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First published online May 19, 2008
Journal of Experimental Biology 211, 1805-1813 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.013045
The adaptive evolution and processing of sensory systems |
Reconstructing the ancestral butterfly eye: focus on the opsins
Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA
e-mail: abriscoe{at}uci.edu
Accepted 26 November 2007
Summary
The eyes of butterflies are remarkable, because they are nearly as diverse
as the colors of wings. Much of eye diversity can be traced to alterations in
the number, spectral properties and spatial distribution of the visual
pigments. Visual pigments are light-sensitive molecules composed of an opsin
protein and a chromophore. Most butterflies have eyes that contain visual
pigments with a wavelength of peak absorbance, 
max, in the
ultraviolet (UV, 300–400 nm), blue (B, 400–500 nm) and long
wavelength (LW, 500–600 nm) part of the visible light spectrum,
respectively, encoded by distinct UV, B and LW opsin genes. In the compound
eye of butterflies, each individual ommatidium is composed of nine
photoreceptor cells (R1–9) that generally express only one opsin mRNA
per cell, although in some butterfly eyes there are ommatidial subtypes in
which two opsins are co-expressed in the same photoreceptor cell. Based on a
phylogenetic analysis of opsin cDNAs from the five butterfly families,
Papilionidae, Pieridae, Nymphalidae, Lycaenidae and Riodinidae, and
comparative analysis of opsin gene expression patterns from four of the five
families, I propose a model for the patterning of the ancestral butterfly eye
that is most closely aligned with the nymphalid eye. The R1 and R2 cells of
the main retina expressed UV–UV-, UV–B- or B–B-absorbing
visual pigments while the R3–9 cells expressed a LW-absorbing visual
pigment. Visual systems of existing butterflies then underwent an adaptive
expansion based on lineage-specific B and LW opsin gene multiplications and on
alterations in the spatial expression of opsins within the eye. Understanding
the molecular sophistication of butterfly eye complexity is a challenge that,
if met, has broad biological implications.
Key words: eye evolution, color vision, photoreceptor, rhodopsin, visual pigment, opsin, sexual dimorphism
Introduction
The butterfly eye is a marvel of evolution. Butterfly vision, like that of
other insects, is based on three major classes of photoreceptor, with peak
sensitivity (max) in the ultraviolet (UV, 300–400
nm), blue (B, 400–500) and long wavelength (LW, 500–600 nm) part
of the light spectrum. At the molecular level, these visual pigments are
composed of a retinal-based chromophore (e.g.
11-cis-3-hydroxyretinal) (Smith
and Goldsmith, 1990
) attached by a Schiffbase linkage to an opsin
protein. The spectral tuning of the visual pigment wavelength of peak
absorbance, max, is achieved through the interaction of the
chromophore with critical amino acid residues within the opsin. Changes in the
polarity of amino acids in the chromophore-binding pocket of opsins, for
example, affect the distribution of electrons in the 
-electron system of
the chromophore, producing a diversity of max values
(Honig et al., 1976). In the
case of the butterfly visual pigments, the three major spectral classes are
encoded by ancient duplications, which produced distinct UV, B and LW opsin
genes.
Unlike those of bees, the eyes of butterflies are anatomically and
physiologically diverse (Peitsch et al.,
1992; Briscoe and Chittka,
2001; Stavenga and Arikawa,
2006; Frentiu et al.,
2007b; Frentiu et al.,
2007a). This is due in part to lineage-specific opsin gene
duplications, as well as to changes in the kind and distribution of lateral
filtering pigments (Arikawa and Stavenga,
1997; Stavenga,
2002).
To understand this diversity, this review focuses on the eyes of four species of butterfly for which we have the most complete information, Danaus plexippus Linnaeus, Lycaena rubidus Behr, Pieris rapae crucivora Boisduval and Papilio xuthus Linnaeus, and whose eyes serve as prototypes for the butterfly families Nymphalidae, Lycaenidae, Pieridae and Papilionidae, respectively. Although the importance of non-opsin-based filtering pigments for modifying photoreceptor sensitivity to light is mentioned, it is not yet clear whether the filtering pigments in different families are homologous or not; therefore I have intentionally spotlighted the evolution of the opsins themselves because of the homologous relationship between opsin protein sequences between butterfly families and the spectral range of vision. By analyzing the physiologically determined photopigment absorbance spectra and the phylogenetic relationship of opsin gene sequences, overlaid with a character map of opsin expression patterns, I propose a novel model of the evolutionary events leading from an ancestral butterfly eye to the radiation of eye types observed today. And with an eye to the future, I emphasize a few fertile areas for further investigation.
