More than meets the eye-a simulation of natural selection

One of the most easily understood examples of natural selection occurs when predators preferentially feed on conspicuous varieties in a prey population and thus confer a selective advantage on cryptic varieties. This effect can be demonstrated by using wild birds as predators, pastry ‘baits’ as prey, and coloured stones as backgrounds. We have carried out five experiments using two variations of this method and the results confirm its potential as an exercise in simulating natural selection.     

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.     

The influence of density on frequency-dependent selection by wild birds feeding on artificial prey

Previous work has demonstrated frequency-dependent selection by wild garden birds when feeding on green and brown pastry ''baits''. When the density of baits is low, the common colour is eaten disproportionately more than the rare colour (apostatic selection), and when the density is very high, the rare colour is eaten disproportionately more than the common (anti-apostatic selection). We explored the relationship between frequency-dependent predation and density in an experiment at 16 separate sites, using four levels of density and two frequencies of green and brown. Analysis of estimates of log-relative risk ratios showed little evidence for frequency-independent selection, but frequency-dependent selection changed gradually from apostatic at low density to anti-apostatic at high density. The validity of these conclusions in terms of individual bird behaviour was confirmed by Monte-Carlo simulations. We thus conclude that selection by wild birds feeding on green and brown artificial prey is frequency dependent, and that the strength and direction of this selection changes with prey density in a gradual and predictable manner.     

Further evidence for apostatic selection by wild passerine birds -9 :1 experiments.

Apostatic selection occurs when predators concentrate disproportionately on the common varieties of non-mimetic polymorphic prey species. This has been tested in 14 experiments by presenting populations of green and brown lard-and-flour "baits" to inexperienced wild passerine birds in their normal surroundings. In seven experiments a 9 green : 1 brown population was presented for a number of days, followed by a 1 green : 9 brown population for a similar period. in the remaining seven experiments the populations were presented in the reverse order. The birds often had strong "natural" colour preferences (for example, blackbirds and songthrushes preferred browns) which were not caused by the relative conspicuousness of the two colours. The data within most of the experiments were very heterogeneous, but in every experiment there was good evidence that the birds tended to concentrate on the common colour. The consistency of the replicated experiements gives strong reason to believe that apostatic selection is a widespread phenomenon among avian predators, and provides an explanation for many of the non-mimetic colour and pattern polymorphisms found among their prey.     

Apostatic selection on prey that match the background

There is good experimental evidence that predators often remove disproportionately more of the common prey types. This 'apostatic selection' could maintain colour polymorphisms within prey species. In nature, morphs of many species appear to match components in the background, but most of the experiments that have tested apostatic selection have used prey that were conspicuous. In work described in this paper, wild birds at one site were presented a random order of 51 experiments. Seventeen frequencies of orange and grey pastry prey were presented on each of three types of background: a hessian sheet scattered with either orange and grey stones (the 'matching' background), or lilac and yellow stones, or green stones (two sorts of 'control' background). Each experiment consisted of four trials in succession and the numbers of the two colours eaten in each trial were recorded when about half the total prey had been eaten. Two methods of graphical analysis revealed that apostatic selection occurred on the prey on all three backgrounds, but was strongest in the grey/orange one. This last result must have been caused by some effect of the match between prey and background colour, and behavioural explanations are suggested. It is unclear whether the prey were exhibiting 'crypsis' or 'masquerade'.     

