In the eyes of the beholders: Female choice and avian predation risk associated with an exaggerated male butterfly color

Color ornaments are often viewed as products of countervailing sexual and natural selection, because more colorful, more attractive individuals may also be more conspicuous to predators. However, while evidence for such countervailing selection exists for vertebrate color ornaments (e.g., Trinidadian guppies), similar studies have yet to be reported in invertebrates. Indeed, evidence for female mate choice based on extant variation in male coloration is limited in invertebrates, and researchers have not explicitly asked whether more attractive males are also more conspicuous to predators. Here we provide evidence that more chromatic male cabbage white butterflies (Pieris rapae) are more attractive to females but should also be more conspicuous to predators. Female P. rapae preferentially mate with more chromatic males when choosing from populations of males with naturally occurring or commensurate, experimentally induced color variation. Mathematical models of female color vision confirm that females should be able to discriminate color differences between prospective mates. Further, chromatic and luminance contrast scores from female visual system models better predicted male mating success than did measures of male color derived more directly from color spectra. Last, models of avian color vision suggest that preferred males should be more conspicuous to known avian predators.     

Patterns on the insect wing

The evolution of wings and the adaptive advantage they provide have allowed insects to become one of the most evolutionarily successful groups on earth. The incredible diversity of their shape, size, and color patterns is a direct reflection of the important role wings have played in the radiation of insects. In this review, we highlight recent studies on both butterflies and Drosophila that have begun to uncover the types of genetic variations and developmental mechanisms that control diversity in wing color patterns. In butterflies, these analyses are now possible because of the recent development of a suite of genomic and functional tools, such as detailed linkage maps and transgenesis. In one such study, extensive linkage mapping in Heliconius butterflies has shown that surprisingly few, and potentially homologous, loci are responsible for several major pattern variations on the wings of these butterflies. Parallel work on a clade of Drosophila has uncovered how cis-regulatory changes of the same gene correlate with the repeated gain and loss of pigmented wing spots. Collectively, our understanding of formation and evolution of color pattern in insect wings is rapidly advancing because of these recent breakthroughs in several different fields.     

Spot distribution in the meadow brown butterfly, Maniola jurtina L. (Lepidoptera: Satyridae): South Welsh populations

Meadow brown butterflies, Maniola jurtina , were studied on Skokholm Island, off the Pembrokeshire coast, from 1976 to 1978 and at six other sites in south Wales from 1973 to 1977.
Daily survival of butterflies on Skokholm was estimated by capture-recapture data to be 0.70–0.84, but these values may be low because in the year of detailed study, 1976, dispersal rates between study sites were high and increased through the emergence period.
The butterflies were scored for the number and placing of the hind wing spots (Ford, 1975). Female populations in the east of our study area resembled English populations for they were unimodal at 0 spots. Spotting increased westwards until on Skokholm and the adjacent mainland the females caught were roughly equally likely to have 0, 1 or 2 spots. The Skokholm male populations had many 3-spotted individuals and so the mode of 2 in the spot-frequency distribution was less clear cut that in English populations. The trends in south Wales therefore resemble those found along the Cornish peninsula and on the Isles of Scilly. We suggest the increasingly maritime climate and the fragmentation of habitat on the coastal fringes of the species range are factors which may selectively favour butterflies with high flying and dispersal ability. Brakefield (1983) has offered evidence that more highly spotted meadow browns indeed have such an ability.     

The significance of wing pattern diversity in the Lycaenidae: mate discrimination by two recently diverged species

Closely related species of lycaenid butterflies are determinable, in part, by subtle differences in wing pattern. We found that female wing patterns can act as an effective mate‐recognition signal in some populations of two recently diverged species. In field experiments, we observed that males from a Lycaeides idas population and an alpine population of L. melissa preferentially initiate courtship with conspecific females. A morphometric study indicated that at least two wing pattern elements were important for distinguishing the two species: hindwing spots and orange crescent‐shaped pattern elements called aurorae. We deceived male L. idas into initiating courtship with computer generated paper models of heterospecific females when these pattern elements were manipulated, indicating that the wing pattern elements that define the diversity of this group can be effective mate recognition signals.     

