pollinated orchidDactylorhiza sambucina commonly produces yellow-flowered and purple-flowered individuals in frequencies that range from balanced (per population) to very unbalanced, with parts of the species’ range entirely monochromatic. We studied male and female reproductive success of the two morphs in 22 populations in the Czech Republic, relating it to morph frequency, population size and density, and presence and abundance of yellow and purple co-flowering nectar-providing species visited by the same bee species. Cumulative abundances of yellow nectar-producing co-flowering species (of which, on average,Primula veris made up 56%) had a negative effect on male reproductive success of the yellow morph, and spectral analyses showed that to bumblebees the colours ofP. veris and yellowD. sambucina are different, permitting ready visual discrimination. The cumulative abundance of purple co-flowering species had no significant effect on morph reproductive success. Morph frequencies were unrelated to reproductive success and population size, and there was no evidence of frequency-dependent selection except in one highly unbalanced population. Density of flowering conspecifics was negatively correlated with male reproductive success of the purple morph. Seed mass, viability, and germination success depended on whether seeds resulted from outcrossed or selfed matings and on morph colour. Selfed seeds and seeds produced by the yellow morph from yellow × yellow and yellow × purple crosses had zero germination (after three months), providing the first hint that differential vegetative fitness, rather than differential reproductive fitness via pollinator selection, may explain morph frequencies inD. sambucina.     

A new morph of Telmatochromis temporalis (Cichlidae; Cichliformes) from Lake Tanganyika

Telmatochromis temporalis is a cichlid fish endemic to Lake Tanganyika. Two morphs of this species, normal and dwarf, form a good model for the study of ecological speciation through divergent natural selection on body size. This study reports a third morph of this species, slender morph, which was collected from deep waters off Kasenga, Zambia, whereas the normal morph inhabits shallow waters of the same locality. This study examined morphological characters and mitochondrial DNA sequences in 18 populations of the three T. temporalis morphs and two closely related species. The slender morph was morphologically similar to the normal and dwarf morphs of the same species, but clearly differed from closely related species. Genetic analyses showed that the slender morph was closest to but significantly different from the parapatric normal morph, suggesting reproductive isolation between them. Due to the lack of colour differences between morphs and of obvious geographical barriers between habitats, reproductive isolation between these morphs may be attributed to ecological factors, rather than sexual or geographical segregation. Further studies examining the evolution of the slender morph may deepen our knowledge of initial stages of speciation, like in the dwarf morph.