Abstract:The eyes of the female small white butterfly, Pieris rapae crucivora, are furnished with three classes of short-wavelength photoreceptors, with sensitivity peaks in the ultraviolet (UV) ( max ϭ 360 nm), violet (V) ( max ϭ 425 nm), and blue (B) ( max ϭ 453 nm) wavelength range. Analyzing the spectral origin of the photoreceptors, we isolated three novel mRNAs encoding opsins corresponding to shortwavelength-absorbing visual pigments. We localized the opsin mRNAs in the retinal tissue and found that each of the … Show more
“…To our knowledge, no other insects besides pierid and lycaenid butterflies have two blue opsin genes. Our finding of independent duplication events is quite consistent with the very different max values (425·nm and 453·nm) of the pierid blue visual pigments (Arikawa et al, 2005) compared to the lycaenid ( max =437·nm and 500·nm, respectively). Our results also indicate (bootstrap support=100%) that the L. rubidus blue opsin gene duplication event occurred before the radiation of the coppers, hairstreaks and blues.…”
Section: Origins Of a Gene And A Family Of Blue Butterfliessupporting
confidence: 89%
“…In the case of the small white cabbage butterfly, Pieris rapae (Pieridae) (Arikawa et al, 2005), three short wavelength receptors were found, sensitive to ultraviolet ( max =360·nm), violet ( max =425·nm) and blue ( max =453·nm) light, and each expressing a unique opsin. A spectral filtering pigment was found co-expressed with the blue opsin only in males, producing a uniquely narrow blue receptor, highlighting the changes in the spatial expression patterns of non-opsin filtering pigments as a mechanism for producing a sexually dimorphic retina.…”
Section: Discussionmentioning
confidence: 99%
“…The situation in L. rubidus differs markedly from that of the nymphalid butterflies Vanessa cardui or the monarch Danaus plexippus, in which only three opsin mRNAs are expressed (UV, B, and LW) in the photoreceptor cells of the adult eye (Briscoe et al, 2003;Sauman et al, 2005), or that of the swallowtail butterfly, in which three duplicate LW opsin genes are expressed (Briscoe, 1998;Kitamoto et al, 1998). The L. rubidus opsin expression pattern does, however, resemble the situation in Pieris rapae, in which duplicate B opsin genes are also expressed in the eye (Arikawa et al, 2005) (but see below).…”
Section: Opsin Sequences and Phylogenymentioning
confidence: 95%
“…Within the true butterflies (Papilionoidea) the current understanding of familial relationships is (Papilionidae+(Pieridae+(Nymphalidae+(Riodinidae+Lycaeni dae)))) (Wahlberg et al, 2005), where papilionid and pierid butterflies represent the most basal lineages, and riodinid and lycaenid the most derived. Because the two pairs of B opsin genes identified from pierid (Pieris rapae) (Arikawa et al, 2005) and lycaenid butterflies (this study) are from distantly related families, we were interested in testing the hypothesis that the blue opsin genes of pierids and lycaenids evolved independently. We therefore screened eye-specific cDNA libraries from an additional ten butterfly taxa from four families (supplementary material Table·S3).…”
Section: Origins Of a Gene And A Family Of Blue Butterfliesmentioning
confidence: 99%
“…In the sphingid moth, the painted lady and monarch butterfly, these visual pigments are encoded by paralogous UV, B and LW opsin genes, which were present in the ancestor of all lepidopterans (Briscoe et al, 2003;White et al, 2003;Sauman et al, 2005). Deviations from this basic plan have been described in the most primitive of butterfly families, the papilionids, in which two rounds of duplication of the LW eye opsin gene have occurred (Briscoe, 1998;Kitamoto et al, 1998;Briscoe, 2001); and in the pierids, in which a duplicate blue opsin gene has been reported (Arikawa et al, 2005). In all butterfly species studied, opsin mRNA expression in the eye is similar between the sexes: the R1 and R2 photoreceptor cells express either UV or B opsin mRNAs and the R3-9 photoreceptors express LW opsin mRNAs.…”
SUMMARY