Conspicuous male coloration impairs survival against avian predators in Aegean wall lizards,Podarcis erhardii

Animal coloration is strikingly diverse in nature. Within‐species color variation can arise through local adaptation for camouflage, sexual dimorphism and conspicuous sexual signals, which often have conflicting effects on survival. Here, we tested whether color variation between two island populations of Aegean wall lizards (Podarcis erhardii) is due to sexual dimorphism and differential survival of individuals varying in appearance. On both islands, we measured attack rates by wild avian predators on clay models matching the coloration of real male and female P. erhardii from each island population, modeled to avian predator vision. Avian predator attack rates differed among model treatments, although only on one island. Male‐colored models, which were more conspicuous against their experimental backgrounds to avian predators, were accordingly detected and attacked more frequently by birds than less conspicuous female‐colored models. This suggests that female coloration has evolved primarily under selection for camouflage, whereas sexually competing males exhibit costly conspicuous coloration. Unexpectedly, there was no difference in avian attack frequency between local and non‐local model types. This may have arisen if the models did not resemble lizard coloration with sufficient precision, or if real lizards behaviorally choose backgrounds that improve camouflage. Overall, these results show that sexually dimorphic coloration can affect the risk of predator attacks, indicating that color variation within a species can be caused by interactions between natural and sexual selection. However, more work is needed to determine how these findings depend on the island environment that each population inhabits.     

Butterfly Wings Are Three-Dimensional: Pupal Cuticle Focal Spots and Their Associated Structures in Junonia Butterflies

Butterfly wing color patterns often contain eyespots, which are developmentally determined at the late larval and early pupal stages by organizing activities of focal cells that can later form eyespot foci. In the pupal stage, the focal position of a future eyespot is often marked by a focal spot, one of the pupal cuticle spots, on the pupal surface. Here, we examined the possible relationships of the pupal focal spots with the underneath pupal wing tissues and with the adult wing eyespots using Junonia butterflies. Large pupal focal spots were found in two species with large adult eyespots, J. orithya and J. almana, whereas only small pupal focal spots were found in a species with small adult eyespots, J. hedonia. The size of five pupal focal spots on a single wing was correlated with the size of the corresponding adult eyespots in J. orithya. A pupal focal spot was a three-dimensional bulge of cuticle surface, and the underside of the major pupal focal spot exhibited a hollowed cuticle in a pupal case. Cross sections of a pupal wing revealed that the cuticle layer shows a curvature at a focal spot, and a positional correlation was observed between the cuticle layer thickness and its corresponding cell layer thickness. Adult major eyespots of J. orithya and J. almana exhibited surface elevations and depressions that approximately correspond to the coloration within an eyespot. Our results suggest that a pupal focal spot is produced by the organizing activity of focal cells underneath the focal spot. Probably because the focal cell layer immediately underneath a focal spot is thicker than that of its surrounding areas, eyespots of adult butterfly wings are three-dimensionally constructed. The color-height relationship in adult eyespots might have an implication in the developmental signaling for determining the eyespot color patterns.     

INTRASEXUAL COMPETITION ALONE FAVORS A SEXUALLY DIMORPHIC ORNAMENT IN THE RUBYSPOT DAMSELFLY HETAERINA AMERICANA

I studied the sex-limited red spots on the wings of male rubyspot damselflies (Hetaerina americana) in relation to territoriality and fitness in the wild. Both observational and experimental (wing spot manipulation) studies indicated that wing spots were selected through competition among males for mating territories, not through female choice or direct competition for females. Males with naturally or artificially large wing spots were more successful at holding territories and consequently mated at higher rates than males with relatively small wing spots. In contrast, sexual selection on male body size appeared to operate among nonterritorial males at the clasping stage of the mating sequence, perhaps because larger males were better at clasping females forcibly. Of four models proposed to explain the evolution of ornaments through territory competition, only the agonistic handicap model makes predictions consistent with the results of this study.     

