Ultraviolet signaling in a butterfly is preferred by females and conveys male genetic quality.

Indicator models of sexual selection posit that females chose males on the basis of traits that reveal male genetic quality and thereby enjoy increased offspring production. Here we report that females of the butterfly Eurema hecabe receive indirect benefits from choosing males based on their UV wing coloration, a heritable and condition-dependent trait in this species. We first used a large laboratory-bred pedigree to demonstrate a per-family association between inbreeding and male UV trait value. Females exerted choice for UV-bright males within this protocol, and average male UV trait value increased over six consecutive generations presumably due to such selection and despite an increasing rate of pedigree-wide inbreeding. We then experimentally imposed a standard strength of inbreeding upon lines of divergent male UV trait value. Inbreeding depressed the siring performance of low-UV treatment males more severely and resulted in a marginal reduction of their UV brightness, which rebounded sharply following subsequent outcrossing. These findings are consistent with the ornament-based signaling of genetic quality as a function of underlying individual-level mutational load.

The quantitative genetic basis of variation in sexual versus non-sexual butterfly wing colouration: autosomal, Z-linked, and maternal effects.

Viability indicator traits are expected to be integrated extensively across the genome yet sex-limited to ensure that any benefits are sexually concordant. Understanding how such expectations are accommodated requires elucidating the quantitative genetic architecture of candidate traits in and across the sexes. Here we applied an animal modelling approach to partition the autosomal, allosomal, and direct maternal bases of variation in sexual versus non-sexual dorsal wing colouration in the butterfly Eurema hecabe. The sexual colour trait-coherently scattered ultraviolet that is under strong directional selection due to female choice-is brighter and more expansive in males, and overlays non-sexual pigmentary yellow markings that otherwise dominate both wing surfaces in each sex. Our modelling estimated high and sexually equivalent autosomal variances for ultraviolet reflectance (furnishing h2 ~ 0.58 overall and ~0.75 in males), accompanied by smaller but generally significant Z-linked and maternal components. By contrast, variation in non-sexual yellow was largely attributed to Z-linked sources. Intersexual genetic correlations based upon the major source of variation in each trait were high and not different from 1.0, implying regulation by a pool of genes common to each sex. An expansive autosomal basis for ultraviolet is consistent with its hypothesized role as a genome-wide viability indicator and ensures that both sons and daughters will inherit their father's attractiveness.

How to generate and test hypotheses about colour: insights from half a century of guppy research.

Coloration facilitates evolutionary investigations in nature because the interaction between genotype, phenotype and environment is relatively accessible. In a landmark set of studies, Endler addressed this complexity by demonstrating that the evolution of male Trinidadian guppy coloration is shaped by the local balance between selection for mate attractiveness versus crypsis. This became a textbook paradigm for how antagonistic selective pressures may determine evolutionary trajectories in nature. However, recent studies have challenged the generality of this paradigm. Here, we respond to these challenges by reviewing five important yet underappreciated factors that contribute to colour pattern evolution: (i) among-population variation in female preference and correlated variation in male coloration, (ii) differences in how predators versus conspecifics view males, (iii) biased assessment of pigmentary versus structural coloration, (iv) the importance of accounting for multi-species predator communities, and (v) the importance of considering the multivariate genetic architecture and multivariate context of selection and how sexual selection encourages polymorphic divergence. We elaborate these issues using two challenging papers. Our purpose is not to criticize but to point out the potential pitfalls in colour research and to emphasize the depth of consideration necessary for testing evolutionary hypotheses using complex multi-trait phenotypes such as guppy colour patterns.

Additive genetic variation, but not temperature, influences warning signal expression in Amata nigriceps moths (Lepidoptera: Arctiinae).