Although previous investigations have shown that wing coloration is an important component of social signaling in butterflies, the contribution of opsin evolution to sexual wing color dichromatism and interspecific divergence remains largely unexplored. Here we report that the butterfly Lycaena rubidus has evolved sexually dimorphic eyes due to changes in the regulation of opsin expression patterns to match the contrasting life histories of males and females. The L. rubidus eye contains four visual pigments with peak sensitivities in the ultraviolet (UV;λ max=360 nm), blue (B; λmax=437 nm and 500 nm, respectively) and long (LW; λmax=568 nm) wavelength range. By combining in situ hybridization of cloned opsinencoding cDNAs with epi-microspectrophotometry, we found that all four opsin mRNAs and visual pigments are expressed in the eyes in a sex-specific manner. The male dorsal eye, which contains only UV and B (λmax=437 nm)visual pigments, indeed expresses two short wavelength opsin mRNAs, UVRh and BRh1. The female dorsal eye, which also has the UV and B (λmax=437 nm) visual pigments, also contains the LW visual pigment, and likewise expresses UVRh, BRh1 and LWRh mRNAs. Unexpectedly, in the female dorsal eye, we also found BRh1 co-expressed with LWRh in the R3-8 photoreceptor cells. The ventral eye of both sexes, on the other hand, contains all four visual pigments and expresses all four opsin mRNAs in a non-overlapping fashion. Surprisingly, we found that the 500 nm visual pigment is encoded by a duplicate blue opsin gene, BRh2. Further, using molecular phylogenetic methods we trace this novel blue opsin gene to a duplication event at the base of the Polyommatine+Thecline+Lycaenine radiation. The blue opsin gene duplication may help explain the blueness of blue lycaenid butterflies.
“…To our knowledge, no other insects besides pierid and lycaenid butterflies have two blue opsin genes. Our finding of independent duplication events is quite consistent with the very different max values (425·nm and 453·nm) of the pierid blue visual pigments (Arikawa et al, 2005) compared to the lycaenid ( max =437·nm and 500·nm, respectively). Our results also indicate (bootstrap support=100%) that the L. rubidus blue opsin gene duplication event occurred before the radiation of the coppers, hairstreaks and blues.…”
Section: Origins Of a Gene And A Family Of Blue Butterfliessupporting
confidence: 89%
“…In the case of the small white cabbage butterfly, Pieris rapae (Pieridae) (Arikawa et al, 2005), three short wavelength receptors were found, sensitive to ultraviolet ( max =360·nm), violet ( max =425·nm) and blue ( max =453·nm) light, and each expressing a unique opsin. A spectral filtering pigment was found co-expressed with the blue opsin only in males, producing a uniquely narrow blue receptor, highlighting the changes in the spatial expression patterns of non-opsin filtering pigments as a mechanism for producing a sexually dimorphic retina.…”
Section: Discussionmentioning
confidence: 99%
“…The situation in L. rubidus differs markedly from that of the nymphalid butterflies Vanessa cardui or the monarch Danaus plexippus, in which only three opsin mRNAs are expressed (UV, B, and LW) in the photoreceptor cells of the adult eye (Briscoe et al, 2003;Sauman et al, 2005), or that of the swallowtail butterfly, in which three duplicate LW opsin genes are expressed (Briscoe, 1998;Kitamoto et al, 1998). The L. rubidus opsin expression pattern does, however, resemble the situation in Pieris rapae, in which duplicate B opsin genes are also expressed in the eye (Arikawa et al, 2005) (but see below).…”
Section: Opsin Sequences and Phylogenymentioning
confidence: 95%
“…Within the true butterflies (Papilionoidea) the current understanding of familial relationships is (Papilionidae+(Pieridae+(Nymphalidae+(Riodinidae+Lycaeni dae)))) (Wahlberg et al, 2005), where papilionid and pierid butterflies represent the most basal lineages, and riodinid and lycaenid the most derived. Because the two pairs of B opsin genes identified from pierid (Pieris rapae) (Arikawa et al, 2005) and lycaenid butterflies (this study) are from distantly related families, we were interested in testing the hypothesis that the blue opsin genes of pierids and lycaenids evolved independently. We therefore screened eye-specific cDNA libraries from an additional ten butterfly taxa from four families (supplementary material Table·S3).…”
Section: Origins Of a Gene And A Family Of Blue Butterfliesmentioning
confidence: 99%