Dorsal Forewing White Spots of Male <Emphasis Type="Italic">Papilio polytes</Emphasis>(Lepidoptera: Papilionidae) not Maintained by Female Mate Choice

Palatable animals sometimes mimic the color patterns of noxious animals to gain protection from predators. This phenomenon, known as Batesian mimicry, is seen in many butterflies of the genus Papilio, and in some species the mimicry is limited to females. Although female-limited Batesian mimicry has been hypothesized to be caused by females preferring to mate with non-mimetic males, this hypothesis is rarely tested. In this study, we tested whether female mate choice is driving female-limited Batesian mimicry in Papilio polytes. Males have white spots on the dorsal forewings, which are absent in mimetic female sand in the toxic model, Pachliopta aristolochiae. Hence, we conducted mate choice experiments to examine whether these white spots are important to females. We offered females a choice of males with intact dorsal forewing white spots and males with artificially blackened dorsal forewings, resembling the model. Females did not show a preference for males with the white spots, suggesting that they are not being maintained by female mate choice. Future studies should investigate the presence of female mate choice on other parts of males’ wings to further understand the role of female mate choice, as well as explore other factors driving female-limited mimicry in these butterflies.     

UV photoreceptors and UV-yellow wing pigments in Heliconius butterflies allow a color signal to serve both mimicry and intraspecific communication

Mimetic wing coloration evolves in butterflies in the context of predator confusion. Unless butterfly eyes have adaptations for discriminating mimetic color variation, mimicry also carries a risk of confusion for the butterflies themselves. Heliconius butterfly eyes, which express recently duplicated ultraviolet (UV) opsins, have such an adaptation. To examine bird and butterfly color vision as sources of selection on butterfly coloration, we studied yellow wing pigmentation in the tribe Heliconiini. We confirmed, using reflectance and mass spectrometry, that only Heliconius use 3-hydroxy-DL-kynurenine (3-OHK), which looks yellow to humans but reflects both UV- and long-wavelength light, whereas butterflies in related genera have chemically unknown yellow pigments mostly lacking UV reflectance. Modeling of these color signals reveals that the two UV photoreceptors of Heliconius are better suited to separating 3-OHK from non-3-OHK spectra compared with the photoreceptors of related genera or birds. The co-occurrence of potentially enhanced UV vision and a UV-reflecting yellow wing pigment could allow unpalatable Heliconius private intraspecific communication in the presence of mimics. Our results are the best available evidence for the correlated evolution of a color signal and color vision. They also suggest that predator visual systems are error prone in the context of mimicry.     

Morpho蝴蝶结构显色特性研究

M orpho蝴蝶结构显色是结构显色研究中最热门的分支之一,其显色原理主要在于物理光学作用。根据M orpho蝴蝶的表皮微结构,建立了计算模型;利用时域有限差分方法(fin ite d ifference tim e dom a in m ethodFDTD)对结构模型在自然光照射下的结构显色特性进行计算,根据计算结果分析了M orpho蝴蝶的颜色之谜,揭示了其结构显色的原理。计算分析结果与观察结果完全吻合,说明研究方法具有可行性。     

Butterfly nectaring flowers: butterfly morphology and flower form

The profitability of butterfly foraging depends in part on the corolla depth and clustering of flowers, and the tongue length, body mass and wing loading of butterflies. Interactions among these attributes of flowers and butterflies were investigated, using data from a field study in Cornwall and from Porter et al. (1992). The maximum corolla depth from which a butterfly can feed depends on tongue length, which correlates with the more easily measured attributes of body mass and wing loading. Small, short-tongued butterflies did not visit deep flowers. The quantity of nectar sugar per flower necessary for profitable foraging depends on foraging costs, which are expected to correlate with wing loading. Butterfly species with a high wing loading generally confined their visits to flowers that were clustered or very nectar-rich. Butterfly species with a low wing loading included solitary and less nectar-rich flowers in their diet. Body mass and wing loading affect a butterfly's load-carrying capacity (limiting the distance between fuelling stops) and cooling rate (limiting the distance between stops for basking or endothermic warming), and will therefore influence the capacity for floral selectivity and for migration and dispersal. Body mass, wing loading and tongue length characterised families or subfamilies of butterflies. For example vanessine nymphalids, with their long tongues and high wing loading, visited the deep, massed flowers of Buddleja davidii, but lycaenids, with their short tongues and low wing loading, did not. These often visited members of the Asteraceae. Eupatorium cannabinum, with massed flowers offering abundant and accessible nectar, was visited by butterflies of all tongue lengths and both high and low wing loading. These findings may help to inform habitat management for butterfly nectaring flowers.     

