The relationship between mimetic imperfection and phenotypic variation in insect colour patterns

Many hoverflies (Syrphidae) mimic wasps or bees through colour or behavioural adaptations. The relationship between phenotypic variation in colour pattern and mimetic perfection (as determined by pigeons) was investigated in three species of Müllerian mimics (Vespula spp.) and 10 Batesian hoverfly mimics, plus two non-mimetic species of flies. Four predictions were tested: (i) Batesian mimics might be imperfect because they are in the process of evolving towards perfection, hence there should be a positive relationship between variation and imperfection; (ii) some Batesian mimics are imperfect because they do not have the appropriate genetic variation to improve and have evolved to be as good as possible, hence there should be no differences between species, all displaying a low level of variation; (iii) very common hoverflies should show the highest levels of variation because they outnumber their models, resulting in high predation and a breakdown in the mimetic relationship; and (iv) social wasps (Vespula) have such a powerful defence that anything resembling a wasp, both Müllerian and perfect Batesian mimics, would be avoided, resulting in relaxed selection and high variance. Poor mimics may still evolve to resemble wasps as well as possible and display lower levels of variation. The data only provided support for the fourth prediction. The Müllerian mimics, one of the most perfect Batesian mimics, and the non-mimetic flies displayed much higher levels of variation than the other species of Batesian mimics.     

The key mimetic features of hoverflies through avian eyes

Batesian mimicry occurs when a palatable species (the mimic) gains protection from predators by resembling an unpalatable or otherwise protected species (the model). While some mimetic species resemble their models closely, other species ('imperfect mimics') are thought to bear only a crude likeness. In an earlier study, pigeons (Columba livia) were trained to recognize wasp images in one experiment and non-mimetic (NM) fly images in another by rewarding the pigeons for pecking on the respective image types. These pigeons were subsequently presented with different images, including seemingly wasp-like hoverfly species, and the recorded peck rates on these images were used as a measure of the pigeons' perception of the hoverflies' mimetic similarity. To identify a candidate set of morphological features that the pigeons used when assessing this mimetic similarity, we first extracted a range of biometrical measurements from images originally presented to the pigeons. We then repeatedly optimized an empirical model in an attempt to match the recorded pigeon peck rates while using as few biometrical features as input as possible. Our models were able to fit the pigeon peck rates with considerable accuracy even while excluding many input features. Antennal length, a feature commonly used to discriminate between flies and wasps, was regularly retained as an input variable, but overall a different set of biometrical features was important for predicting the peck rates of pigeons rewarded for identifying wasps compared to those rewarded for identifying NM flies. In highlighting the importance of specific biometrical features in promoting mimicry and the irrelevance of others, our optimized models provide an explanation as to why certain species that appear to be poor mimics to humans are judged to be good mimics by birds.     

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.     

DOES THE ABUNDANCE OF HOVERFLY (SYRPHIDAE) MIMICS DEPEND ON THE NUMBERS OF THEIR HYMENOPTERAN MODELS?

We tested the prediction that, if hoverflies are Batesian mimics, this may extend to behavioral mimicry such that their numerical abundance at each hour of the day (the daily activity pattern) is related to the numbers of their hymenopteran models. After accounting for site, season, microclimatic responses, and general hoverfly abundance at three sites in northwestern England, the residual numbers of mimics were significantly correlated positively with their models nine times of 17. Sixteen of 17 relationships were positive, itself a highly significant nonrandom pattern. Several eristaline flies showed significant relationships with honeybees even though some of them mimic wasps or bumblebees, perhaps reflecting an ancestral resemblance to honeybees. There was no evidence that good and poor mimics differed in their daily activity pattern relationships with models. However, the common mimics showed significant activity pattern relationships with their models, whereas the rarer mimics did not. We conclude that many hoverflies show behavioral mimicry of their hymenopteran models.     

Why are there good and poor mimics?

