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Mechanisms of structural colour in the Morpho butterfly: cooperation of regularity and irregularity in an iridescent scale.

Structural colour in the Morpho butterfly originates from submicron structure within a scale and, for over a century, its colour and reflectivity have been explained as interference of light due to the multilayer of cuticle and air. However, this model fails to explain the extraordinarily uniform colour of the wing with respect to the observation direction. We have performed microscopic, optical and theoretical investigations, and have found that the separate lamellar structure with irregular heights is extremely important. Using a simple model, we have shown that the combined action of interference and diffraction is essential for the structural colour of the Morpho butterfly.

Animals↗

Responses of butterflies to twentieth century climate warming: implications for future ranges.

We analyse distribution records for 51 British butterfly species to investigate altitudinal and latitudinal responses to twentieth century climate warming. Species with northern and/or montane distributions have disappeared from low elevation sites and colonized sites at higher elevations during the twentieth century, consistent with a climate explanation. We found no evidence for a systematic shift northwards across all species, even though 11 out of 46 southerly distributed species have expanded in the northern part of their distributions. For a subset of 35 species, we model the role of climate in limiting current European distributions and predict potential future distributions for the period 2070-2099. Most northerly distributed species will have little opportunity to expand northwards and will disappear from areas in the south, resulting in reduced range sizes. Southerly distributed species will have the potential to shift northwards, resulting in similar or increased range sizes. However, 30 out of 35 study species have failed to track recent climate changes because of lack of suitable habitat, so we revised our estimates accordingly for these species and predicted 65% and 24% declines in range sizes for northern and southern species, respectively. These revised estimates are likely to be more realistic predictions of future butterfly range sizes.

Adaptation, Physiological↗

Sexual selection and speciation in mammals, butterflies and spiders.

Recently refined evolutionary theories propose that sexual selection and reproductive conflict could be drivers of speciation. Male and female reproductive optima invariably differ because the potential reproductive rate of males almost always exceeds that of females: females are selected to maximize mate 'quality', while males can increase fitness through mate 'quantity'. A dynamic, sexually selected conflict therefore exists in which 'competitive' males are selected to override the preference tactics evolved by 'choosy' females. The wide variation across taxa in mating systems therefore generates variance in the outcome of intrasexual conflict and the strength of sexual selection: monandry constrains reproductive heterozygosity and allows female choice to select and maintain particular (preferred) genes; polyandry promotes reproductive heterozygosity and will more likely override female choice. Two different theories predict how sexual selection might influence speciation. Traditional ideas indicate that increased sexual selection (and hence conflict) generates a greater diversity of male reproductive strategies to be counteracted by female mate preferences, thus providing elevated potentials for speciation as more evolutionary avenues of male-female interaction are created. A less intuitively obvious theory proposes that increased sexual selection and conflict constrains speciation by reducing the opportunities for female mate choice under polyandry. We use a comparative approach to test these theories by investigating whether two general measures of sexual selection and the potential for sexual conflict have influenced speciation. Sexual size dimorphism (across 480 mammalian genera, 105 butterfly genera and 148 spider genera) and degree of polyandry (measured as relative testes size in mammals (72 genera) and mating frequency in female butterflies (54 genera)) showed no associations with the variance in speciosity. Our results therefore show that speciation occurs independently of sexual selection.

Animals↗

Mating system and the evolution of sex-specific mortality rates in two nymphalid butterflies.

Life-history theory predicts that organisms should invest resources into intrinsic components of lifespan only to the degree that it pays off in terms of reproductive success. The benefit of a long life may differ between the sexes and different mating systems may therefore select for different sex-specific mortality rates. In insects with polyandrous mating systems, females mate throughout their lives and male reproductive success is likely to increase monotonously with lifespan. In monandrous systems, where the mating season is less protracted because receptive females are available only at the beginning of the flight season, male mating success should be less dependent on a long lifespan. Here, we show, in a laboratory experiment without predation, that the duration of the mating season is longer in the polyandrous comma butterfly, Polygonia c-album, than in the monandrous peacock butterfly, Inachis io, and that, in line with predictions, male lifespan is shorter than female lifespan in I. io, whereas male and female lifespans are similar in P. c-album.