Selection by passerine birds is anti-apostatic at high prey density

Most of the results from past experiments with wild birds and green and brown pastry 'baits' have suggested that disproportionately more of the rare forms are eaten when bait density is high (i.e. selection is anti-apostatic). In two separate series of experiments we presented birds with dishes containing 270 baits of one colour and 30 of another. In series I, five different pairs of colours were presented simultaneously to wild birds at two sites. One colour of each pair was common at one site and the same colour was rare at the other site. After 35 days the ratios of the colours were reversed and the dishes were presented for another 35 days. There was a statistically significant tendency for the colours to be at a higher risk when rare. In series II, three caged blackbirds were offered green and brown baits in two dishes simultaneously; in one dish green was rare and in the other brown was rare. Selection over 6 days was anti-apostatic for all three birds combined but the data proved heterogeneous both between and within individuals. At any one time, each bird tended to concentrate on one colour, irrespective of whether that colour was rare or common. We believe that this behaviour leads to anti-apostatic selection, as has been observed in these and other experiments with pastry prey.     

Reactions of hand-reared and wild-caught predators toward warningly colored, gregarious, and conspicuous prey

Recently there has been debate over the importance of innateavoidance of aposematic prey by predators, particularly birds.There is evidence that the predators have innate or unlearned,thus, inherited avoidance against certain colors, but whetherthere is any innate avoidance against gregariousness or conspicuousnessis unclear. Previously predator behavior toward these charactersof aposematic prey have been tested in separate experiments.We designed an experiment to separate inheritance toward color,gregariousness, and conspiucuosness. We simultaneously offeredthe predators warningly colored and nonwarningly colored preyitems, both aggregated and solitary, on white (conspicuous)or brown (cryptic) backgrounds. The predators we used were naive (handraised), wild-caught yearling and adult great tits (Parus major L.).The results confirm previous results regarding the innate avoidanceof color. Naive predators seemed to have a genetically or culturallytransmitted avoidance of yellow and black prey compared to brownprey. Surprisingly, yearling wild-caught great tits were moreselective than adults, which did not show as strong avoidanceof yellow and black prey. More importantly, birds did not findgregarious prey more aversive than single prey, which indicatesthat grouping alone does not serve as an innate avoidance signal.Conspicuousness itself was not aversive to the predators. Ourresults suggest that the avoidance against a particular colorpattern probably has an inherited basis, whereas gregariousand conspicuous characters of prey presumably aid the avoidancelearning.     

Selection by wild birds on artificial dimorphic prey on varied backgrounds

Our aim was to test the effects of prey frequency and background composition on selection by free-ranging birds. We did three series of experiments with populations of grey and orange pastry prey scattered among coloured stones that made the prey either conspicuous or inconspicuous. Series 1 tested whether the predicted equilibrium frequency of the two prey types was influenced by the frequency of matching grey and orange stones. Birds at a single site were given a random sequence of combinations of prey frequency and stone frequency. Selection was dependent on background and the effect of prey frequency also varied with background. In series 2, we explored the frequency-independent effect of background: birds at five sites were given equal numbers of the two prey in three frequencies of matching stones and two of non-matching. There was a higher risk of predation for prey that matched rarer stones. In series 3 we attempted to measure, at a single site, the actual equilibrium prey frequencies in three different backgrounds: two extreme stone frequencies and one intermediate. Each experiment started with a population of equal numbers of grey and orange prey. After half the prey had been eaten we calculated the frequencies of the survivors and presented a new population of the original size but with the new prey frequencies; each experiment ran for 25 such 'generations'. The results suggested that at equilibrium the commoner 'morph' was the one that resembled the commoner colour of stone. Overall, our findings support the idea that visual selection can result in morph frequencies becoming related to the proportions of their matching background components and that this equilibrium will 'track' temporal or spatial changes in the background.     

Does prey dispersion affect frequency-dependent predation by wild birds?

