Thomas E. White

Signal design and courtship presentation coincide for highly biased delivery of an iridescent butterfly mating signal

Sensory drive theory contends that signaling systems should evolve to optimize transmission between senders and intended receivers, while minimizing visibility to eavesdroppers where possible. In visual communication systems, the high directionality afforded by iridescent coloration presents underappreciated avenues for mediating this trade‐off. This hypothesis predicts functional links between signal design and presentation such that visual conspicuousness is maximized only under ecologically relevant settings and/or to select audiences. We addressed this prediction using Hypolimnas bolina, a butterfly in which males possess ultraviolet markings on their dorsal wing surfaces with a narrow angular reflectance function. Males bearing brighter dorsal markings are increasingly attractive to females, but also likely more conspicuous to predators. Our data indicate that, during courtship (and given the ritualized wingbeat dynamics at these times), males position themselves relative to females in such a way as to simultaneously maximize three components of known or putative signal conspicuousness: brightness, area, and iridescent flash. This suggests that male signal design and display have coevolved for the delivery of an optimally conspicuous signal to courted females. More broadly, these findings imply a potential signaling role for iridescence itself, and pose a novel example for how signal design may coevolve with the behavioral context of display.

Sexual signals for the colour-blind: cryptic female mantids signal quality through brightness

Summary Cryptic coloration may evolve in response to selective pressure imposed by predators, yet effective intraspecific communication may require some level of detectability. This creates a tension between the benefits of sexually selected visual traits and the predatory costs imposed by greater conspicuousness, and little is known about how this tension may be ameliorated in highly cryptic species. We explore these competing demands in the false garden mantid Pseudomantis albofimbriata, a colour-blind and seemingly cryptic insect. We use reflectance spectrometry and receptor-noise modelling to characterize the conspicuousness of mantid body regions in the visual systems of mates (mantids), as well as potential predators (birds) and prey (bees). We then use condition manipulation and conspecific choice tests to further explore the colour traits of interest. Based on visual modelling, we find that male mantids are inconspicuous to conspecifics, prey and predators – that is, they are chromatically and achromatically cryptic. In contrast, female mantids are chromatically cryptic to all potential receivers, but their abdomens are achromatically conspicuous. Our food manipulation experiment shows that females in good condition (and therefore with more eggs) have brighter abdomens than females in poor condition. Choice assays show male mantids are consistently attracted to females bearing brighter abdomens. Our results reveal brightness-mediated sexual signalling in a colour-blind and classically cryptic insect. By communicating in the only visual channel available to them, female mantids are conspicuously signalling their quality to mates, while potentially minimizing their conspicuousness to predators and prey. Furthermore, by signalling with only a single body region, female mantids are apparently using coincident disruptive coloration to further decrease detectability to potential eavesdroppers. Our data reveal a novel example of the way in which the trade-off between sexual selection for conspicuousness and natural selection for crypsis may be mediated in a visual signalling system. Such signals may be common in apparently cryptic species, and this study once again demonstrates the importance of analysing visual signals beyond the capacity of human vision.

Reproducible research in the study of biological coloration

The study of colour in nature has generated insights intofundamental evolutionary and ecological processes, and researchinto colour traits is a rapidly growing field (Kelber & Osorio, 2010).Theongoinginterestinbiologicalcolorationhasinpartbeendrivenby the increased availability of key technologies, including spec-trometry and photography, and concurrent advances in methodsfor analysing colour data, such as visual models (e.g. Endler M Kelber, Vorobyev, & Osorio, 2003; Stevens, Parraga,Cuthill, Partridge, & Troscianko, 2007). While these developmentsare positive for the field, the increasingly complex analyses beingrun on ever greater amounts of data heighten the need forcomprehensive methods reporting and diligent data management(Alsheikh-Ali, Qureshi, Al-Mallah, & Ioannidis, 2011; Nekrutenko T Van Noorden, 2011; Whitlock, 2011). Astudy may be considered truly reproducible when it satisfies threebroad criteria: (1) methods are reported completely, (2) data arepubliclyavailable and archived,and (3) the chain of modification ofraw data is documented and preserved. While completely repro-ducible research (e.g. FitzJohn et al., 2014) is a laudable goal, theconsiderable demands it imposes on researchers means that it willoften, in practice, be unattainable. Nevertheless, even partialreproducibility through the relatively simple practices of completemethodsreportingandpublicdataarchivingisoftremendousvalue.Our aim was to explore the state of reproducibility in the studyofbiological coloration, and to suggest simpleways inwhich it maybe improved. We first outline common methods for studying bio-logical coloration and present guidelines for comprehensivemethods reporting. We then explore how well some of theseimportant criteria have been reported in the literature. We alsoquantify the availability of publicly archived data and code andsuggest some useful tools for increasing the reproducibility ofcolour trait research more broadly.