Anatomy of the butterfly eye
Anatomically, the basic unit of the butterfly compound eye is the ommatidium. An ommatidium is composed of nine photoreceptor cells (R1–9) along with primary and secondary pigment cells. An ommatidium from the simplest eye, that of nymphalid butterflies, consists of two tiers composed, respectively, of eight photoreceptor cells (R1–8) that are elongated, and a tiny R9 cell that sits just above the basement membrane (Fig. 1A). Light passing through the cornea is focused by the crystalline cone onto the rhabdom. The fused rhabdom is composed of nine rhabdomeres, the microvillous membranes protruded by the individual photoreceptor cells, in which the visual pigments are embedded.
|
UV and B opsin mRNA expression define three ommatidial subtypes in the main retina
The ommatidia of the main retina of the nymphalid eye are divided into
three subtypes with respect to opsin mRNA expression, with R1 and R2
photoreceptor cells expressing UV–UV, UV–B or B–B, while the
outer R3–8 cells express the LW opsin
(Fig. 1B)
(Briscoe et al., 2003). The
monarch butterfly, Danaus plexippus, is a nymphalid butterfly whose
eye typifies this pattern of opsin mRNA expression
(Fig. 1C–E)
(Sauman et al., 2005). The
identity of the opsin expressed in the R9 cell of monarchs is unknown, but is
likely to be the same as in another nymphalid Vanessa cardui, in
which R9 expresses the LW opsin (Briscoe
et al., 2003).
In addition to the ommatidia of the main retina, butterfly eyes also
contain a dorsal rim area (DRA), like that found in other insects
(Labhart and Meyer, 1999). In
monarchs, the DRA R1–8 cells express the UV opsin exclusively
(Sauman et al., 2005); these
ommatidia contain rhabdoms whose microvilli are anatomically specialized to
detect polarized skylight (Reppert et al.,
2004). This monochromatic pattern of opsin expression in the DRA
is important for efficient perception of polarized light, by avoiding
interference with color information
(Labhart and Meyer, 1999).
Spectral diversity of butterfly visual pigments
The wavelength of peak absorbance, max, of visual
pigments can be directly measured using epi-microspectrophotometry, or derived
from the spectral sensitivity curves of intracellular recordings of individual
photoreceptor cells. In both cases, the experimental data are matched to an
idealized rhodopsin template (Stavenga et
al., 1993; Palacios et al.,
1996), and a computational model is then applied to find the best
estimate of max.
Based on such measurements, the spectral diversity of visual pigments in
the eyes of butterflies is striking. As already alluded to, the eye of the
monarch contains the smallest number of butterfly photopigments (P) with one
UV (max=340 nm or P340), one B (P435) and one LW (P545)
(Stalleicken et al., 2006;
Frentiu et al., 2007a)
(Fig. 2A). The lycaenid
Lycaena rubidus eye contains four photopigments: one UV (P360), two B
(P437 and P500) and one LW (P568) (Bernard
and Remington, 1991) (Fig.
2B). The papilionid Papilio xuthus eye contains the
largest number of butterfly photopigments so far described, with one UV
(P360), one B (P460) and three LW (P515, P530 and P575)
(Arikawa, 2003)
(Fig. 2C). The eye of the
pierid Pieris rapae contains four photopigments: one UV (P360), two B
(P425 and P453) and one LW (P563) (Qiu and
Arikawa, 2003a; Qiu and
Arikawa, 2003b) (Fig.
2D).
|
;
Kitamoto et al., 2000;
Wakakuwa et al., 2004;
Arikawa et al., 2005;
Sauman et al., 2005;
Sison-Mangus et al., 2006;
Frentiu et al., 2007a), and
with these data a gene tree has been constructed for each of the three
spectral classes of opsin: UV, B and LW
(Fig. 3A–C,
respectively). Species from all five butterfly families, Papilionidae
(Papilio xuthus and P. glaucus Linnaeus), Pieridae
(Pieris rapae), Nymphalidae (Danaus plexippus), Lycaenidae
(Lycaena rubidus) and Riodinidae (Apodemia mormo Felder and
Felder) have been included to illustrate the astonishing fact that independent
duplications of either the B or LW opsin have occurred in each family,
rendering the eyes of butterflies the most diverse yet characterized among
insects.
|
For each of the butterfly family examples, only one UV opsin gene has been
isolated, including from the riodinid Apodemia mormo, presented here
for the first time (Fig. 3A).
