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This study uncovers a correlation between the mid-infrared emissivity of butterfly wings and the average air temperature of their habitats across the world. Butterflies from cooler climates have a lower mid-infrared emissivity, which limits heat losses to surroundings, and butterflies from warmer climates have a higher mid-infrared emissivity, which enhances radiative cooling. The mid-infrared emissivity showed no correlation with other investigated climatic factors. Phylogenetic independent contrasts analysis indicates the microstructures of butterfly wings may have evolved in part to regulate mid-infrared emissivity as an adaptation to climate, rather than as phylogenetic inertia. Our findings offer new insights into the role of microstructures in thermoregulation and suggest both evolutionary and physical constraints to butterflies’ abilities to adapt to climate change.

 

The visual pigments known as opsins are the primary molecular basis for colour vision in animals. Insects are among the most diverse of animal groups and their visual systems reflect a variety of life histories. The study of insect opsins in the fruit fly Drosophila melanogaster has led to major advances in the fields of neuroscience, development and evolution. In the last 25 years, research in D. melanogaster has improved our understanding of opsin genotype–phenotype relationships while comparative work in other insects has expanded our understanding of the evolution of insect eyes via gene duplication, coexpression and homologue switching. Even so, until recently, technology and sampling have limited our understanding of the fundamental mechanisms that evolution uses to shape the diversity of insect eyes. With the advent of genome editing and in vitro expression assays, the study of insect opsins is poised to reveal new frontiers in evolutionary biology, visual neuroscience, and animal behaviour. This article is part of the theme issue ‘Understanding colour vision: molecular, physiological, neuronal and behavioural studies in arthropods’. 

Abstract The evolution of color vision is often studied through the lens of receptor gain relative to an ancestor with fewer spectral classes of photoreceptor. For instance, in Heliconius butterflies, a genus-specific UVRh opsin duplication led to the evolution of UV color discrimination in Heliconius erato females, a rare trait among butterflies. However, color vision evolution is not well understood in the context of loss. In Heliconius melpomene and Heliconius ismenius lineages, the UV2 receptor subtype has been lost, which limits female color vision in shorter wavelengths. Here, we compare the visual systems of butterflies that have either retained or lost the UV2 photoreceptor using intracellular recordings, ATAC-seq, and antibody staining. We identify several ways these butterflies modulate their color vision. In H. melpomene, chromatin reorganization has downregulated an otherwise intact UVRh2 gene, whereas in H. ismenius, pseudogenization has led to the truncation of UVRh2. In species that lack the UV2 receptor, the peak sensitivity of the remaining UV1 photoreceptor cell is shifted to longer wavelengths. Across Heliconius, we identify the widespread use of filtering pigments and co-expression of two opsins in the same photoreceptor cells. Multiple mechanisms of spectral tuning, including the molecular evolution of blue opsins, have led to the divergence of receptor sensitivities between species. The diversity of photoreceptor and ommatidial subtypes between species suggests that Heliconius visual systems are under varying selection pressures for color discrimination. Modulating the wavelengths of peak sensitivities of both the blue- and remaining UV-sensitive photoreceptor cells suggests that Heliconius species may have compensated for UV receptor loss. 

ABSTRACT In true color vision, animals discriminate between light wavelengths, regardless of intensity, using at least two photoreceptors with different spectral sensitivity peaks. Heliconius butterflies have duplicate UV opsin genes, which encode ultraviolet and violet photoreceptors, respectively. In Heliconius erato, only females express the ultraviolet photoreceptor, suggesting females (but not males) can discriminate between UV wavelengths. We tested the ability of H. erato, and two species lacking the violet receptor, Heliconius melpomene and Eueides isabella, to discriminate between 380 and 390 nm, and between 400 and 436 nm, after being trained to associate each stimulus with a sugar reward. We found that only H. erato females have color vision in the UV range. Across species, both sexes show color vision in the blue range. Models of H. erato color vision suggest that females have an advantage over males in discriminating the inner UV-yellow corollas of Psiguria flowers from their outer orange petals. Moreover, previous models ( McCulloch et al., 2017) suggested that H. erato males have an advantage over females in discriminating Heliconius 3-hydroxykynurenine (3-OHK) yellow wing coloration from non-3-OHK yellow wing coloration found in other heliconiines. These results provide some of the first behavioral evidence for female H. erato UV color discrimination in the context of foraging, lending support to the hypothesis ( Briscoe et al., 2010) that the duplicated UV opsin genes function together in UV color vision. Taken together, the sexually dimorphic visual system of H. erato appears to have been shaped by both sexual selection and sex-specific natural selection. 