Aging↗

Cooler butterflies lay larger eggs: developmental plasticity versus acclimation.

We use a full factorial design to investigate the effects of maternal and paternal developmental temperature, as well as female oviposition temperature, on egg size in the butterfly Bicyclus anynana. Butterflies were raised at two different temperatures and mated in four possible sex-by-parental-temperature crosses. The mated females were randomly divided between high and low oviposition temperatures. On the first day after assigning the females to different temperatures, only female developmental temperature affected egg size. Females reared at the lower temperature laid larger eggs than those reared at a higher temperature. When eggs were measured again after an acclimation period of 10 days, egg size was principally determined by the prevailing temperature during oviposition, with females ovipositing at a lower temperature laying larger eggs. In contrast to widely used assumptions, the effects of developmental temperature were largely reversible. Male developmental temperature did not affect egg size in either of the measurements. Overall, developmental plasticity and acclimation in the adult stage resulted in very similar patterns of egg size plasticity. Consequently, we argue that the most important question when testing the significance of acclamatory changes is not at which stage a given plasticity is induced, but rather whether plastic responses to environmental change are adaptive or merely physiological constraints.

Acclimatization↗

Sexual dichroism and pigment localization in the wing scales of Pieris rapae butterflies.

The beads in the wing scales of pierid butterflies play a crucially important role in wing coloration as shown by spectrophotometry and scanning electron microscopy (SEM). The beads contain pterin pigments, which in Pieris rapae absorb predominantly in the ultraviolet (UV). SEM demonstrates that in the European subspecies Pieris rapae rapae, both males and females have dorsal wing scales with a high concentration of beads. In the Japanese subspecies Pieris rapae crucivora, however, only the males have dorsal wing scales studded with beads, and the dorsal scales of females lack beads. Microspectrophotometry of single scales without beads yields reflectance spectra that increase slightly and monotonically with wavelength. With beads, the reflectance is strongly reduced in the UV and enhanced at the longer wavelengths. By stacking several layers of beaded scales, pierid butterflies achieve strong colour contrasts, which are not realized in the dorsal wings of female P. r. crucivora. Consequently, P. r. crucivora exhibits a strong sexual dichroism that is absent in P. r. rapae.

Animals↗

Pterin pigment granules are responsible for both broadband light scattering and wavelength selective absorption in the wing scales of pierid butterflies.

A small but growing literature indicates that many animal colours are produced by combinations of structural and pigmentary mechanisms. We investigated one such complex colour phenotype: the highly chromatic wing colours of pierid butterflies including oranges, yellows and patterns which appear white to the human eye, but strongly absorb the ultraviolet (UV) wavelengths visible to butterflies. Pierids produce these bright colours using wing scales that contain collections of minute granules. However, to date, no work has directly characterized the molecular composition or optical properties of these granules. We present results that indicate these granules contain pterin pigments. We also find that pterin granules increase light reflection from single wing scales, such that wing scales containing denser granule arrays reflect more light than those with less dense granule collections. As male wing scales contain more pterin granules than those of females, the sexual dichromatism found in many pierid species can be explained by differences in wing scale pterin deposition. Additionally, the colour pattern elements produced by these pterins are known to be important during mating interactions in a number of pierid species. Therefore, we discuss the potential relevance of our results within the framework of sexual selection and colour signal evolution.

Absorption↗

The genetics of the mimetic butterfly Hypolimnas bolina (L.).

Hypolimnas bolina is a Nymphalid butterfly having a west to east distribution from Madagascar to Easter Island, and a north to south one from Japan to Australasia. It is highly migratory in some areas. In much of the western part of its range the female is both monomorphic and a mimic of Euploea. Further east it is frequently polymorphic with the majority of the forms being non-mimetic. The polymorphism is sex-limited to the female and controlled by two unlinked loci, one with two allelomorphs, E and e, determining the extent of the dark pigmentation, the other with three allelomorphs, P, Pn and p, determining the presence and distribution of orange-brown. Only butterflies of the genotypes EEpp and to a lesser extent Eepp are satisfactory Batesian mimics of their Euploea models. The details of the mimetic pattern are under multifactorial control, following those of their local model, as is much of the variation within the non-mimetic forms, particularly with regard to the distribution of white and blue scaling.