By contrast, duplicate B opsin genes have been isolated from P.
rapae, encoding blue-absorbing (P453) and violet (V)-absorbing (P425)
photopigments (Arikawa et al.,
2005), and from L. rubidus, encoding blue-absorbing
(P437) and blue–green-absorbing (P500) photopigments
(Sison-Mangus et al., 2006).
The bootstrap values of the relevant nodes and branching order of the tree,
which nicely matches the current phylogeny of butterfly families based on
independent molecular and morphological markers (see below)
(Wahlberg et al., 2005),
indicate that the duplication of the blue opsin gene in pierids and in
lycaenids occurred independently.
The situation for the LW opsins, with respect to the frequency of gene
duplication, is more complex. The eyes of pierids, nymphalids and lycaenids
express only one LW opsin gene encoding photopigments of P563, P545 and P568,
respectively (Wakakuwa et al.,
2004; Sauman et al.,
2005; Sison-Mangus et al.,
2006), while the papilionid eye expresses three (P515, P530 and
P575) (Kitamoto et al., 1998)
and the riodinid eye expresses two LW opsin genes (P505 and P600)
(Frentiu et al., 2007a)
(Fig. 3C). To add more
complexity, at least one additional near full-length LW opsin cDNA,
PglRh4, for a total of four LW opsin genes, has been isolated from
head tissue of Papilio glaucus
(Briscoe, 1998;
Briscoe, 2000) – an
opsin that is not apparently expressed in the eye (A.D.B., unpublished data)
(Lampel et al., 2005). The
presence of two LW opsin genes in the genome of the silkmoth Bombyx
mori, and the apparent close homology of the sphingid moth Manduca
sexta opsin gene MANOP1 with one of them
(Fig. 3C), suggests that M.
sexta too may contain a second LW opsin, which is a homolog of the
silkmoth larval `brain opsin' gene Boceropsin
(Shimizu et al., 2001).
The fate of duplicate genes is typically classified into one of two
categories: subfunctionalization (`division of labor'), in which one or both
of the paralogs acquires a more restricted expression pattern and/or
biological activity than the common ancestral gene, and neofunctionalization,
in which the paralogs are free to acquire new expression patterns and/or
functions (Force et al.,
1999). Opsin duplication in butterflies can fall into either
category (Briscoe, 2001).
Importantly, duplication of butterfly opsin genes has led to the evolution of
novel max values that ultimately impact on behavior
(Kelber, 1999;
Kelber and Pfaff, 1999;
Kinoshita et al., 1999).
Subfunctionalization of B opsins in Pieris
In Pieris rapae, LW opsin expression is identical to that of the
nymphalid eye in that its single LW opsin transcript is expressed in
R3–8 (Wakakuwa et al.,
2004). In addition, the expression of the UV opsin in
Pieris also follows that of the nymphalid in that it is found in
either UV–UV or UV–B combinations in R1 and R2. In what appears to
be a complete departure from the nymphalid ground plan for the eye, however,
the B–B ommatidial subtype has been completely replaced in P.
rapae ventral eye by a V–V ommatidial class that is the product of
a B opsin gene duplication (Fig.
4). Since the violet-absorbing visual pigment is encoded by a
duplicate B opsin (Fig. 3B),
and the pattern of B opsin expression in other butterflies considered so far
is restricted to the R1 and R2 cells, the V–V class of ommatidium can be
interpreted as an example of subfunctionalization of the ancestral B opsin
domain of expression, into a more limited expression pattern.
|
Subfunctionalization and neofunctionalization of B opsins in Lycaena has led to a sexually dimorphic eye
The pattern of duplicate B opsin expression in Lycaena rubidus
illustrates both neofunctionalization and subfunctionalization and leads to
the situation in which male and female butterflies literally see the world
through different eyes. In the compound eye of this animal, four opsin genes
are expressed – one UV (UVRh), duplicate B, B1 (BRh1)
and B2 (BRh2), and one LW (LWRh) opsin
(Fig. 3). It is the dorsal eye
of L. rubidus that is sexually dimorphic. Unlike the papilionid,
pierid or nymphalid eye, in which R3–8 express one or more LW opsins, in
L. rubidus males, R3–8 exclusively express the B1 (dark blue
ovals) opsin, while in females, R3–8 co-express the B1 and LW (dark
blue–orange ovals) opsins (Fig.