Butterfly genomics eclosing

Technological and conceptual advances of the last decade have led to an explosion of genomic data and the emergence of new research avenues. Evolutionary and ecological functional genomics, with its focus on the genes that affect ecological success and adaptation in natural populations, benefits immensely from a phylogenetically widespread sampling of biological patterns and processes. Among those organisms outside established model systems, butterflies offer exceptional opportunities for multidisciplinary research on the processes generating and maintaining variation in ecologically relevant traits. Here we highlight research on wing color pattern variation in two groups of Nymphalid butterflies, the African species Bicyclus anynana (subfamily Satyrinae) and species of the South American genus Heliconius (subfamily Heliconiinae), which are emerging as important systems for studying the nature and origins of functional diversity. Growing genomic resources including genomic and cDNA libraries, dense genetic maps, high-density gene arrays, and genetic transformation techniques are extending current gene mapping and expression profiling analysis and enabling the next generation of research questions linking genes, development, form, and fitness. Efforts to develop such resources in Bicyclus and Heliconius underscore the general challenges facing the larger research community and highlight the need for a community-wide effort to extend ongoing functional genomic research on butterflies.     

Müllerian mimetic radiation of Delias butterflies (Lepidoptera: Pieridae) in Bali and Timor

Mimicry rings are present among Delias butterflies, and those butterflies are also considered to be mimetic models of other lepidopteran insects; however, experimental evidence for their unpalatability to predators is limited. In Bali and Timor, a total of three mimicry rings of Delias species are present; particularly, male and female D. lemoulti join different rings in Timor. The present study examined the unpalatability of Delias in Bali and Timor to the caged avian predator Pycnonotus aurigaster. The birds ate eight Delias species in similar numbers, and ate the palatable butterfly Mycalesis horsfieldii much more frequently than Delias butterflies. The result suggests that the three mimicry rings of Delias species in Bali and Timor are Müllerian rather than Batesian. Based on previous findings on their phylogenetic relationships, the Müllerian mimicry rings of Delias in Bali and Timor are suggested to have emerged through the convergent evolution and phylogenetic constraints of wing color patterns. In the D. hyparete species group, mimetic radiation may have occurred between Bali and Timor.     

Body Colors Indicate the Reproductive Status of Female Common Chameleons: Experimental Evidence for the Intersex Communication Function

Female common chameleons, Chamaeleo chamaeleon , show temporary body color changes during the reproductive season, probably in synchrony with their reproductive status. In a field study, the color changes of 21 radio-tagged females were monitored for the apparent effects that three selected colorations (green body with yellow lines, green body with yellow spots and black body with yellow spots, abbreviated to GYL, GYS and BYS, respectively) had on the reproductive behavior of both sexes. In a field experiment, females naturally displaying GYL were artificially painted to resemble GYL (or control), GYS and BYS. They were released in the wild and the response of males was recorded. The frequency of male-female behaviors, the pairing time and the outcome of male copulation attempts were consistent with the respective neutral (GYL), receptive (GYS) and gravid (BYS) functions of female color phases since a high percentage of copulations occurred during the short-term GYS phase, whereas all copulation attempts by males were violently rejected during the BYS phase. In addition, BYS females also displayed specific behavioral postures to prevent matings. In the field experiment, the number of approaching males and the strength of the response by males were significantly higher for painted GYS females. The data show strong evidence that temporary body color changes in female common chameleons are associated with changes in their reproductive status and hence, function as signals used in inter-sex communication.     

长尾管蚜蝇Eristalis tenax体色变异的研究

通过对长尾管蚜蝇体色变异的研究,发现该种蚜蝇在体色变异方面有如下特点：（1）腹部色斑的变异形式多样,种群中以浅色者为主,深色的个体比例较少;腹部色斑变异表现出明显的性别差异,雄性变异形式比雌性丰富;（2）后足腿节颜色变异呈现出一定的连续性,从主要呈黑色（肉眼观察）到黄褐色;且这种变化与性别无关;（3）翅上暗色云斑的变化仅有2种形式,种群中具暗色云斑者占大多数;云斑的有无与性别无关;（4）体色变异与发生季节、海拔无关.     

