Colour polymorphic lures exploit innate preferences for spectral versus luminance cues in dipteran prey
© The Author(s). 2017
Received: 7 February 2017
Accepted: 8 August 2017
Published: 14 August 2017
Theory predicts that colour polymorphism may be favored by variation in the visual context under which signals are perceived. The context encompasses all environmental determinants of light availability and propagation, but also the dynamics of perception in receivers. Color vision involves the neural separation of information into spectral versus luminance channels, which often differentially guide specific tasks. Here we explicitly tested whether this discrete perceptual basis contributes to the maintenance of polymorphism in a prey-luring system. The orb-weaving spider Gasteracantha fornicata is known to attract a broad community of primarily dipteran prey due to their conspicuous banded dorsal signal. They occur in two morphs (“white” and “yellow”) which should, respectively, generate greater luminance and color contrast in the dipteran eye. Given that arthropods often rely upon luminance-versus-spectral cues for relatively small-versus-large stimulus detection, we predicted a switch in relative attractiveness among morphs according to apparent spider size.
Our experimental tests used colour-naïve individuals of two known prey species (Drosophila hydei and Musca domestica) in replicate Y-maze choice trials designed to manipulate the apparent size of spider models via the distance at which they are viewed. Initial trials confirmed that flies were attracted to each G. fornicata morph in single presentations. When given a simultaneous choice between morphs against a viewing background typical of those encountered in nature, flies exhibited no preference regardless of the visual angle subtended by models. However, when backgrounds were adjusted to nearer the extremes of those of each morph in the wild, flies were more attracted by white morphs when presented at longer range (consistent with a reliance on achromatic cues), yet were unbiased in their close-range choice.
While not fully consistent with predictions (given the absence of a differential preference for stimuli at close range), our results demonstrate an effect of apparent stimulus size upon relative morph attractiveness in the direction anticipated from present knowledge of fly visual ecology. This implies the potential tuning of G. fornicata morph signal structure according to a perceptual feature that is likely common across their breadth of arthropod prey, and complements recent observational work in suggesting a candidate mechanism for the maintenance of deceptive polymorphism through the exploitation of different visual channels in prey.
The maintenance of intraspecific diversity is of enduring interest in evolutionary biology. Colour polymorphisms have proven valuable for examining the causes and consequences of conspicuous variation [1–4]. Research on classic cryptic [5, 6], sexual , and mimicry [8–10] systems has done much to identify the selective processes that mediate the coexistence of discrete morphs. Divergent selection is one factor that has been implicated in the maintenance of stable polymorphisms (e.g. the Papilio dardanus and coral snake mimicry systems; [8, 11]).
In visual communication systems, the effectiveness of signals is shaped by the interaction between viewing environments and the perceptual systems of receivers [12, 13]. Variation in environmental features such as the spectral quality and/or intensity of available light will modify the appearance of a given signal design . When unpredictable, variation of this nature contributes ‘noise’ to signaling systems, which is a basic challenge for effective communication. In response, selection may favour more precise behavioural delivery of signals [14, 15], restricting displays only to favourable environmental conditions , or actively modifying viewing environments [17, 18].
A general possibility, formalised in sensory drive theory, is that variation in the components of signalling systems may favour signal polymorphism by generating distinct signalling ‘niches’ [19, 20]. This may be particularly applicable in static signalling contexts, such as prey attraction by sit-and-wait predators. In these cases, encounters with receivers are largely unpredictable—that is, they occur under variable visual conditions—and behavioural fine-tuning of signal delivery is largely unavailable. The signaling niche hypothesis is supported by evidence from sexual and aposematic systems in which selection for effective communication in heterogeneous environments has driven the diversification of visual signals [5, 21–25]. For example, recent experimental work has shown that the polymorphic warning colours of dyeing poison frogs (Dendrobates tinctorius) are differentially detectable to vertebrate predators under varied lighting conditions . This variation in ambient light occurs across fine spatial and temporal scales throughout the frogs’ natural forest habitat, which may favour the maintenance of signal polymorphism. Such work has, however, almost exclusively focused on abiotic sources of variation—such as light environments and viewing backgrounds—rather than potential biotic sources, including receiver perception .