Despite the fact that the vast majority of natural prey items are dispersed in a non-random manner, few studies of frequency-dependent selective predation have explicitly examined the effect of prey dispersion on selectivity. We examined the effect of prey dispersion on the direction and strength of frequency-dependent selection by wild birds feeding on artificial prey (green or brown pastry baits). In a series of four experimental manipulations, we tested for the occurrence of frequency dependence with two different dispersion patterns (random or clumped). Manipulations were carried out at one of two absolute densities (25 prey m⁻² or 100 prey m⁻²), and were repeated at different sites in Southampton, England and Aljarafe, Spain. Our results suggest that prey dispersion has no effect on either frequency-dependent or -independent preferences. One possible explanation for this is that the birds had virtually complete information about prey frequencies at the relatively high densities used and based their preferences on their overall perception of availability. However, we cannot rule out the possibility that dispersion may influence selectivity when prey are cryptic or available at lower absolute densities. Although there was no effect of dispersion, frequency-dependent selection was, overall, significantly anti-apostatic (i.e. rare baits were more preferred than common baits). This anti-apostatic effect was stronger in Southampton than Aljarafe and stronger at 100 prey m⁻² than 25 prey m⁻². The differences in the strength of selection between the two locations was interpreted in terms of (i) whether the avian predators foraged in flocks or not, and (ii) the number of different species present (and, consequently, the variation in preference among individual birds). Received: 21 December 1996 / Accepted: 26 February 1997     

The Repertoire of Plant Cells

Cryptic (camouflaged) prey often seek out backgrounds that match their coloration, and when at rest adopt an attitude that makes their crypsis most effective. We suggest a simple method for investigating the adaptive significance of such orientation. We used flat discs of pastry as the ‘prey’, either plain white or painted with a central black stripe, and wild garden birds as the predators. In the eight main experiments the backgrounds were white wooden boards painted with black parallel stripes of the same width as the stripes on the prey. In each experiment we presented equal numbers of two (of seven) ‘treatments’ of prey. The selection resulting from the combined predation by the birds confirmed the advantages of resting on a matching background and in the ‘correct’ orientation. We suggest that the technique can be developed further to explore the adaptive significance of background matching     

Frequency-dependent predation by birds at edges and interiors of woodland

Structural variations between edge and interior areas within forest fragments may bring about differences in food availability that may influence the selective behaviour of predators and prey population dynamics. The purpose of this paper was to assess patterns of artificial prey selection by wild birds (House Sparrow Passer domesticus and Rock Dove Columba livid) between edge and interior areas of woodland, taking into account differences in prey frequency (10% of one food type and 90% of the other) and density (30 baits/m^-2 and 50 baits/m-²). Experiments were conducted at 24 plots in 3 forest fragments in the city of Madrid, Spain. Selectivity did not vary among parks or between densities. However, selectivity did vary with the frequency and location of baits, showing an anti-apostatic trend (baits were preferred at low rather than at high frequencies) that was more pronounced at interiors than at edges. Two possible factors that may account for stronger anti-apostatic selection at edges are the higher densities of predators and pedestrians found there. However, there are many other possible explanations, and no specific conclusion can be supported with the current data. The results of this study also point out that site heterogeneity should be taken into account in the experimental design of future studies on frequency-dependent food selection by wild birds, particularly in fragmented landscapes.     

Predator experience on cryptic prey affects the survival of conspicuous aposematic prey

Initially, aposematism, which is an unprofitable trait, e.g. noxiousness conspicuously advertised to predators, appears to be a paradox since conspicuousness should increase predation by naive predators. However, reluctance of predators for eating novel prey (e.g. neophobia) might balance the initial predation caused by inexperienced predators. We tested the novelty effects on initial predation and avoidance learning in two separate conspicuousness levels of aposematic prey by using a 'novel world' method. Half of the wild great tits (Parus major) were trained to eat cryptic prey prior to the introduction of an aposematic prey, which potentially creates a bias against the aposematic morph. Both prey types were equally novel for control birds and they should not have shown any biased reluctance for eating an aposematic prey. Knowledge of cryptic prey reduced the expected initial mortality of the conspicuous morph to a random level whereas control birds initially ate the conspicuous morph according to the visibility risk. Birds learned to avoid conspicuous prey in both treatments but knowledge of cryptic prey did not increase the rate of avoidance learning. Predators' knowledge of cryptic prey did not reduce the predation of the less conspicuous aposematic prey and additionally predators did not learn to avoid the less conspicuous prey. These results indicate that predator psychology, which was shown as reluctance for attacking novel conspicuous prey, might have been important in the evolution of aposematism.     