Many aposematic species show variation in their color patterns even though selection by predators is expected to stabilize warning signals toward a common phenotype. Warning signal variability can be explained by trade-offs with other functions of coloration, such as thermoregulation, that may constrain warning signal expression by favoring darker individuals. Here, we investigated the effect of temperature on warning signal expression in aposematic Amata nigriceps moths that vary in their black and orange wing patterns. We sampled moths from two flight seasons that differed in the environmental temperatures and also reared different families under controlled conditions at three different temperatures. Against our prediction that lower developmental temperatures would reduce the warning signal size of the adult moths, we found no effect of temperature on warning signal expression in either wild or laboratory-reared moths. Instead, we found sex- and population-level differences in wing patterns. Our rearing experiment indicated that ~70% of the variability in the trait is genetic but understanding what signaling and non-signaling functions of wing coloration maintain the genetic variation requires further work. Our results emphasize the importance of considering both genetic and plastic components of warning signal expression when studying intraspecific variation in aposematic species.

Genotype-environment interaction reveals varied developmental responses to unpredictable host phenology in a tropical insect.

Understanding the genetic architecture of life history plasticity may inform resilience under environmental change, but relatively little is known for the inhabitants of unpredictable wet-dry tropical environments. Here, I explore the quantitative genetics of juvenile growth and development relative to hostplant phenology in the butterfly Eurema hecabe. Wet season generations of this species breed explosively on leguminous annuals whereas dry season generations subsist at low density upon an alternative perennial host. The wet-to-dry season transition is temporally unpredictable and marked by widespread host defoliation, forcing a large cohort of stranded larvae to either pupate prematurely or prolong development in the hope of renewed foliage production. A split-brood experiment demonstrated greater performance on high quality annual as opposed to perennial host foliage and a marked decline under the stressed conditions faced by stranded wet season larvae. Genetic variances for rates of growth and development were equivalent among high quality treatments but strikingly elevated under resource stress, and the associated cross-environment genetic correlations were indistinguishable from zero. The results demonstrate genotype-environment interaction involving both rank order and variance scale, thereby revealing genetic variance for norms of reaction that may reflect variable risk aversion given an unpredictable tropical host phenology.

Macroecological patterns in flower colour are shaped by both biotic and abiotic factors.

There is a wealth of research on the way interactions with pollinators shape flower traits. However, we have much more to learn about influences of the abiotic environment on flower colour. We combine quantitative flower colour data for 339 species from a broad spatial range covering tropical, temperate, arid, montane and coastal environments from 9.25ºS to 43.75ºS with 11 environmental variables to test hypotheses about how macroecological patterns in flower colouration relate to biotic and abiotic conditions. Both biotic community and abiotic conditions are important in explaining variation of flower colour traits on a broad scale. The diversity of pollinating insects and the plant community have the highest predictive power for flower colouration, followed by mean annual precipitation and solar radiation. On average, flower colours are more chromatic where there are fewer pollinators, solar radiation is high, precipitation and net primary production are low, and growing seasons are short, providing support for the hypothesis that higher chromatic contrast of flower colours may be related to stressful conditions. To fully understand the ecology and evolution of flower colour, we should incorporate the broad selective context that plants experience into research, rather than focusing primarily on effects of plant-pollinator interactions.

Predator chemical cues decrease attack time and increase metabolic rate in an orb-web spider.

Animals are able to assess the risk of predation and respond accordingly via behavioural and physiological changes. Web-building spiders are in the unique situation where they reside in the middle of their web and are therefore relatively exposed to predators. Thus, these spiders might moderate either their web-building behaviour or their behaviour on the web when exposed to the threat of predation. In this study, we experimentally explored how chemical cues from a predator influence foraging behaviour and metabolic rate in females of the orb-web spider Argiope keyserlingi We found that female spiders restricted their foraging time budget when exposed to the predator cues from a praying mantid: they responded 11% and 17% quicker to a vibratory stimulus compared with control and non-predator cues, respectively, and spent less time handling the prey. Moreover, spiders were less likely to rebuild the web under predator cues. Female A. keyserlingi exposed to the praying mantid cue significantly elevated their metabolic rate compared with the control group. Our findings revealed short-term modifications over the 2 week trials in foraging behaviour and the physiology of female spiders in response to predator cues. This study suggests that under predator cues the spiders move quicker and this could be facilitated by elevation in metabolic rate. Reduced foraging activity and less frequent web repair/rebuilding would also reduce the spiders' exposure to praying mantid predators.