Visual systems are typically equipped to extract both colour and luminance information from scenes, which often involves the use of specialised neural architectures . Birds, for example, process colour information by comparing the relative stimulation among sets of opposing photoreceptors (i.e., a cone-based opponency system), but largely rely on broadly tuned double-cones to perceive luminance (reviewed in ). Honeybees (Apis mellifera), in contrast, have three photoreceptor sub-types that are partly responsible for both tasks. Colour vision is based on the comparison of outputs from all three receptors, while luminance-based tasks are likely guided by outputs from the long-wavelength ‘green’ receptor [29–31]. Animals often (though not exclusively) use colour and luminance information to guide distinct visual tasks [27, 32–34]. Colour information is typically relied upon for the task of large-object detection and classification, for example, while luminance information may inform motion vision, as well as the perception of form and texture at a distance [27, 31–33, 35, 36; see further specific discussion in the methods].
From the perspective of signallers, the partitioning of visual information may offer alternate routes to visual conspicuousness through the enhancement of colour- or luminance-based contrast. This may be particularly true in noisy environments, wherein viewing conditions—and hence the demands on a visual system—can shift rapidly over small temporal and spatial scales . The conspicuous and often polymorphic visual lures of orb-web spiders (reviewed in ) offer excellent opportunities for examining this hypothesis. Their deceptive signals are statically displayed in visually noisy forest environments [12, 35], and we know little about the adaptive maintenance of polymorphism in this context.
We conducted a series of experiments using colour-naive Drosophila hydei and Musca domestica in a common “y-maze” apparatus (Additional file 1: Figure S1). This apparatus provided test subjects with the opportunity to orient towards one of two destinations according to the visual stimulus being presented in either arm (as broadly equivalent to a “binary choice test”). In order to test whether G. fornicata morphs are differentially attractive depending on the visual channel being prioritised, we sought to manipulate the visual channel being relied upon by varying the apparent size of model spiders presented to dipteran viewers (i.e. the visual angle subtended by models at the point at which they were first viewed; Additional file 1: Figure S1). This manipulation was informed by research across taxa (as outlined above) suggesting that a general feature of diurnal visual systems, including birds, bees, and primates, is the differential use of colour and luminance information depending on the apparent size of the stimulus. Achromatic cues are often used for the detection of stimuli subtending small visual angles, while stimuli spanning relatively larger visual angles are primarily identified using chromatic cues [31–33, 43, 44]. Given the weight of this assumption, we first conducted a pilot experiment to test whether innate preferences for colour and luminance cues in flies may alternate as a function of apparent stimulus size. We used a modified version of the choice assay outlined below, and our results are broadly consistent with the notion that D. hydei and M. domestica innately prefer achromatic cues at relatively small visual angles (10°), and chromatic cues at larger angles (50°; see Additional file 1 information for full details).
All D. hydei used in the experiments were first- to third- generation offspring of wild caught adults, and we did not differentiate sexes. We stored wild-caught adults in in 750 ml Pyrex glass storage bottles, with 100 ml of colourless food-culture lining the base. The culture was a 4.0:1.0:1.0:0.1 ratio of instant mashed potato, icing sugar, water, and yeast, and we removed F0 adults within 24 h of laying eggs. We purchased M. domestica as pupae from a commercial breeder (Pisces Enterprises, Queensland, Australia), and stored them in 750 ml Pyrex glass storage bottles until eclosion, with unlimited access to sugar-solution. We reared all flies in a temperature controlled laboratory (25 ± 2 °C) with a 14:10 L: D photoperiod, and used all individuals in experimental trials within four days of eclosion.