Adaptation, Biological↗

The evolution of wing color: male mate choice opposes adaptive wing color divergence in Colias butterflies.

Correlated evolution of mate signals and mate preference may be constrained if selection pressures acting on mate preference differ from those acting on mate signals. In particular, opposing selection pressures may act on mate preference and signals when traits have sexual as well as nonsexual functions. In the butterfly Colias philodice eriphyle, divergent selection on wing color across an elevational gradient in response to the thermal environment has led to increasing wing melanization at higher elevations. Wing color is also a long-range signal used by males in mate searching. We conducted experiments to test whether sexual selection on wing melanization via male mate choice acts in the same direction as natural selection on mate signals due to the thermal environment. We performed controlled mate choice experiments in the field over an elevational range of 1500 meters using decoy butterflies with different melanization levels. Also, we obtained a more direct estimate of the relation between wing color and sexual selection by measuring mating success in wild-caught females. Both our experiments showed that wing melanization is an important determinant of female mating success in C. p. eriphyle. However, a lack of elevational variation in male mate preference prevents coevolution of mate signals and mate preference, as males at all elevations prefer less-melanized females. We suggest that this apparently maladaptive mate choice may be maintained by differences in detectability between the morphs or by preservation of species recognition.

Animals↗

Independent gene phylogenies and morphology demonstrate a malagasy origin for a wide-ranging group of swallowtail butterflies.

Madagascar is home to numerous endemic species and lineages, but the processes that have contributed to its endangered diversity are still poorly understood. Evidence is accumulating to demonstrate the importance of Tertiary dispersal across varying distances of oceanic barriers, supplementing vicariance relationships dating back to the Cretaceous, but these hypotheses remain tentative in the absence of well-supported phylogenies. In the Papilio demoleus group of swallowtail butterflies, three of the five recognized species are restricted to Madagascar, whereas the remaining two species range across the Afrotropical zone and southern Asia plus Australia. We reconstructed phylogenetic relationships for all species in the P. demoleus group, as well as 11 outgroup Papilio species, using 60 morphological characters and about 4 kb of nucleotide sequences from two mitochondrial (cytochrome oxidase I and II) and two nuclear (wg and EF-1alpha) genes. Of the three endemic Malagasy species, the two that are formally listed as endangered or at risk represented the most basal divergences in the group, while the more common third endemic was clearly related to African P. demodocus. The fifth species, P. demoleus, showed little differentiation across southern Asia, but showed divergence from its subspecies sthenelus in Australia. Dispersal-vicariance analysis using cladograms derived from morphology and three independent genes indicated a Malagasy diversification of lime swallowtails in the middle Miocene. Thus, diversification processes on the island of Madagascar may have contributed to the origin of common butterflies that now occur throughout much of the Old World tropical and subtemperate regions. An alternative hypothesis, that Madagascar is a refuge for ancient lineages resulting from successive colonizations from Africa, is less parsimonious and does not explain the relatively low continental diversity of the group.

Animals↗

Specialized avian predators repeatedly attack novel color morphs of Heliconius butterflies.

The persistence of Müllerian mimicry and geographically distinct wing patterns, as observed in many Heliconius species (Lepidoptera: Nymphalidae), is difficult to explain from a predator's perspective: predator selection against locally rare patterns must persist despite avoidance learning. Maintaining spatial color-pattern polymorphism requires local pattern avoidance, fine-scale discrimination among similar wing patterns, and repeated attacks on novel color patterns. I tested for these behaviors by presenting 80 adult rufous-tailed jacamars (Galbula ruficauda) with three morphs of Heliconius butterflies, and then presenting the same suite of butterflies to 46 of these jacamars between four and 429 days later. These trials offer the first direct evidence of the selective predator behavior required to maintain aposematic polymorphism: jacamars avoid local aposematic morphs while repeatedly attacking similar but novel morphs over time.

Adaptation, Physiological↗

Delayed population explosion of an introduced butterfly.