Among the many Batesian mimetic hoverflies (Diptera: Syrphidae) some have a very precise resemblance to the presumed model ('good' or 'specific' mimics) while others have a much less precise resemblance ('poor' or 'general' mimics). Intuitively one might expect that the specific mimics would be commoner and more successful than the general mimics. However, many specific mimics (e.g. Serkomyia silentis, Volucella bombylans) are quite rare, while general mimics are common (e.g. Syrphus ribesii, Episyrphus balteatus and Eristalis intricarius). Similarly, some ant-mimicking spiders from several different families are very good morphological and behavioural mimics of just one species of ant while others have a less detailed resemblance to ants in general. Six hypotheses are presented to explain the occurrence of so many poor mimics, and a theoretical model is outlined (the multi-model hypothesis) which shows how a poor general mimic can have a larger population than a good, specific mimic. This hypothesis may apply to some species of hoverfly and to some ant-mimicking spiders.     

Nest site competition between cavity nesting passerines and golden paper wasps Polistes fuscatus

Nest boxes provide sheltered nesting sites for both passerines and paper wasps. Although neither wasps nor birds appear to evict the other once one is fully established, it is unclear which is the dominant competitor at the onset of the breeding season. Using wire mesh, we excluded birds but not golden paper wasps Polistesfuscatus from alternating boxes along a transect through edge habitat in North Carolina from 2006 – 2008. If wasps dominate Carolina chickadees Poecile carolinensis and eastern bluebirds Sialia sialis during the early spring (all have similar nest initiation dates), we would expect wasps to settle in both box types at equal frequencies. However, if birds dominate wasps, we would expect wasp nests to be concentrated in “bird‐proof” boxes. We found wasps in bird‐proof boxes significantly more often than in bird‐accessible boxes, indicating that secondary‐cavity nesting birds are able to exclude wasps from available nest sites. Additionally, we found that during the period of nest initiation, birds usurp wasps more often than vice versa.     

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.     

Is the evolution of inaccurate mimicry a result of selection by a suite of predators? A case study using myrmecomorphic spiders

Several hypotheses have been put forward to explain the evolution of inaccurate mimicry. Here we investigated the novel hypothesis that inaccurate mimicry (in color and shape) is maintained by opposing selective pressures from a suite of different predators: model-aversive visually oriented predators and model- and mimic-specialized predators indifferent to mimetic cues. We hypothesize that spiders resembling ants in color and shape escape predators that typically avoid ants but fall prey to ant-eating predators. We tested whether inaccurate myrmecomorphic spiders are perceived as their models by two types of predators and whether they can escape from these predators. We found that model-specialized (ant-eating) predators captured mimics significantly less frequently than their ant models, because mimics changed their behavior by fleeing predatory attacks. The fastest escape was found in less accurate mimics, indicating a negative association between visual resemblance and effectiveness of defenses. In trials with spider-eating predators, mimics were not captured more frequently than their models. The quality of defensive mechanisms appears to result from opposing selection forces exerted by the predator complex: mimics are more accurate (in color and shape) in microhabitats dominated by model-aversive predators and less accurate in microhabitats with model- and mimic-specialized predators.     

Mimicry profiles are affected by human-induced habitat changes.

Mimicry theory predicts that mimics in a Batesian mimicry complex evolve to resemble models closely, and that there is a limit on the numbers of mimics relative to models. For hoverflies (Diptera: Syrphidae), supposed mimics of social wasps (Hymenoptera: Vespidae, neither of these is true; many mimics are imperfect and in the UK and Europe they outnumber their models manifold. We hypothesized that the high abundance of mimics relative to models in the UK may be the result not just of mimic model dynamics, but of habitat changes caused by humans. Most of the larvae of poor mimics are aphidophagous, and changes from ancient forest to agricultural and/or urban habitats may have vastly augmented aphid numbers. Using new and literature data, we compared mimicry profiles of habitats differing in their degree of habitat disturbance. In both cases more highly disturbed habitats had proportionally more poor mimics and fewer high-fidelity mimics than less disturbed habitats. This supports the hypothesis that habitat change has an effect on model to mimic ratios.     