Manipulation of natal host modifies adult reproductive behaviour in the butterfly Heliconius charithonia.

Advances in understanding non-genetic inheritance have prompted broader interest in environmental effects. One way in which such effects may influence adaptation is via the transmission of acquired habitat biases. Here I explore how natal experience influences adult host orientation in the oligophagous passion vine butterfly Heliconius charithonia. As an exemplar of the 'pupal mating' system, this species poses novelty among diurnal Lepidoptera for the extent to which male as well as female reproductive behaviours are guided by olfactory host cues. I sampled wild adult females breeding exclusively upon Passiflora incarnata, assigned their offspring to develop either upon this species or its local alternative Passiflora suberosa, and then assessed the behaviour of F1 adults in a large rainforest enclosure. Despite the fact that juvenile performance was superior upon P. incarnata, females oviposited preferentially upon their assigned natal species. Mate-seeking males also indicated a bias for the proximity of their natal host, and there was evidence for assortative mating based upon host treatment, although these data are less robust. This study is, to my knowledge, the first to support Hopkins' hostplant principle in butterflies, and points to inducible host preferences capable of reinforcing ecological segregation and ultimately accelerating evolutionary divergence in sympatry.

The effect of captive breeding upon adult thermal preference in the Queensland fruit fly (Bactrocera tryoni).

The Queensland fruit fly (Bactrocera tryoni) is a generalist pest that poses a significant threat to the Australian horticultural industry. This species has become broadly established across latitudes that encompass tropical to temperate climates, and hence populations occupy diverse thermal niches. Successful expansion across this range may have been brokered by evolutionarily labile features of breeding phenology, physiology and/or behaviour. We explored the potential role of behavioural flexibility by characterizing variation in adult thermal preference using a novel gradient apparatus. Flies oriented within this apparatus essentially at random in the absence of thermal variation, but sought and maintained precise positions when presented with an established gradient. Male and female flies from an 'old' colony (>300 generations) and a 'young' (F7) colony were compared. Whereas we found no difference between the sexes, flies from the young colony preferred higher temperatures (30.93 ±â€¯7.30 °C) and had greater individual variation than their counterparts from the old colony (28.16 ±â€¯5.63 °C). Given that B. tryoni are routinely maintained at 25 °C in the laboratory, a lower mean preference of the old colony is consistent with thermal adaptation. This is further supported by their reduced phenotypic variance, which follows as a logical consequence of stabilising selection given long-term environmental constancy. These results demonstrate that B. tryoni seek to thermoregulate via adult behaviour, and that individual temperature preference can be precisely measured using a gradient apparatus. The evidence for adaptive tuning of this behaviour has importance for both the design of captive rearing protocols as well as the prediction of invasive potential and species biogeography under future climatic variation.

Predictable adaptive trajectories of sexual coloration in the wild: Evidence from replicate experimental guppy populations.

The question of whether populations evolve predictably and consistently under similar selective regimes is fundamental to understanding how adaptation proceeds in the wild. We address this question with a replicated evolution experiment focused upon male sexual coloration in guppies (Poecilia reticulata). Fish were transplanted from a single high predation population in the Guanapo River to four replicate, guppy-free low predation headwater streams. Two streams had their canopies thinned to adjust the setting under which male coloration is displayed and perceived. We assessed evolutionary divergence using second-generation lab-bred offspring of fish sampled four to six years following translocation. A prior experiment of the same design, performed in an adjacent drainage, resulted in the evolution of more extensive orange, black, and iridescent markings. We however found evidence for expansion only in structural coloration (iridescent blue/green), no change in orange, and a reduction in black. This response amplifies earlier findings for Guanapo fish, revealing that trajectories of color elaboration differ among drainages. We also found that color phenotypes evolved more greatly at the thinned-canopy sites. Our findings support the predictability of sexual trait evolution in the wild, and underscore the importance of signaling conditions and ornamental starting points in shaping adaptive trajectories.

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.

Colour polymorphic lures exploit innate preferences for spectral versus luminance cues in dipteran prey.