1. The causes of lagged population and geographical range expansions after species introductions are poorly understood, and there are relatively few detailed case studies. 2. We document the 29-year history of population dynamics and structure for a population of Euphydryas gillettii Barnes that was introduced to the Colorado Rocky Mountains, USA in 1977. 3. The population size remained low (< 200 individuals) and confined to a single habitat patch (approximately 2.25 ha) to 1998. These values are similar to those of many other populations within the natural geographical range of the species. 4. However, by 2002 the population increased dramatically to > 3000 individuals and covered approximately 70 ha, nearly all to the south of the original site. The direction of population expansion was the same as that of predominant winds. 5. By 2004, the butterfly's local distribution had retracted mainly to three habitat patches. It thus exhibited a 'surge/contraction' form of population growth. Searches within 15 km of the original site yielded no other new populations. 6. In 2005, butterfly numbers crashed, but all three habitat patches remained occupied. The populations within each patch did not decrease in the same proportions, suggesting independent dynamics that are characteristic of metapopulations. 7. We postulate that this behaviour results, in this species, in establishment of satellite populations and, given appropriate habitat structure, may result in lagged or punctuated expansions of introduced populations.

Animals↗

Wing scale microstructures and nanostructures in butterflies--natural photonic crystals.

The aim of our study was to investigate the correlation between structural colour and scale morphology in butterflies. Detailed correlations between blue colour and structure were investigated in three lycaenid subfamilies, which represent a monophylum in the butterfly family Lycaenidae (Lepidoptera): the Coppers (Lycaeninae), the Hairstreaks (Theclinae) and the Blues (Polyommatinae). Complex investigations such as spectral measurements and characterization by means of light microscopy, scanning electron microscopy and transmission electron microscopy enabled us to demonstrate that: (i) a wide array of nanostructures generate blue colours; (ii) monophyletic groups use qualitatively similar structures; and (iii) the hue of the blue colour is characteristic for the microstructure and nanostructure of the body of the scales.

Animals↗

The history and geography of diversification within the butterfly genus Lycaeides in North America.

The Lycaeides butterfly species complex in North America consists of two nominal, morphologically defined species. These butterflies are ecologically diverse and appear to be distributed as a geographically complex mosaic of locally differentiated populations that may be undergoing adaptive radiation. We asked whether patterns of molecular genetic variation within the species complex are congruent with currently recognized morphological species and whether the distribution of molecular variation is consistent with the hypothesis that Pleistocene climate changes contributed to the process of differentiation within the genus. Variation in the form of the genitalia from 726 males from 59 populations clearly distinguishes both species with only six populations containing morphologically intermediate or ambiguous individuals. However, partitioning of molecular variance in a 236 bp section of the mitochondrial AT-rich region from 628 individuals (57 populations) surveyed using single strand conformation polymorphism analysis (SSCP) indicates that only 26% of the total genetic variation is distributed along nominal species boundaries as defined by morphology. Instead, three phylogeographical groups were detected, represented by three major haplotype clades, which account for 90% of the total genetic variance. Pleistocene glaciations appear to have fostered divergence during glacial maxima, while post-glacial range expansions created opportunities for gene exchange and reticulation along suture zones between geographical groups. Data presented here allow us to make inferences about the history of the species complex. However, evidence of ancestral polymorphism and reticulation limit our ability to define species boundaries based on mitochondrial DNA sequence variation.

Analysis of Variance↗

Prevalence and penetrance variation of male-killing Wolbachia across Indo-Pacific populations of the butterfly Hypolimnas bolina.