The influence of density on frequency-dependent food selection: a comparison of four experiments with wild birds

We compare the results of four experiments, conducted at different times and with different protocols, that explored the relationship between frequency-dependent selection and prey density in wild birds feeding on artificial populations of coloured baits. One (experiment 4) used pastry baits that differed only in the presence or absence of a red stripe, and this experiment provided no evidence for any kind of selective behaviour. The other three experiments used green and brown baits, and they all provided evidence for a trend towards increasing anti-apostatic selection with high densities (>100 baits m^–2). However, one of these (experiment 3) provided no evidence for frequency-dependent selection at low densities (0.5–20 baits m^–2), while the other two experiments concurred in suggesting a trend towards increasing apostatic selection with low densities (down to 2 baits m^–2). Together, these experiments both support and qualify the published findings of experiment 1 that frequency- dependent selection by wild birds on bait populations is modified by density. Experiment 4 indicates that frequency-dependent selection may break down entirely if bait types are too similar, while experiment 3 indicates that some details of this trend with density will depend either on the protocol used or on exogenous changes in the birds’ feeding behaviour. Received: 1 September 1999 / Accepted: 22 March 2000     

Does predation maintain eyespot plasticity in Bicyclus anynana?

The butterfly Bicyclus anynana exhibits phenotypic plasticity involving the wet-season phenotype, which possesses marginal eyespots on the ventral surface of the wings, and the dry-season form, which lacks these eyespots. We examined the adaptive value of phenotypic plasticity of B. anynana in relation to the defence mechanisms of crypsis and deflection. We assessed the visibility differences between spotless and spotted butterflies against backgrounds of brown (dry season) or green (wet season) leaves. Spotless butterflies were highly cryptic and less predated by adult bird predators than were spotted ones when presented against brown leaf litter. However, the advantage of crypsis disappeared in the wet-season habitat as both forms were equally visible. In later experiments, naive birds presented with resting butterflies in the wet-season habitat tended to learn more rapidly to capture spotless butterflies, suggesting a slight selective advantage of possessing eyespots. Moreover, marginal eyespots increased significantly the escape probability of butterflies that were attacked by naive birds compared to those attacked by adult birds, although there were no differences in prey capture success within naive predators. Our results show that natural selection acts against eyespots in the dry season, favouring crypsis, whereas in the wet season it may favour eyespots as deflective patterns.     

Countershading enhances crypsis with some bird species but not others

Although the theory of self-shadow concealing countershadingis over a century old, there are very few direct empirical teststo substantiate the prediction that prey that are dorsally darkenedand ventrally lightened (generally termed countershaded) sufferlower rates of attack than other prey. In this paper, we reportexperiments designed to determine whether artificial, countershadedprey are chosen by predators less often than those that areall light, all dark, or reverse shaded (i.e., dorsally lightenedand ventrally darkened). Artificial prey were presented in gardensand parks to free-living birds, either on white backgroundsor on backgrounds with some degrees of color matching. In oneexperiment, birds were unmarked, and in the other, they wereindividually identifiable. We found that in three experimentaltrials, countershaded baits were attacked at a rate not significantlydifferent from that of uniformly dark baits. In one experimentaltrial, countershaded baits were at some advantage. When we examinedthe data set for this trial more closely, it was apparent thatblackbirds were taking countershaded baits least often, butblue tits and robins conferred no special advantage to countershadedbaits. Hence, the efficacy of countershading may vary with speciesof predator.     