4), an example of neofunctionalization of the B1 opsin domain of
expression. In addition, the R1 and R2 cells of the dorsal eye of both males
and females express UV–UV almost exclusively, with a minor number of
ommatidia expressing the UV–B1 or B1–B1 combination
(Sison-Mangus et al., 2006).
The highly territorial male L. rubidus
(Bernard and Remington, 1991)
probably use their dorsal eye for dichromatic color vision and the detection
of moving objects, such as airborne males.
The ventral eye, by contrast, has a pattern of LW opsin expression that is more consistent with the other butterfly families examined: R3–8 of the ventral retina express the LW opsin. It is here, though, that subfunctionalization of the second blue opsin duplicate gene, B2 (light blue ovals, Fig. 4), is evident. The ventral retina contains six classes of ommatidia that differ according to the opsins expressed in R1 and R2: UV–UV, UV–B1, UV–B2, B1–B2, B1–B1 or B2–B2 (Fig. 4).
Intriguingly, while butterflies in the genus Papilio use duplicate
LW opsins to see green (Kelber,
1999), the lycaenid Polyommatus icarus, uses its
duplicate B2 opsin, in conjunction with its LW opsin, to see in the green part
of the spectrum extending up to 560 nm
(Sison-Mangus et al., 2008).
This suggests that natural selection has hit upon alternative strategies for
color vision in the green range in lycaenid and papilionid butterflies.
Subfunctionalization and neofunctionalization of LW opsin expression in Papilio
The basic pattern of photoreceptor cell morphology and opsin mRNA
expression exemplified by the nymphalid eye is also complicated in the
swallowtail butterfly Papilio by alterations in the shapes of the
photoreceptor cells and by the expression of the three duplicate LW opsins.
For example, the ommatidium of the papilionid eye is organized into three
tiers rather than two: a distal tier in which the cell bodies of the
R1–4 cells are the widest, a middle tier in which the cell bodies of the
R5–8 cells are the widest, and a third tier in which the cell body of
the tiny R9 cell is located (Fig.
5).
|
In Papilio xuthus, the butterfly eye about which we know the most,
three LW opsin genes (PxRh1, PxRh2 and PxRh3) are also
expressed in the eye. In this butterfly, as in lycaenids, the main retina is
divided into two parts: the dorsal eye and the ventral eye. Like nymphalids,
the R1 and R2 cells of both the dorsal and ventral eye express UV–UV,
UV–B or B–B opsin mRNAs. Unlike nymphalids, the R3 and R4 cells of
the dorsal eye of P. xuthus express the PxRh2 opsin mRNA
(orange ovals, Fig. 4), while
in the ventral eye, the R3 and R4 cells co-express PxRh1 and
PxRh2 (green–orange ovals,
Fig. 4)
(Kitamoto et al., 1998).
Strikingly, the expression of opsins in R5–8 is coordinated with the
expression of opsins in R1 and R2 (Arikawa,
2003). In the dorsal eye, one subtype contains B–B in R1 and
R2 and PxRh2 (orange ovals) in R5–8, another subtype contains
UV–B in R1 and R2 and PxRh3 (yellow ovals) in R5–8 and a
third subtype contains UV–UV in R1 and R2 and PxRh2 and
PxRh3 (orange–yellow) in R5–8. The ventral eye contains
the same three ommatidial subtypes as in the dorsal eye, except as noted
above, the PxRh1 opsin is also co-expressed with the PxRh2
opsin in R3 and R4. Altogether, there are at least six classes of ommatidia
with respect to opsin expression in the main retina of P. xuthus
(Fig. 4).
Interestingly, the most phylogenetically basal of the P. xuthus LW
opsin gene duplicates expressed in the eye, PxRh2
(Fig. 3), is also the one that
has the widest expression in the R3–8 cells. And, like the LW opsin of
V. cardui (Briscoe et al.,
2003) and P. glaucus
(Fig. 5K,L), it is also
expressed in the R9 cell. This pattern is consistent with an ancestral
function for PxRh2 and a subfunctionalization of the more recent
duplicates, PxRh1 and PxRh3
(Briscoe, 2000), into a more
limited domain of expression. It is also worth noting that PxRh3
exemplifies neofunctionalization, as it encodes P575, whose absorbance
spectrum maximum is quite red shifted compared with PxRh2, which
encodes P530 [see discussion in Briscoe
(Briscoe, 2000)].
|
;
Arikawa, 2003;
Stavenga and Arikawa, 2006).