Male-killing bacteria are generally thought to attain low to intermediate prevalence in natural populations, with only mild effects on the host population sex ratio. This view was recently challenged by reports of extremely high infection frequencies in three butterfly species, raising the prospect that male killers, by making males rare, might drive many features of host ecology and evolution. To assess this hypothesis, it is necessary to evaluate how often male killers actually produce a highly female-biased population sex ratio in nature, which requires both high prevalence of infection and high penetrance of action. To this end, we surveyed South Pacific and Southeast Asian populations of Hypolimnas bolina, a butterfly in which extreme prevalence of male-killing Wolbachia bacteria has recently been recorded. Our results indicate that highly female-biased populations are common in Polynesia, with 6 out of 12 populations studied having in excess of 70% of females infected with a fully efficient male killer. However, heterogeneity is extreme in Polynesia, with the male-killing Wolbachia absent from three populations. In contrast to the Polynesian situation, Wolbachia does not kill males in any of the three Southeast Asian populations studied, despite its very high prevalence there. We conclude that male killers are likely to have significant ongoing ecological and evolutionary impact in 6 of the 15 populations surveyed. The causes and consequences of the observed spatial variation are discussed with respect to host resistance evolution, host ecology and interference with additional symbionts.

Animals↗

Identifying units for conservation using molecular systematics: the cautionary tale of the Karner blue butterfly.

The federally endangered North American Karner blue butterfly (Lycaeides melissa samuelis) and the closely related Melissa blue butterfly (L. m. melissa) can be distinguished based on life history and morphology. Western populations of L. m. samuelis share mitochondrial haplotypes with L. m. melissa populations, while eastern populations of L. m. samuelis have divergent haplotypes. Here we test two hypotheses concerning the presence of L. m. melissa mitochondrial haplotypes in western L. m. samuelis populations: (i) mitochondrial introgression has occurred from L. m. melissa populations into western L. m. samuelis populations, or (ii) western populations of the nominal L. m. samuelis are more closely related to L. m. melissa than to eastern L. m. samuelis populations, yet are phenotypically similar to the latter. A Bayesian algorithm was used to cluster 190 L. melissa individuals based on 143 informative amplified fragment length polymorphism (AFLP) loci. This method clearly differentiated L. m. samuelis and L. m. melissa. Thus, genomic divergence was greater between western L. m. samuelis populations and L. m. melissa populations than it was between western and eastern populations of L. m. samuelis. This supports the hypothesis that the presence of L. m. melissa mitochondrial haplotypes in western L. m. samuelis populations is the result of mitochondrial introgression. These data provide valuable information for conservation and management plans for the endangered L. m. samuelis, and illustrate the risks of using data from a single locus for diagnosing significant units of biodiversity for conservation.

Algorithms↗

Evolutionary genetics of dorsal wing colour in Colias butterflies.

The evolution of butterfly wing colouration is strongly affected by its multiple functions and by the correlated evolution of wing colour elements. Both factors may prevent local adaptation to ecological conditions. We investigated one aspect of wing colouration, the degree of dorsal wing melanization, in the butterfly Colias philodice eriphyle across an elevational gradient and its correlation with another aspect of wing colouration, ventral wing melanization. Dorsal wing melanization increased with elevation and these differences persisted in a common environment. Full-sibling analysis revealed high heritability for males but only intermediate heritability for females. The correlation between ventral and dorsal melanization showed significant elevational and sex-specific differences. In males the two traits were highly correlated, whereas in females the strength of the correlation decreased with increasing elevation. We conclude that uncoupling of ventral and dorsal melanization has evolved in females but not in males and discuss possible mechanisms underlying uncoupling.

Altitude↗

Dynamics of host plant use and species diversity in Polygonia butterflies (Nymphalidae).

The ability of insects to utilize different host plants has been suggested to be a dynamic and transient phase. During or after this phase, species can shift to novel host plants or respecialize on ancestral ones. Expanding the range of host plants might also be a factor leading to higher levels of net speciation rates. In this paper, we have studied the possible importance of host plant range for diversification in the genus Polygonia (Nymphalidae, Nymphalini). We have compared species richness between sistergroups in order to find out if there are any differences in number of species between clades including species that utilize only the ancestral host plants ('urticalean rosids') and their sisterclades with a broader (or in some cases potentially broader) host plant repertoire. Four comparisons could be made, and although these are not all phylogenetically or statistically independent, all showed clades including butterfly species using other or additional host plants than the urticalean rosids to be more species-rich than their sisterclade restricted to the ancestral host plants. These results are consistent with the theory that expansions in host plant range are involved in the process of diversification in butterflies and other phytophagous insects, in line with the general theory that plasticity may drive speciation.

Animals↗