Experimental stimuli and environment
We conducted all experiments using the y-maze apparatus situated in a temperature-controlled laboratory (25 ± 1 °C) at Macquarie University, Australia. The maze consisted of a flight cage (400 × 300 × 300 mm; length, width, height) attached to two arms (1100 × 250 × 300 mm) at 90° (Additional file 1: Figure S1). The top of the maze was covered with a single sheet of clear screen (Rosco “Supergel 00”), which evenly transmits >95% of wavelengths in the 300–700 nm range. We illuminated the maze with a 400 W Sylvania metalarc-halogen light diffused with a single sheet of ultraviolet-transmitting Rosco 216 diffusion screen. This imitates natural overcast conditions (sensu [45, 46]) and represents a reasonable approximation of of possible illumination conditions under which G. fornicata are viewed in the wild (Fig. 1).
We ensured that models, backgrounds, and illuminants fell within natural ranges of intensity and colour (Fig. 1) by matching them to spectral measurements obtained previously for spiders at sites in North Queensland, Australia . All spectral measurements were taken using a JAZ EL-200 portable spectrometer fitted with a cosine-corrected irradiance module, and a PX-2 pulsed xenon light source (OceanOptics Ltd., Dunedin, USA). Reflectance was quantified using a “beam measurement” set-up (boxcar width = 10, integration time = 100 ms, scans to average = 10), as extensively used to measure G. fornicata specimens [35, 37]. This consisted of separate light source (PX-2) and collector probes situated at 90° and 45° relative to the sample plane, with a 99% diffuse “spectralon” reflectance standard used for calibration (Labsphere, New Hampshire) between samples. We captured the spectra via OceanOptics SpectraSuite software (ver. 1.6.0_11), and processed them using the development version of the package ‘pavo’ (ver. 1.0; ) for R (ver. 3.2.5; ). Following auto-calibration for ambient intensity, we recorded vector irradiance at a point immediately above and parallel to the top of the y-maze.
We conducted four separate experiments, varying the stimuli and backgrounds presented to receivers in each. In all experiments, spider models were presented in the centre of a 250 × 300 mm cardboard background (see further below for details). We varied the distance between the stimuli and the maze’s ‘choice point’ (D in Additional file 1: Figure S1) to control the visual angle subtended by the models (calculated using the left-right axis of model spiders) in nine increments: 1°, 6°, 11°, 16°, 21°, 26°, 31°, 36°, and 41°.
We initiated trials by introducing each colour-naive subject into an enclosed compartment at the head of the Y-maze. After three minutes of visual adaptation time we opened the entrance to the decision chamber and the flies, upon entering, were able to simultaneously view both arms. A decision was registered when the subject crossed the ‘choice’ line at the entrance to a maze arm (Additional file 1: Figure S1). We discarded individuals that did not leave the flight chamber within 10 minutes of the entrance opening (ca. 14% of M. domestica, and 6% of D. hydei). Model stimuli were randomly assigned across arms of the Y-maze, and the ordering of visual angles at which models were presented was randomised at the beginning of each experiment. We recorded the responses of 80 individuals of both D. hydei and M. domestica at each visual angle, and did not re-use individuals; each fly made a single choice. We therefore used 80 individuals at each of nine apparent model sizes, totalling 720 individuals/choices per species in each experiment.
Experiments 1 and 2: Spider models versus plain backgrounds
In experiments one and two we offered flies a choice between either a yellow (experiment 1) or white (experiment 2) spider model versus a background with no spider model. The card background in these experiments approximated the visual average for this species as measured in extensive field sampling , that is, the averaged spectrum presented by visual backgrounds of G. fornicata in the wild. The purpose of this was twofold. First, it allowed us to assess the baseline attractiveness (if any) of each G. fornicata morph to naive receivers, as a function of apparent model size. Second, it allowed us to determine the point at which receivers no longer responded to the models, which we expected to occur at or near visual angles on the order of the spacing of individual ommatidia (ca. 1–11°; [49–52]).