“…In the sphingid moth, the painted lady and monarch butterfly, these visual pigments are encoded by paralogous UV, B and LW opsin genes, which were present in the ancestor of all lepidopterans (Briscoe et al, 2003;White et al, 2003;Sauman et al, 2005). Deviations from this basic plan have been described in the most primitive of butterfly families, the papilionids, in which two rounds of duplication of the LW eye opsin gene have occurred (Briscoe, 1998;Kitamoto et al, 1998;Briscoe, 2001); and in the pierids, in which a duplicate blue opsin gene has been reported (Arikawa et al, 2005). In all butterfly species studied, opsin mRNA expression in the eye is similar between the sexes: the R1 and R2 photoreceptor cells express either UV or B opsin mRNAs and the R3-9 photoreceptors express LW opsin mRNAs.…”
SUMMARY
Although previous investigations have shown that wing coloration is an important component of social signaling in butterflies, the contribution of opsin evolution to sexual wing color dichromatism and interspecific divergence remains largely unexplored. Here we report that the butterfly Lycaena rubidus has evolved sexually dimorphic eyes due to changes in the regulation of opsin expression patterns to match the contrasting life histories of males and females. The L. rubidus eye contains four visual pigments with peak sensitivities in the ultraviolet (UV;λ max=360 nm), blue (B; λmax=437 nm and 500 nm, respectively) and long (LW; λmax=568 nm) wavelength range. By combining in situ hybridization of cloned opsinencoding cDNAs with epi-microspectrophotometry, we found that all four opsin mRNAs and visual pigments are expressed in the eyes in a sex-specific manner. The male dorsal eye, which contains only UV and B (λmax=437 nm)visual pigments, indeed expresses two short wavelength opsin mRNAs, UVRh and BRh1. The female dorsal eye, which also has the UV and B (λmax=437 nm) visual pigments, also contains the LW visual pigment, and likewise expresses UVRh, BRh1 and LWRh mRNAs. Unexpectedly, in the female dorsal eye, we also found BRh1 co-expressed with LWRh in the R3-8 photoreceptor cells. The ventral eye of both sexes, on the other hand, contains all four visual pigments and expresses all four opsin mRNAs in a non-overlapping fashion. Surprisingly, we found that the 500 nm visual pigment is encoded by a duplicate blue opsin gene, BRh2. Further, using molecular phylogenetic methods we trace this novel blue opsin gene to a duplication event at the base of the Polyommatine+Thecline+Lycaenine radiation. The blue opsin gene duplication may help explain the blueness of blue lycaenid butterflies.
Butterflies of the family Pieridae are brightly colored, ranging from white to red, caused by various pterin pigments concentrated in scattering spheroidal beads in the wing scales. Given the sparsity of the beads in the wing scales, the high brightness suggests a scattering strength of the beads that significantly surpasses that of typical cuticular chitin beads with the areal density found in the wing scales. To elucidate this apparent contradiction, the optical signature of the pierids' highly saturated pigmentary colors are analyzed by using Jamin–Lebedeff interference microscopy combined with Kramers–Kronig theory and light scattering modeling. This study shows that extreme pterin pigment concentrations cause a very high refractive index of the beads with values above 2 across the visible wavelength range, thus creating one of the most highly light scattering media thus far discovered in the animal kingdom.
As most work on flower foraging focuses on bees, studying Lepidoptera can offer fresh perspectives on how sensory capabilities shape the interaction between flowers and insects. Through a combination of innate preferences and learning, many Lepidoptera persistently visit particular flower species. Butterflies tend to rely on their highly developed sense of colour to locate rewarding flowers, while moths have evolved sophisticated olfactory systems towards the same end. However, these modalities can interact in complex ways; for instance, butterflies' colour preference can shift depending on olfactory context. The mechanisms by which such cross-modal interaction occurs are poorly understood, but the mushroom bodies appear to play a central role. Because of the diversity seen within Lepidoptera in terms of their sensory capabilities and the nature of their relationships with flowers, they represent a fruitful avenue for comparative studies to shed light on the co-evolution of flowers and flower-visiting insects.
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