Phenotypic plasticity in hoverflies: the relationship between colour pattern and season in Episyrphus balteatus and other Syrphidae

1. The abdominal colour patterns of some multivoltine species of hoverfly are phenotypically plastic and change through the flying season.
2. It was predicted how the abdominal colour pattern of one species, Episyrphus balteatus , should change in the field with season based on a hypothesis that the pattern influences the thermoregulatory capabilities of the animal. The colour patterns were quantified using image analysis. The observed changes in the colour pattern through the year supported the thermoregulation hypothesis.
3. A further three Metasyrphus species were analysed similarly to allow a comparative study of the forms of the plasticities of the above four species and four Eristalis species from a previous study.
4. Whilst it was clear that the abdominal colour patterns of many of the species were plastic, it was also apparent that not all species used the same developmental pathway to control the seasonal colour pattern changes. This suggests convergent evolution towards a general type of plasticity and that abdominal colour pattern plasticity in hoverflies is functional.     

Signal convergence in fruits: a result of selection by frugivores?

The Dispersal Syndrome hypothesis remains contentious, stating that apparently nonrandom associations of fruit characteristics result from selection by seed dispersers. We examine a key assumption under this hypothesis, i.e. that fruit traits can be used as reliable signals by frugivores. We first test this assumption by looking at whether fruit colour allows birds and primates to distinguish between fruits commonly dispersed by birds or primates. Second, we test whether the colours of fruits dispersed by primates are more contrasting to primates than the colours of bird‐dispersed fruits, expected if fruit colour is an adaptation to facilitate the detection by seed dispersers. Third, we test whether fruit colour has converged in unrelated plant species dispersed by similar frugivores. We use vision models based on peak sensitivities of birds’ and primates’ cone cells. We base our analyses on the visual systems of two types of birds (violet and ultraviolet based) and three types of primates (trichromatic primates from the Old and the New Worlds, and a dichromatic New World monkey). Using a Discriminant Function Analysis, we find that all frugivore groups can reliably discriminate between bird‐ and primate‐dispersed fruits. Fruit colour can be a reliable signal to different seed dispersers. However, the colours of primate‐dispersed fruits are less contrasting to primates than those of bird‐dispersed fruits. Fruit colour convergence in unrelated plants is independent of phylogeny and can be better explained by disperser type, which supports the hypothesis that frugivores are important in fruit evolution. We discuss adaptive and nonadaptive hypotheses that can potentially explain the pattern we found.     

Prey from the eyes of predators: Color discriminability of aposematic and mimetic butterflies from an avian visual perspective

Predation exerts strong selection on mimetic butterfly wing color patterns, which also serve other functions such as sexual selection. Therefore, specific selection pressures may affect the sexes and signal components differentially. We tested three predictions about the evolution of mimetic resemblance by comparing wing coloration of aposematic butterflies and their Batesian mimics: (a) females gain greater mimetic advantage than males and therefore are better mimics, (b) due to intersexual genetic correlations, sexually monomorphic mimics are better mimics than female‐limited mimics, and (c) mimetic resemblance is better on the dorsal wing surface that is visible to predators in flight. Using a physiological model of avian color vision, we quantified mimetic resemblance from predators’ perspective, which showed that female butterflies were better mimics than males. Mimetic resemblance in female‐limited mimics was comparable to that in sexually monomorphic mimics, suggesting that intersexual genetic correlations did not constrain adaptive response to selection for female‐limited mimicry. Mimetic resemblance on the ventral wing surface was better than that on the dorsal wing surface, implying stronger natural and sexual selection on ventral and dorsal surfaces, respectively. These results suggest that mimetic resemblance in butterfly mimicry rings has evolved under various selective pressures acting in a sex‐ and wing surface‐specific manner.     