Conditions for the spread of conspicuous warning signals: a numerical model with novel insights

The initial evolution of conspicuous warning signals presents an evolutionary problem because selection against rare conspicuous signals is presumed to be strong, and new signals are rare when they first arise. Several possible solutions have been offered to solve this apparent evolutionary paradox, but disagreement persists over the plausibility of some of the proposed mechanisms. In this paper, we construct a deterministic numerical simulation model that allows us to derive the strength of selection on novel warning signals in a wide range of biologically relevant situations. We study the effects of predator psychology (learning, rate of mistaken attacks, and neophobia) on selection. We also study the how prey escape, predation intensity, number of predators, and abundance of different prey types affects selection. The model provides several important results. Selection on novel warning signals is number rather than frequency dependent. In most cases, there exists a threshold number of aposematic individuals below which aposematism is selected against and above which aposematism is selected for. Signal conspicuousness (which increases detection rate) and distinctiveness (which allows predator to distinguish defended from nondefended prey) have opposing effects on evolution of warning signals. A more conspicuous warning signal cannot evolve unless it makes the prey more distinctive from palatable prey, reducing mistaken attacks by predators. A novel warning signal that is learned quickly can spread from lower abundance more easily than a signal that is learned more slowly. However, the relative rate at which the resident signal and the novel signal are learned is irrelevant for the spread of the novel signal. Long-lasting neophobia can facilitate the spread of novel warning signals. Individual selection via the ability of defended prey to escape from predator is not likely to facilitate evolution of conspicuous warning signals if both the resident (cryptic) morph and the novel morph have the same escape probability. Predation intensity (defined as the proportion of palatable prey eaten by the predator) has a strong effect on selection. More intense predation results in strong selection against rare signals, but also strong selective advantage to common signals. The threshold number of aposematic individuals is lower when predation is intense. Thus, the evolution of warning signals may be more likely in environments where predation is intense. The effect of numbers of predators depends on whether predation intensity also changes. When predation intensity is constant, increasing numbers of predators raises the threshold number of aposematic individuals, and thus makes evolution of aposematism more difficult. If predation intensity increases in parallel with number of predators, the threshold number of aposematic individuals does not change much, but selection becomes more intense on both sides of the threshold.     

Wild birds prefer the familiar of striped and unstriped artificial prey

Previous work has shown that wild birds can become trained to search for a prey type on the basis of its colour. The experiments presented in this paper extended this work to two types of green artificial prey that were identical except for the presence or absence of a red stripe. Wild birds at six widely separated sites were trained on populations of one type and then were offered a choice between equal numbers of the familiar type and a second type. All the populations were presented on lawn backgrounds. The experiments were then repeated at each site with the birds being trained on the second prey type. The results showed that there was a consistent tendency for the familiar prey type to be overpredated and this was statistically significant. The behaviour described in this paper, if it occurs in nature, could lead to frequency-dependent (apostatic) selection and the maintenance of polymorphism in prey species in which the morphs are distinguished by colour patterns.     

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.     

Evidence for search image in blackbirds Turdus merula L.: long-term learning

The feeding behaviour of free-flying and captive blackbirds Turdus merula L. was observed over a number of days to investigate their ability to see cryptic food. Sequences of eight tests which contained equal numbers of ‘cryptic’ and ‘conspicuous’ tests were presented to the birds of the first two experiments. The blackbirds in experiment 1 increased their feeding rate for both cryptic and conspicuous food, which suggests that search images were not acquired but that the physical acts of feeding were perfected (or that they altered their acceptance of green food). In contrast, the ‘residual search time’ (the bird's total search time minus handling and movement times) decreased over the series of four tests with cryptic green prey, but remained constant over the four tests with conspicuous prey (experiment 2). The blackbirds exploited the cryptic prey using their previous experience of searching for such food. This suggests that search images can be effective over eight feeding sessions, spanning 4–30 days. Similar results were obtained over a 9-day period with four juvenile blackbirds in captivity (experiment 3). With experience they also became expert in their assessment of backgrounds set up without prey.     

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.