Experiments 3 and 4: Yellow versus white spider models against “average” versus “augmented” backgrounds
These two experiments aimed to test the hypothesis that flies should orient preferentially towards yellow morphs when relying on chromatic cues, and white morphs when guided by achromatic cues. If M. domestica and D. hydei alternate their reliance on colour-versus-luminance information as a function of apparent stimulus size (as discussed above and supported by the pilot experiment; see Additional file 1), this hypothesis predicts that subjects will be attracted to yellow morphs at relatively larger visual angles but shift towards white morphs at relatively smaller visual angles (across both experiments).
The broadly estimated chromatic (unitless) and achromatic (Michelson) contrast of model spider morphs against their backgrounds in all experiments, as modelled according to the visual systems of D. melanogaster and M. domestica (Additional file 1)
We used goodness of fit tests (G-tests) of homogeneity throughout to test for deviations from equal-choice frequency as a function of the visual angle at which models were presented. When significant heterogeneity was detected, we used a-posteriori simultaneous G-tests for homogeneity to identify which sets of responses differed from one another . Briefly, this entailed a stepwise testing procedure wherein the response data, beginning with the largest visual angle category (41°), were cumulatively grouped into sets and tested for homogeneity (against a critical G-value adjusted for multiple comparisons). In experiment 1, for example, the 41° and 36° response-categories were first tested, then the 31° data were added to this set and retested, and so on. This continued until a maximally non-significant set was found, at which point we repeated the procedure in reverse, moving from the smallest-to-largest visual angle category. This procedure allowed us to identify any significant shifts in the attractiveness of model spiders as a function of visual cues being prioritised by receivers’ visual systems (e.g. Fig. 2). In experiments one and two, we expected at least one change-point corresponding to the apparent model size at which flies no longer respond to stimuli. In experiments three and four, our hypothesis (as discussed above) predicts that yellow morphs should be relatively more attractive at larger apparent sizes, while white morphs should be relatively more attractive at smaller sizes, though the precise point at which this should occur cannot be predicted a-priori. We excluded tests at the 1° and 6° visual angles in experiments three and four because the first two experiments established no effective response to stimuli subtending less than 11°.
Experiments 1 and 2: Spider models versus plain backgrounds
Summary of a-posteriori simultaneous tests for homogeneity, from experiments 1 and 2 in which flies were offered the choice of spider models were presented versus a plain background
Experiment 1 (White model vs plain bkg)
Experiment 2 (Yellow model vs plain bkg)
Simultaneous test set (visual angle category)
We found qualitatively identical results in experiment two. Yellow G. fornicata were attractive to D. hydei (G8 = 28.63, P < 0.001) and M. domestica (G8 = 22.11, P = 0.005), but only once they subtended visual angles >11° across a range of apparent model sizes (Fig. 2b). This too was consistent at presentation angles of 11–41°, and fell to equality at 6° or less (Fig. 2b; Table 2).
Experiments 3 and 4: Yellow versus white spider models against “average” versus “augmented” backgrounds
Summary of a-posteriori simultaneous tests for homogeneity, from experiment 4 in which flies were offered the simultaneous choice of yellow or white-banded spider models, presented versus an “augmented” background
Simultaneous test set (visual angle category)
Theory predicts that variation in selection may maintain intraspecific diversity, including polymorphism [54, 55]. Signalling environments and the perceptual systems of receivers are sources of ample variation known to drive intraspecific diversity, albeit chiefly in sexual ornaments [21, 24, 56]. Here we tested the potential for conditional use of visual information in receivers to favour colour polymorphism in a prey-lure context. We found evidence that each G. fornicata morph appeals to innate spectral and luminance biases in dipteran prey (which may include simple stimulus-presence; Fig. 2), at least relative to a non-stimulus background. However, the central prediction—that yellow and white morphs should differentially exploit colour and luminance preferences, respectively—was only partly supported by our data. Although relative morph attractiveness did vary depending on the visual cues putatively prioritised by flies’ visual systems (i.e., as a function of apparent model size), this effect was conditional upon the relative magnitude of signal/background visual contrast between morphs (Fig. 3). We expand upon these results in discussion of how interactions between signal structure, signalling environments, and innate receiver biases may favour colour-lure polymorphism.