Even more remarkable is that the eye of Pieris rapae crucivora is
sexually dimorphic with respect to the expression of a blue-absorbing
filtering pigment that is present only in the eye of males and is co-expressed
with the violet opsin (Arikawa et al.,
2005). Moreover, some butterfly eyes not reviewed here lack
filtering pigments entirely (Briscoe and
Bernard, 2005). Lateral filtering pigments coat the rhabdom, and
filter short wavelength light, thus shifting the sensitivity of the visual
pigments to the longer wavelengths. Examples of such an effect for red
filtering pigments have been shown electrophysiologically in Heliconius
erato (Bernhard et al.,
1970; Swihart and Gordon,
1971; Struwe,
1972), Papilio xuthus
(Arikawa et al., 1987;
Arikawa et al., 1999a) and
Pieris rapae crucivora (Qiu et
al., 2002; Wakakuwa et al.,
2004), and for the blue-absorbing filtering pigment of P.
rapae (Arikawa et al.,
2005).
The biological significance of filtering pigments is that while they do not
expand the total visual range of the animal (this is dependent on the visual
pigments themselves), they may expand the animal's color vision range. The red
filtering pigments in the eyes of butterflies, however, do not appear to have
a unified function. For instance, behavioral tests have shown that the
nymphalid Heliconius erato uses a heterogeneously expressed red
filtering pigment together with a single LW opsin to produce expanded color
vision in the long wavelength range when foraging
(Zaccardi et al., 2006), but
the lycaenid Polyommatus icarus, which also has a heterogeneously
expressed red filtering pigment in its eye, does not appear to have expanded
color vision, at least when tested in the context of feeding
(Sison-Mangus et al.,
2008).
Providing a clearer role for filtering pigments in color vision will
require further behavioral testing in a larger collection of butterfly species
and, in some cases, such as the red receptor of Papilio, which
co-expresses a red-filtering pigment with a red-absorbing visual pigment
(Arikawa, 2003), it will be
difficult to disentangle the impact of the filtering pigment on color vision
from that of their coordinately expressed opsin.
Reconstructing the ancestral butterfly eye
The phylogeny of the butterflies provides a framework for reconstructing
the pattern of opsin expression in the ancestral eye. Within the true
butterflies (Papilionoidea) the current understanding of familial
relationships is Papilionidae+{Pieridae+[Nymphalidae+
(Lycaenidae+Riodinidae)]} (Wahlberg et
al., 2005), where papilionid and pierid butterflies represent the
most basal lineages, and nymphalid, lycaenid and riodinid the most derived
(Fig. 6). The inferred
instances of lineage-specific opsin gene duplications
(Fig. 3) together with the
extant pattern of opsin mRNA expression (summarized in
Fig. 4) can be mapped onto the
butterfly family species tree to infer the most parsimonious ancestral state,
using the sphingid moth Manduca sexta as an outgroup. Remarkably, the
ancestral state is not represented by the most basal butterfly lineages but,
instead, is manifested in the nymphalids.
Fig. 6A shows the most
parsimonious reconstruction of the ancestral pattern of opsin mRNA expression
in the R1 and R2 cells. Using this reconstruction, the ancestor of all
butterfly eyes had merely one UV (gray box and ovals) and one B opsin (dark
blue box and ovals) gene expressed in a non-overlapping fashion in the R1 and
R2 cells – a pattern shared with the opsin expression in the main retina
of sphingid moths (White et al.,
2003) and bees (Spaethe and
Briscoe, 2005; Wakakuwa et
al., 2005) and consistent with the existence of only one UV and
one B opsin gene in the genome of the silkmoth, Bombyx mori
(Mita et al., 2004;
Xia et al., 2004).
Subsequently, sometime after the divergence of the pierid from the
papilionid and nymphalid+(lycaenid+riodinid) lineages, a B opsin gene
duplication arose, presumably prior to the radiation of the
Pierinae+Coliadinae subfamilies, since a homologue of the P. rapae
(Pierinae) V opsin has been cloned from Colias philodice
(Sison-Mangus et al., 2006), a
species in one of the other major pierid subfamilies, Coliadinae. [The two
more basal subfamilies, Pseudopontiinae and Dismorphiinae
(Braby et al., 2006;
Chew and Watt, 2006) have not
yet been assayed for opsins.]