BACKGROUND: 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. RESULTS: 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. CONCLUSION: 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 genetic basis of discrete and quantitative colour variation in the polymorphic lizard, Ctenophorus decresii.

BACKGROUND: Colour polymorphic species provide invaluable insight into processes that generate and maintain intra-specific variation. Despite an increasing understanding of the genetic basis of discrete morphs, sources of colour variation within morphs remain poorly understood. Here we use the polymorphic tawny dragon lizard Ctenophorus decresii to test simple Mendelian models for the inheritance of discrete morphs, and to investigate the genetic basis of continuous variation among individuals across morphs. Males of this species express either orange, yellow, orange surrounded by yellow, or grey throats. Although four discrete morphs are recognised, the extent of orange and yellow varies greatly. We artificially elevated testosterone in F0 females and F1 juveniles to induce them to express the male throat colour polymorphism, and quantified colour variation across the pedigree. RESULTS: Inheritance of discrete morphs in C. decresii best fit a model whereby two autosomal loci with complete dominance respectively determine the presence of orange and yellow. However, a single locus model with three co-dominant alleles for orange, yellow and grey could not be definitively rejected. Additionally, quantitative expression of the proportion of orange and yellow on the throat was strongly heritable (orange: h(2) = 0.84 ± 0.14; yellow: h(2) = 0.67 ± 0.19), with some evidence for covariance between the two. CONCLUSIONS: Our study supports the theoretical prediction that polymorphism should be governed by few genes of major effect, but implies broader genetic influence on variation in constituent morph traits.

Colour polymorphism.

White and Kemp introduce colour polymorphism in animals.

Color polymorphic lures target different visual channels in prey.

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

Information in the Biosphere: Biological and Digital Worlds.

Evolution has transformed life through key innovations in information storage and replication, including RNA, DNA, multicellularity, and culture and language. We argue that the carbon-based biosphere has generated a cognitive system (humans) capable of creating technology that will result in a comparable evolutionary transition. Digital information has reached a similar magnitude to information in the biosphere. It increases exponentially, exhibits high-fidelity replication, evolves through differential fitness, is expressed through artificial intelligence (AI), and has facility for virtually limitless recombination. Like previous evolutionary transitions, the potential symbiosis between biological and digital information will reach a critical point where these codes could compete via natural selection. Alternatively, this fusion could create a higher-level superorganism employing a low-conflict division of labor in performing informational tasks.

An integrative framework for the appraisal of coloration in nature.

The world in color presents a dazzling dimension of phenotypic variation. Biological interest in this variation has burgeoned, due to both increased means for quantifying spectral information and heightened appreciation for how animals view the world differently than humans. Effective study of color traits is challenged by how to best quantify visual perception in nonhuman species. This requires consideration of at least visual physiology but ultimately also the neural processes underlying perception. Our knowledge of color perception is founded largely on the principles gained from human psychophysics that have proven generalizable based on comparative studies in select animal models. Appreciation of these principles, their empirical foundation, and the reasonable limits to their applicability is crucial to reaching informed conclusions in color research. In this article, we seek a common intellectual basis for the study of color in nature. We first discuss the key perceptual principles, namely, retinal photoreception, sensory channels, opponent processing, color constancy, and receptor noise. We then draw on this basis to inform an analytical framework driven by the research question in relation to identifiable viewers and visual tasks of interest. Consideration of the limits to perceptual inference guides two primary decisions: first, whether a sensory-based approach is necessary and justified and, second, whether the visual task refers to perceptual distance or discriminability. We outline informed approaches in each situation and discuss key challenges for future progress, focusing particularly on how animals perceive color. Given that animal behavior serves as both the basic unit of psychophysics and the ultimate driver of color ecology/evolution, behavioral data are critical to reconciling knowledge across the schools of color research.

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.

Nature-via-nurture and unravelling causality in evolutionary genetics.

Quantitative geneticists traditionally attribute phenotypic variation to genetic or environmental sources. New findings with near-clonal mice raised in a single enriched environment demonstrated significant developmental and behavioural divergence. This suggests intriguing possibilities for how (epi)genomes and environments might interact to drive phenotypic individuality, thus shaping evolutionary pathways.