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.
more »
« less
The jumping spider Saitis barbipes lacks a red photoreceptor to see its own sexually dimorphic red coloration
Abstract Examining the role of color in mate choice without testing what colors the study animal is capable of seeing can lead to ill-posed hypotheses and erroneous conclusions. Here, we test the seemingly reasonable assumption that the sexually dimorphic red coloration of the male jumping spiderSaitis barbipesis distinguishable, by females, from adjacent black color patches. Using microspectrophotometry, we find clear evidence for photoreceptor classes with maximal sensitivity in the UV (359 nm) and green (526 nm), inconclusive evidence for a photoreceptor maximally sensitive in the blue (451 nm), and no evidence for a red photoreceptor. No colored filters within the lens or retina could be found to shift green sensitivity to red. To quantify and visualize whether females may nevertheless be capable of discriminating red from black color patches, we take multispectral images of males and calculate photoreceptor excitations and color contrasts between color patches. Red patches would be, at best, barely discriminable from black, and not discriminable from a low-luminance green. Some color patches that appear achromatic to human eyes, such as beige and white, strongly absorb UV wavelengths and would appear as brighter “spider-greens” toS. barbipesthan the red color patches. Unexpectedly, we discover an iridescent UV patch that contrasts strongly with the UV-absorbing surfaces dominating the rest of the spider. We propose that red and black coloration may serve identical purposes in sexual signaling, functioning to generate strong achromatic contrast with the visual background. The potential functional significance of red coloration outside of sexual signaling is discussed.
more »
« less
- PAR ID:
- 10362530
- Publisher / Repository:
- Springer Science + Business Media
- Date Published:
- Journal Name:
- The Science of Nature
- Volume:
- 109
- Issue:
- 1
- ISSN:
- 0028-1042
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
For color vision, retinal circuits separate information about intensity and wavelength. In vertebrates that use the full complement of four “ancestral” cone types, the nature and implementation of this computation remain poorly understood. Here, we establish the complete circuit architecture of outer retinal circuits underlying color processing in larval zebrafish. We find that the synaptic outputs of red and green cones efficiently rotate the encoding of natural daylight in a principal components analysis–like manner to yield primary achromatic and spectrally opponent axes, respectively. Blue cones are tuned to capture most remaining variance when opposed to green cones, while UV cone present a UV achromatic axis for prey capture. We note that fruitflies use essentially the same strategy. Therefore, rotating color space into primary achromatic and chromatic axes at the eye’s first synapse may thus be a fundamental principle of color vision when using more than two spectrally well-separated photoreceptor types.more » « less
-
Abstract Color vision is thought to play a key role in the evolution of animal coloration, while achromatic vision is rarely considered as a mechanism for species recognition. Here we test the hypothesis that brightness vision rather than color vision helpsAdelpha fessoniabutterflies identify potential mates while their co-mimetic wing coloration is indiscriminable to avian predators. We examine the trichromatic visual system ofA. fessoniaand characterize its photoreceptors using RNA-seq, eyeshine, epi-microspectrophotometry, and optophysiology. We model the discriminability of its wing color patches in relation to those of its co-mimic,A. basiloides, throughA. fessoniaand avian eyes. Visual modeling suggests that neitherA. fessonianor avian predators can readily distinguish the co-mimics’ coloration using chromatic or achromatic vision under natural conditions. These results suggest that mimetic colors are well-matched to visual systems to maintain mimicry, and that mate avoidance between these two look-alike species relies on other cues.more » « less
-
Parins-Fukuchi, Tomomi; Connallon, Tim (Ed.)Abstract Sexual dichromatism is thought to evolve primarily as a function of sexual selection, especially female choice. However, other forces, from sex-specific environmental conditions to social signaling in females, can also generate color differences between sexes. We studied dewlap dichromatism across 292 species of Anolis lizards. Dewlaps are colorful throat ornaments found on males of most anole species but are also present in females in many species. Although male and female dewlaps often have similar coloration, in some species, they are strikingly dichromatic. We found that ornament color is labile and that dichromatism results from the loss of costly pigments in females. This pattern could indicate a shift towards signal loss in females; however, the secondary gains of female dewlaps across the phylogeny suggest a potential advantageous function. Possible mechanisms for female dewlap coloration include social selection, nonsexual signaling, or detectability in different microhabitats (e.g., sensory drive). Female dewlap color overlap between co-occurring species is both less than expected by chance overall and reduced in species-rich communities, suggesting that dichromatism could be driven by competition. Our results highlight that selection on females drives the observed pattern of dichromatism, suggesting a potentially adaptive role for female ornaments and emphasizing the need for additional work to understand female ornament evolution.more » « less
-
Abstract Melanin-based plumage coloration in birds is shaped by pigment composition as well as melanosome morphology and distribution, however, the ways in which these factors together modulate observable color remain poorly understood. We investigate this relationship in the Capuchino Seedeaters (genusSporophila), whose recent, rapid radiation driven by sexual selection resulted in 12 species with diverse coloration patterns. Using scanning electron microscopy (SEM) and micro-computed tomography (µCT), combined with a novel application of Fontana-Masson stain to image melanosomes at high resolution, we characterize melanosome distribution and morphology in several variably colored plumage patches across Capuchino species. Melanosome morphologies followed patch-specific patterns that did not directly correlate with coloration: crown feather melanosomes were larger, more elongated, and had greater percent eumelanin content than those in belly, throat, or dorsum/rump patches. We also observed that dorsal patches had more total melanin than ventral ones, with pigment and coloration patterns suggesting possible signaling and photoprotective roles. More generally, we show how the patch-specific coloration of male Capuchinos is accompanied by differences in melanosome morphology and melanin composition and abundance. Our work highlights the challenges that remain in understanding how the nanoscale mechanisms of melanin-based pigmentation translate into macroscale plumage coloration.more » « less
An official website of the United States government