金斑蝶觅食求偶过程中的视觉嗅觉利用

【目的】阐明金斑蝶Danaus chrysippus觅食求偶时视觉嗅觉信息利用机制。【方法】通过行为学观察,测试金斑蝶成虫对7种不同颜色的假花和假花喷施10%蜂蜜水后的觅食响应;通过自然种群求偶和塑封模型访问试验,验证金斑蝶对颜色和气味行为响应。【结果】在无气味的7种颜色的假花条件下,金斑蝶成虫访花总次数为138次,对长波长红色(620～750 nm)显示出明显的颜色趋性(占总访花次数的 52.17%),访问蓝色(占总访花次数的15.22%)和橙色(占总访花次数的11.59%)次之,其他4种颜色假花较少访问;在假花上喷洒10%蜂蜜水后,金斑蝶成虫访花总次数增加3.05倍,雌雄蝶访花次数分别增加3.31和2.86倍;去花冠无气味的花枝几乎没有蝴蝶访问,然而在去花冠无气味的假花花枝上喷洒10%蜂蜜水后,金斑蝶成虫访花总次数增加146次,对单一颜色的访问次数与对单一气味的访问次数相比无显著差异,金斑蝶成虫对气味加颜色的访问总次数较对单一气味的访问总次数增加2.88倍,雌雄蝶访花次数分别增加2.95和2.83倍;金斑蝶雄蝶对颜色和气味的敏感性高于雌蝶。在求偶过程中,金斑蝶对自然种群与蝶翅模型都有雄追雄、雄追雌、雌追雌和雌追雄4种模式,但金斑蝶对无气味蝶翅模型的追逐次数显著低于对自然种群的追逐次数。在自然光下,雌雄蝶翅颜色和图案相近,除了雄蝶后翅腹面多一白色性标斑点外,其他无显著区别;在紫外光下,蝶翅模型的颜色和图案比自然蝶翅更为明显,可能有助于异性识别。【结论】金斑蝶成虫在觅食和求偶过程中,视觉嗅觉同等重要。颜色较稳定、醒目、容易被发现;气味不稳定、易挥发、受环境干扰较大。在觅食中,金斑蝶利用视觉先进行初步定位,通过嗅觉和味觉确认食物资源;在求偶中,金斑蝶成虫通过视觉初步区分异性,然后依靠嗅觉进行精确识别。     

Differential Involvement of Hedgehog Signaling in Butterfly Wing and Eyespot Development

Butterfly eyespots may have evolved from the recruitment of pre-existent gene circuits or regulatory networks into novel locations on the wing. Gene expression data suggests one such circuit, the Hedgehog (Hh) signaling pathway and its target gene engrailed (en), was recruited from a role in patterning the anterior-posterior insect wing axis to a role patterning butterfly eyespots. However, while Junonia coenia expresses hh and en both in the posterior compartment of the wing and in eyespot centers, Bicyclus anynana lacks hh eyespot-specific expression. This suggests that Hh signaling may not be functioning in eyespot development in either species or that it functions in J. coenia but not in B. anynana. In order to test these hypotheses, we performed functional tests of Hh signaling in these species. We investigated the effects of Hh protein sequestration during the larval stage on en expression levels, and on wing size and eyespot size in adults. Hh sequestration led to significantly reduced en expression and to significantly smaller wings and eyespots in both species. But while eyespot size in B. anynana was reduced proportionately to wing size, in J. coenia, eyespots were reduced disproportionately, indicating an independent role of Hh signaling in eyespot development in J. coenia. We conclude that while Hh signaling retains a conserved role in promoting wing growth across nymphalid butterflies, it plays an additional role in eyespot development in some, but not all, lineages of nymphalid butterflies. We discuss our findings in the context of alternative evolutionary scenarios that led to the differential expression of hh and other Hh pathway signaling members across nymphalid species.     

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

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