Technicolour deceit: A sensory basis for the study of colour-based lures

The study of deceptive signalling has provided compelling insights into evolutionary and ecological processes. Aside from mimicry, however, research into the use of colour as a deceptive instrument has progressed largely without an explicit theoretical basis. This is especially true for colour-based prey lures, that is, displays of colour used by predators to actively attract and deceive prey. Such lures are widespread and phenotypically diverse, and a valuable body of research has laid the foundation for novel tests of evolutionary theory in these systems. In this review, we aim to cast the study of colour-based luring under a theoretical framework centred on sensory drive, and outline hypotheses and predictions that may guide future work. We first discuss the principles of sensory drive theory, and briefly review its relevance and use in colour lure research. Notably, although rarely framed in explicit sensory drive terms, many studies consider questions highly relevant to this theory, such as the influence of signalling environments on lure evolution. We then highlight how hypotheses drawn from sensory drive theory may guide the study of intriguing features of colour lure systems. To that end, we review the empirical literature with a focus on two key areas: signal function and the evolution and maintenance of polymorphism. We examine the predictions of the relevant model of signal function, sensory traps, against the limited literature evidence in orb-web spiders, and find little support, at present, for the common contention that lures act as sensory traps via floral mimicry. Finally, we suggest that just as a more explicit consideration of sensory drive theory may allow new or broader insights into colour lure evolution, the study of lure systems offers unique opportunities to test theory in visual ecology, predator–prey dynamics and the evolution of polymorphism.

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. fornicatas visual environments. These findings suggest that color polymorphism may be adaptively maintained by selection for conspicuousness within different visual channels in receivers.

Deimatism: a neglected component of antipredator defence

Deimatic or ‘startle’ displays cause a receiver to recoil reflexively in response to a sudden change in sensory input. Deimatism is sometimes implicitly treated as a form of aposematism (unprofitability associated with a signal). However, the fundamental difference is, in order to provide protection, deimatism does not require a predator to have any learned or innate aversion. Instead, deimatism can confer a survival advantage by exploiting existing neural mechanisms in a way that releases a reflexive response in the predator. We discuss the differences among deimatism, aposematism, and forms of mimicry, and their ecological and evolutionary implications. We highlight outstanding questions critical to progress in understanding deimatism.

The perceptual similarity of orb-spider prey lures and flower colours

Receiver biases offer opportunities for the evolution of deception in signalling systems. Many spiders use conspicuous body colouration to lure prey, yet the perceptual basis of such deception remains largely unknown. Here we use knowledge of visual perception in key pollinator groups (bees and flies) to test whether colour-based lures resemble floral signals. We addressed this question at two levels: first according to the spectral reflectance of Australian orb-web spiders and flowers across a broad continental range, and second in reference to polymorphic variation in the species Gasteracantha fornicata. Analysis at the community level supported the hypotheses for broad-scale convergence among spider and flower signals. Moreover, data for G. fornicata indicate that each lure morph presents a signal biased towards the colouration of sympatric flowers. This analysis identified fly- and/or bee-pollinated plants whose flowers are likely to be indistinguishable from each G. fornicata colour morph. Our findings support the hypothesis that deceptive colour-based lures exploit prey preferences for floral resources. Further, the evidence implies a greater role for specific model/mimic relationships over generalised resemblance to flower-like stimuli as a driver of lure colouration and diversity.

Colour and luminance contrasts predict the human detection of natural stimuli in complex visual environments

Much of what we know about human colour perception has come from psychophysical studies conducted in tightly-controlled laboratory settings. An enduring challenge, however, lies in extrapolating this knowledge to the noisy conditions that characterize our actual visual experience. Here we combine statistical models of visual perception with empirical data to explore how chromatic (hue/saturation) and achromatic (luminant) information underpins the detection and classification of stimuli in a complex forest environment. The data best support a simple linear model of stimulus detection as an additive function of both luminance and saturation contrast. The strength of each predictor is modest yet consistent across gross variation in viewing conditions, which accords with expectation based upon general primate psychophysics. Our findings implicate simple visual cues in the guidance of perception amidst natural noise, and highlight the potential for informing human vision via a fusion between psychophysical modelling and real-world behaviour.

Comparing colors using visual models

An outstanding challenge for the study of color traits is how best to use “colour spaces” to represent their visual perception, particularly when asking questions of color difference (e.g. the (dis)similarity of males and females, mimics and models, or sister species, to a given viewer). We use simulations to show that existing methods fail to statistically and biologically estimate the separation of groups in color space, and we suggest a flexible, robust, alternative that avoids those pitfalls.

The nanoanatomical basis of sexual dimorphism in iridescent butterfly colouration

Abstract. Structurally generated colours are at least as commonplace and varied components of animal signals as pigment colours, yet we know far less about the former, both in terms of the patterns and phenotypic variation and of their underlying correlates and causes. Many butterflies exhibit bright and iridescent colour signals that arise from a characteristic ‘ridge-lamellar’ scale surface nanoarchitecture. Although there are multiple axes of functional variation in these traits, few have been investigated. Here we present evidence that sexual dimorphism in the expression of a sexually homologous ridge-lamellar trait (iridescent ultraviolet) is mediated by sex differences in the density of lamellar-bearing scale ridges. This trait – ridge density – has also been causally related to iridescent signal variation in other coliadines (e.g. C. eurytheme), which suggests that it may offer a common basis to both intra- and intersexual differences in ultraviolet wing reflectance among these butterflies.