Our finding that the colour-lures of G. fornicata are attractive to dipteran prey (Fig. 2) is not surprising. Flies are known to orient towards yellow and non-ultraviolet-white stimuli (reviewed in ), and such stimuli have known efficacy across a range of prey luring taxa [36, 57–61]. Precisely which biases are exploited is, however, poorly understood. Our use of colour-naive viewers suggests that innate visual biases, at least in part, underlie the attractiveness of deceptive lures across a range apparent lure sizes. Of course we cannot be certain the innate attractiveness of G. fornicata models was driven by their (UV-negative) yellow or white signals specifically (since these were the only two colours tested), though these results are consistent with the known colour preferences of flies, as discussed above. Experiments one and two also indicated that the absolute strength of preference was strikingly consistent (at ca. 70%) for each morph until the apparent size of models was reduced below 11° (Fig. 2). The loss of attractiveness at smaller visual angles most likely occurred because model size approached the limits of visual resolution in both fly species [49–51]. Our results also imply that both the chromatic and achromatic components of lures are innately attractive to prey; a subtlety that cannot be informed by semi-natural experiments in comparable systems given their inherent lack of precision control over viewing conditions [36, 57, 58]. Because we only have a broad sense of when colour and luminance information might be differentially favoured by flies (see pilot experiment; Additional file 1), we cannot identify the precise conditions under which prey preferences are driven by either cue. These findings nonetheless indicate that both chromatic and achromatic components of deceptive lures are likely targeted by selection for signal efficacy.
Experiments three and four revealed a shifting and at times differential degree of attractiveness among G. fornicata morphs according to signalling conditions (Fig. 3). This is broadly consistent with the principles of sensory drive , but deviates partly from our specific predictions regarding the contextual attractiveness of yellow and white morphs. When presented against a background designed to imitate an average visual scene, morphs were equally attractive to both D. hydei and M. domestica irrespective of visual angle (Fig. 3a). When instead presented against a background that further enhanced the relative (not absolute) luminance contrast of white models and colour contrast of yellow models, white morphs proved distinctly more attractive at smaller visual angles (Fig. 3b). Such angles represent smaller stimulus sizes (indeed, nearing the apparent limit of visual resolution), and therefore typify the task of longer-range orientation when flies are thought to be guided by luminance cues .
We found no support, however, for the predicted greater relative attractiveness of yellow morphs at any larger visual angle (Fig. 3b). This finding has several potential (non-exclusive) explanations. One possibility is simply that neither M. domestica nor D. hydei are able to discriminate between morphs based on chromatic cues, irrespective of the backgrounds against which they are presented. While there is evidence that some flies, such as the blowfly Lucilia sp., have a relatively poor colour-sense [62, 63], this finding is inconsistent across fly taxa. Behavioural tests with D. melanogaster [64, 65], for example, suggest an ability to discriminate between stimuli based on their spectral properties, with optimal performance at the 420 and 490 nm wavelength regions (which coincide with the approximate regions of difference between G. fornicata morphs; Fig. 1). While the implications of these studies for our understanding of dipteran colour discrimination is limited by their use of self-luminous stimuli (discussed in ), it is plausible that D. hydei and M. domestica can discriminate between simultaneously presented models on the basis of colour. A related possibility is that the differential increase in chromatic contrast for yellow morphs in experiment four was too subtle to elicit the predicted increase in relative attractiveness at larger visual angles (Fig. 3b). Assessing this possibility would again require an understanding of the limits of colour discrimination in flies, as well as assays across a great chromatic span of model/background combinations. Finally, as discussed below, the equal attractiveness of morphs at larger presentation angles may reflect genuinely equivalent stimulation under the conditions tested.