Abstract Learning plays an important role in the location and utilization of nectar sources for pollinators. In this work we focus on the plant-pollinator interaction between the butterfly Agraulis vanillae (Nymphalidae) and two Glandularia plant species (Verbenaceae) that grow in sympatry. Bioassays using arrays of artificial flowers (red vs. lilac-purple) showed that naïve A. vanillae butterflies do not have innate colour preferences for any of the tested colours. Trained butterflies were able to learn to associate both floral colours with the presence of nectar rewards. Wild A. vanillae butterflies visited the red flowers of Glandularia peruviana much more frequently than the lilac-purple flowers of Glandularia venturii. Standing nectar crop measurements showed that G. peruviana flowers offered three times more sucrose than the flowers of G. venturii. Analyses confirmed that corolla colour of G. peruviana (red flowers) and G. venturii (lilac-purple flowers) were discriminable in the butterfly’s colour space. These findings may indicate flexibility in A. vanillae preferences due to a learned association between red coloration and higher nectar rewards. 

Purpose: To present a detailed, reliable long range-PCR and sequencing (LR-PCR-Seq) procedure to identify human opsin gene sequences for variations in the long wavelength-sensitive (OPN1LW), medium wavelength-sensitive (OPN1MW), short wavelength-sensitive (OPN1SW), and rhodopsin (RHO) genes. Methods: Color vision was assessed for nine subjects using the Farnsworth-Munsell 100 hue test, Ishihara pseudoisochromatic plates, and the Rabin cone-contrast threshold procedure (ColorDX, Konan Medical). The color vision phenotypes were normal trichromacy (n = 3), potential tetrachromacy (n = 3), dichromacy (n = 2), and unexplained low color vision (n = 1). DNA was isolated from blood or saliva and LR-PCR amplified into individual products: OPN1LW (4,045 bp), OPN1MW (4,045 bp), OPN1SW (3,326 bp), and RHO (6,715 bp). Each product was sequenced using specific internal primer sets. Analysis was performed with Mutation Surveyor software. Results: The LR-PCR-Seq technique identified known single nucleotide polymorphisms (SNPs) in OPN1LW and OPN1MW gene codons (180, 230, 233, 277, and 285), as well as those for lesser studied codons (174, 178, 236, 274, 279, 298 and 309) in the OPN1LW and OPN1MW genes. Additionally, six SNP variants in the OPN1MW and OPN1LW genes not previously reported in the NCBI dbSNP database were identified. An unreported poly-T region within intron 5(c.36+126) of the rhodopsin gene was also found, and analysis showed it to be highly conserved in mammalian species. Conclusions: This LR-PCR-Seq procedure (single PCR reaction per gene followed by sequencing) can identify exonic and intronic SNP variants in OPN1LW, OPN1MW, OPN1SW, and rhodopsin genes. There is no need for restriction enzyme digestion or multiple PCR steps that can introduce errors. Future studies will combine the LR-PCR-Seq with perceptual behavior measures, allowing for accurate correlations between opsin genotypes, retinal photopigment phenotypes, and color perception behaviors. 

Abstract Understanding the origin and maintenance of adaptive phenotypic novelty is a central goal of evolutionary biology. However, both hybridization and incomplete lineage sorting can lead to genealogical discordance between the regions of the genome underlying adaptive traits and the remainder of the genome, decoupling inferences about character evolution from population history. Here, to disentangle these effects, we investigated the evolutionary origins and maintenance of Batesian mimicry between North American admiral butterflies (Limenitis arthemis) and their chemically defended model (Battus philenor) using a combination of de novo genome sequencing, whole-genome resequencing, and statistical introgression mapping. Our results suggest that balancing selection, arising from geographic variation in the presence or absence of the unpalatable model, has maintained two deeply divergent color patterning haplotypes that have been repeatedly sieved among distinct mimetic and nonmimetic lineages of Limenitis via introgressive hybridization. 

While surface microstructures of butterfly wings have been extensively studied for their structural coloration or optical properties within the visible spectrum, their properties in infrared wavelengths with potential ties to thermoregulation are relatively unknown. The midinfrared wavelengths of 7.5 to 14 µm are particularly important for radiative heat transfer in the ambient environment, because of the overlap with the atmospheric transmission window. For instance, a high midinfrared emissivity can facilitate surface cooling, whereas a low midinfrared emissivity can minimize heat loss to surroundings. Here we find that the midinfrared emissivity of butterfly wings from warmer climates such asArchaeoprepona demophoon(Oaxaca, Mexico) andHeliconius sara(Pichincha, Ecuador) is up to 2 times higher than that of butterfly wings from cooler climates such asCelastrina echo(Colorado) andLimenitis arthemis(Florida), using Fourier-transform infrared (FTIR) spectroscopy and infrared thermography. Our optical computations using a unit cell approach reproduce the spectroscopy data and explain how periodic microstructures play a critical role in the midinfrared. The emissivity spectrum governs the temperature of butterfly wings, and we demonstrate thatC. echowings heat up to 8 °C more thanA. demophoonwings under the same sunlight in the clear sky of Irvine, CA. Furthermore, our thermal computations show that butterfly wings in their respective habitats can maintain a moderate temperature range through a balance of solar absorption and infrared emission. These findings suggest that the surface microstructures of butterfly wings potentially contribute to thermoregulation and provide an insight into butterflies' survival.