The pattern of ancestral LW opsin expression can be reconstructed
similarly, and doing so suggests that the common ancestor of all butterfly
eyes expressed a single LW opsin in the R3–8 cells (and also probably in
the R9 cell) (Fig. 6B). Under
this scenario, sometime after the split between the lineage leading to
Papilio and the other butterfly families, two rounds of LW opsin gene
duplication occurred, followed by subfunctionalization of the newer paralogs
in Papilio. Intriguingly, the topology of the LW opsin gene tree also
implies that the LW opsin duplicated prior to the radiation of the riodinid
and lycaenid subfamilies, and that the homolog of the riodinid LWRh1 opsin was
lost in the lineage leading to lycaenids. Subsequently, in the case of the
highly divergent, sexually dimorphic pattern of opsin expression in the
R3–8 cells of L. rubidus, the co-expression of a B opsin, B1 in
R3–8, along with the LW opsin, can be viewed as an intermediate step
along the evolution of a new function for B1 opsin in the dorsal eye of males
(Sison-Mangus et al.,
2006).
An eye to the future
One could imagine extending ancestral state reconstruction to other parts
of the butterfly visual system to further understand the evolution of
photoreceptor patterning, color vision, and even an integration of the
evolution of the visual system with wing color. For instance, at present, the
molecular identity, phylogenetic distribution and behavioral impact of
filtering pigments in the eyes of butterflies are not well understood, but it
seems likely that the ancestral butterfly eye contained heterogeneously
expressed lateral filtering pigments, with secondary losses. Like the opsins,
lateral filtering pigments may have evolved lineage-specific modifications and
expression patterns that could have an impact on the color vision system. And,
as has been pointed out, some of the pigments found in the brightly colored
scales of butterfly wings are evolutionarily derived from eye pigments
(Nijhout, 1991;
Reed and Nagy, 2005). So it is
possible that modifications of wing pigments co-evolved with the modifications
of eye pigments.
Similarly, it is not known how the dorsal rim area ommatidium of the
ancestral butterfly eye was patterned with respect to opsin expression. Unlike
most moths, which are primarily nocturnal and may use polarized moonlight or
starlight for navigation, butterflies are diurnally active and use the
polarized skylight as a navigational cue
(Froy et al., 2003;
Reppert et al., 2004). If
different opsins are expressed in the DRA ommatidia of different butterflies,
this would imply that the polarized skylight cues used by butterflies are not
uniform. In fact, it would not be surprising if this were the case, given the
diversity of spectral classes of photoreceptors found in the DRA ommatidia of
different insects (Labhart and Meyer,
1999) and the apparent ease with which domains of opsin expression
in butterflies have been altered. A hint that the DRA ommatidia themselves may
have evolved in Lepidoptera is evident in the observation that while the
R1–8 cells in monarch DRA ommatidia express only the UV opsin
(Sauman et al., 2005), in the
hawkmoth, Manduca sexta, only some of the photoreceptor cells in the
DRA ommatidia express the UV opsin (P357), while other photoreceptor cells
express none of the other (B and L) opsins cloned
(White et al., 2003).
Finally, alterations in opsin expression patterns beg the question of
whether or not the neural circuitry necessary to process this information has
evolved. At present, correlation between opsin expression and photoreceptor
axon terminals has only been attempted in the swallowtail
(Takemura et al., 2005;
Takemura and Arikawa, 2006).
The collateral morphology of the axons of the R5–8 cells of P.
xuthus varies according to which LW opsin they express. But what about in
other butterflies that do not have duplicated LW opsins?
In conclusion, it is clear that the butterfly eye is one of the most beautifully honed instruments of evolution. Bringing to bear molecular tools that are now becoming available for non-model organisms (e.g. genetic transformation, custom microarrays and RNA interference) will allow a deeper understanding of the biological events involved in butterfly eye diversity that may be applicable to a broader range of biological processes.
Acknowledgments
Thanks to Lisa Nagy for providing a supportive research environment for the Papilio glaucus work, Marilou Sison-Mangus for technical assistance, Matthew McHenry for suggesting character mapping and, especially, Steven Reppert for helpful comments on the manuscript. This work was supported by NSF grants IBN-0346765 and IOS-0646060.
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