Our finding that the relative attractiveness of colour-lure morphs is shaped by an interaction between signal structure, signalling conditions, and receiver visual ecology (Fig. 3) is consistent with the hypothesis that signalling ‘niches’ may emerge as product of variation in the components of communication systems [19, 20]. While the data hint at a consistently greater fitness benefit for white morphs (as they proved equally or more attractive than yellow morphs under all tested conditions; Fig. 3), our assay environments were greatly oversimplified relative to the complexity of natural conditions. The spectral quality and intensity of light, particularly in forests, regularly shifts by orders of magnitude over small spatial (e.g. under patchy canopies) and temporal (e.g. with weather conditions) scales [13, 20]. Receivers’ visual and cognitive systems are similarly changeable. Colour perception may vary with the state of adaptation in photoreceptors, and the attentiveness of receivers will shift based on internal (e.g. hunger) and external (e.g. the presence of potential mates or predators) motivations [19, 66].
The most significant unexplored axis of variation was receiver experience. Controlled behavioural experiments have shown that the use of colour and luminance cues may be relatively plastic, with the attractiveness of colourful versus luminant stimuli shifting based on the past experience of receivers [67, 68]. With specific reference to flies, Troje  examined the responses of naive and trained blowflies to monochromatic stimuli that differed in intensity, and found that the intensity of the stimulus drove innate, but not trained, colour preferences. An intriguing possibility in case of G. fornicata, then, is that while white morphs are disproportionately attractive to naive receivers guided by luminance cues (Fig. 3b), the attractiveness of yellow morphs may be more strongly determined by receivers’ learned experience with coloured stimuli. As pollinators, M. domestica and D. hydei would be exposed to rewarding flowers over the course of their lifetime. Indeed, the signals of many polymorphic spiders, including G. fornicata, are known to resemble sympatric flowers , which may predictably shape the attractiveness of G. forniatica morphs depending on the structure of local floral communities. Determining the relative contributions of innate (colour-naive), spontaneous (colour-experienced, but untrained) and learned (plastic) biases in the maintenance of lure-polymorphism would require experiments across a range of receiver experience, for which the highly tractable orb-web spiders are exceptionally well suited.
Visual signalling systems contain ample sources of variation that may contribute to the maintenance of colour polymorphism. While the role of abiotic variation in establishing ‘signalling niches’ is well supported [21–25], the question of whether perceptual variation may contribute in a similar manner is largely unexamined. In the first direct test of the possibility, our results implicate the conditional prioritisation of visual information in receivers as a likely contributing factor to the maintenance of colour polymorphism in a deceptive context. While not fully consistent with predictions, our results demonstrate an effect of apparent stimulus size upon relative morph attractiveness in the direction anticipated from present knowledge of fly visual ecology . The discrete signals of G. fornicata may thus be tuned according to a perceptual feature that is common across their breadth of arthropod prey. This complements recent observational work  in suggesting an unappreciated avenue for the maintenance of polymorphism through the exploitation of different visual channels in receivers.
We thank Devi Stuart-Fox, Leo J. Fleishman, and Erik Svensson for valuable comments. TEW thanks Elizabeth Mulvenna and Cormac White for all their support.
TEW was supported by an Australian Postgraduate Award. DJK was supported by the Australian Research Council (grant DP140104107).
Availability of data and materials
All data are available via Figshare (https://doi.org/10.6084/m9.figshare.5306080.v1).
TEW and DJK designed the study, analysed the data, and critically revised the manuscript. TEW collected the data and wrote the manuscript. Both authors read and approved the final manuscript.
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