Male bill colour and competition in zebra finches

Several studies have assessed the role of bill colour in sexual selection and especially with respect to sexual preferences. Even though there are indications that bill colour is related to male quality, so far it has not been shown that bill colour influences male-male interaction. We used male zebra finches with artificially coloured bills in a competitive context to measure the effect of bill colour. In these tests the experimental bird could choose between two feeding sites, each near a stimulus bird with a different bill colour. We tested orange against red, no bird against orange/red and orange/red against green respectively. We found no difference in behaviour towards an orange compared to a red billed stimulus. However the birds spent relatively more time eating when alone compared to being close to a potential competitor. In addition, more time was spent eating than on other behaviours when the birds were close to the orange/red billed stimulus compared to the green billed stimulus. So, although no effect was found in the orange against red test, the results suggest that bill colour may play some role in male-male interaction.     

A simulation of evasive mimicry in the wild

The hypothesis of evasive mimicry proposes that: (a) the conspicuous coloration of some animals has evolved to warn predators that they are good at avoiding capture; and (b) this conspicuous coloration is mimicked by other, less evasive species which thus gain protection from predation. We have tested these ideas with wild birds as the predators and red and yellow pastry 'baits' as the prey. We used a specially constructed bird table to make one of the colours good at 'escaping': when a bird was about to eat a bait the observer pulled a cord which activated a mechanism that made the baits of one colour (but not the other) drop out of the bird's reach. We first measured the overall selection by the naive birds by presenting, for one day, a 'control' of equal numbers of non-evasive red and non-evasive yellow baits. The birds were then trained for 20 days on equal numbers of evasive yellow and non-evasive red baits, and were then again given a second control (in which the yellows were now non-evasive 'mimics'). The training was repeated for 18 days but with red as the evasive colour, and a third control was then presented (with reds now as the mimics). The proportions attacked daily in the two training sessions suggested that the birds were learning to ignore yellows in the first and reds in the second. In comparison with the first control, fewer yellows were eaten after they had been trained to ignore escaping yellows, and more were eaten after they had been trained on escaping reds. We conclude that the results are further evidence for the hypothesis of evasive mimicry.     

Phenological relationships of wasps, bumblebees, their mimics and insectivorous birs in northern Michigan

Abstract. 1. In northern Michigan 72% of the high fidelity dipterous Batesian mimics of bumblebees and vespoid wasps occurred in spring while they still outnumbered their models but before the great majority of fledgling birds left their nests to begin foraging for insects on their own.
2. This extends the known occurrence of this sort of phenology to several additional mimetic species and to an area which is radically different climatically and ecologically from the central Illinois areas in which this sort of phenology was first noted.
3. Our observations confirm the hypothesis that Batesian mimics may be selected to avoid the midsummer period when newly fledged insectivorous birds are abundant but have not yet learned to shun their stinging hymenopteran models.
4. The shortness of the warm season in Michigan reduces opportunities for temporal separation and may have forced the other 28% of the high fidelity mimics to occur when naive birds are abundant. The threat from naive birds was, however, presumably somewhat ameliorated by the abundance of models at that time.     

The role of odour and visual cues in the pan-trap catching of hoverflies (Diptera: Syrphidae)

Coloured pan traps are frequently used to attract and catch insects, such as in the monitoring of populations of beneficial insects in classical or conservation biological control. They are also used in the evaluation of the recovery of insect populations after disturbance and in many other situations where an estimate of relative insect numbers is required. However, the fact that traps may be visible to the insects over a considerable distance can influence the interpretation of catch data. This difficulty may arise, for example, if traps along a transect can attract insects from some or all of the other transect positions. This study compared the effect of different coloured traps on attraction and catch of hoverflies. The hypothesis was that completely yellow traps would attract hoverflies from a distance, while traps that were green outside and yellow inside would catch fewer flies because only those from above or near the trap can see the yellow stimulus. A subsidiary hypothesis was that rose water would enhance hoverfly capture rates. For the two main hoverfly species captured, Melanostoma fasciatum (Macquart) and Melangyna novaezelandiae (Macquart), significantly more individuals were caught in completely yellow traps than in yellow and green or in completely green traps. Moreover, the addition of rose water increased the number of hoverflies caught significantly. It is suggested that if a measure of hoverfly numbers relating to a particular distance along a transect is required, consideration should be given to the ability of hoverflies to see yellow traps from a distance. The use of traps that are green outside would more accurately reflect the local abundance of hoverflies. If higher trap catches of hoverflies are needed for statistical purposes, rose water can enhance catches.     

Hoverfly (Diptera: Syrphidae) community of a cultivated arable field and the adjacent hedgerow near Debrecen,Hungary

A hoverfly (Syrphidae) community was investigated in a cultivated wheat field and the adjacent hedgerow near Debrecen (Hungary). We monitored the change of species richness and abundance of hoverflies along three transects in the hedgerow and in the wheat field in different distances (10 m, 20 m) from the hedgerow. The effect of sampling methods on the number of hoverfly species and individuals was analyzed. Two sampling methods were used to catch hoverflies: netting and pan traps. The whole sampling period was divided into three subperiods, which are early (22^nd April–2^nd June), middle (11^th June–1^st August) and late (6^th August–11^th September). Altogether 1,214 individuals of 22 species were sampled. Fourteen species with 78% of individuals belonged to the aphidophagous group, feeding on aphids as larvae. Altogether 861 individuals of 22 hoverfly species were sampled by netting and 353 individuals of 10 species by pan traps. The total number of hoverfly species was significant lower in the late period than in the early. The total abundance was higher in the middle period compared to the early. The species richness and abundance of aphidophagous species followed a similar pattern as the total species values. The species richness and abundance of hoverflies were significant higher in 10 m and 20 m distance in the wheat field than along the hedgerow. The results suggest that the pan traps were less efficient in the hedgerow than the netting, but in the wheat field they sampled more hoverflies because of visually alluring effect on hoverflies in the absence of flowers.     

The evolution of mimicry under constraints

The resemblance between mimetic organisms and their models varies from near perfect to very crude. One possible explanation, which has received surprisingly little attention, is that evolution can improve mimicry only at some cost to the mimetic organism. In this article, an evolutionary game theory model of mimicry is presented that incorporates such constraints. The model generates novel and testable predictions. First, Batesian mimics that are very common and/or mimic very weakly defended models should evolve either inaccurate mimicry (by stabilizing selection) or mimetic polymorphism. Second, Batesian mimics that are very common and/or mimic very weakly defended models are more likely to evolve mimetic polymorphism if they encounter predators at high rates and/or are bad at evading predator attacks. The model also examines how cognitive constraints acting on signal receivers may help determine evolutionarily stable levels of mimicry. Surprisingly, improved discrimination abilities among signal receivers may sometimes select for less accurate mimicry.     

A seed parasitoid wasp prevents berries from changing their colour,reducing their attractiveness to frugivorous birds

1. Frugivorous and seed‐feeding insects may alter the traits of fruits, such as shape and size, which may influence fruit attractiveness to frugivorous birds. Consequently, trait‐mediated interactions may occur in systems where plants, seed‐dispersing frugivorous vertebrates, and frugivorous or seed‐feeding insects interact. We investigated colour manipulation in Ilex integra Thunb. berries caused by the seed parasitoid wasp Macrodasyceras hirsutum Kamijo and how that manipulation relates to fruit attractiveness for frugivorous birds. 2. In winter, the colour of I. integra berries varied from green to red, but most berries were greenish, indicating that the berries were immature. Berry dissection indicated that the number of live parasitoid larvae present within each berry was closely related to berry colour – the greater the number of live larvae, more intense is the green colour of the berry. However, the wasp larvae did not modify the shape or size of the berries. More than 98% of berries that were protected from the insects by gauze bags ripened and turned red. In the present study, berries with unfertilised seeds alone turned red. Field‐feeding preference tests showed that the brown‐eared bulbul Hypsipetes amaurotis Temminck preferred red berries to green berries. 3. We demonstrated that the seed parasitoid wasp manipulates the berry colour, but not its shape or size, in a density‐dependent manner. Because green berries suffered less from bird foraging, we believe that this colour manipulation helps the wasps to avoid being killed by the birds. The present study indicates that manipulation by wasps may reduce the level of mutualism between the tree and seed‐dispersing birds.