|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online January 18, 2008
Journal of Experimental Biology 211, 361-369 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.012617
The lycaenid butterfly Polyommatus icarus uses a duplicated blue opsin to see green
1 Department of Ecology and Evolutionary Biology, University of California,
Irvine, CA 92697, USA
2 Vision Group, Department of Cell and Organism Biology, Lund University,
Helgonavägen 3, S-22362 Lund, Sweden
3 Department of Animal Ecology I, University of Bayreuth, Universitätsstr.
30, D-95440 Bayreuth, Germany
Author for correspondence (e-mail:
almut.kelber{at}cob.lu.se)
Accepted 14 November 2007
 |
Summary |
|---|
 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Key words: lycaenid, color vision, visual pigment, filter pigment, butterfly, opsin
|
INTRODUCTION |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
;
Seki and Vogt, 1998). Spectral
tuning of the visual pigment's wavelength of peak absorbance,
max, is achieved through the interaction of the chromophore
with critical amino acid residues within the opsin. In many insects such as
bees and moths, color vision is based on three classes of photoreceptors with
maximal sensitivity in the ultraviolet (UV), blue (B) and long-wavelength (LW)
range (for reviews, see Briscoe and
Chittka, 2001; Kelber,
2006), that correspond to three classes of opsin protein encoded
by distinct UV, B and LW opsin genes.
Unlike bees and hawkmoths, the visual system among butterfly families is
highly diverse and their color vision abilities have only begun to be explored
(e.g. Kelber and Pfaff, 1999;
Kinoshita et al., 1999;
Weiss and Papaj, 2003;
Ômura and Honda, 2005).
This diversity is based upon lineage-specific opsin gene duplications
(Briscoe, 1998;
Kitamoto et al., 1998;
Arikawa et al., 2005;
Sison-Mangus et al., 2006;
Frentiu et al., 2007) and the
presence in the eye of heterogeneously expressed filtering pigments
(Stavenga, 2002).
In the eyes of several, but not all, butterfly species, lateral
(perirhabdomal) pigment granules are found very close to the rhabdom
(Ribi, 1979;
Arikawa et al., 1999;
Stavenga, 2002;
Briscoe et al., 2003;
Briscoe and Bernard, 2005). In
the described cases, these pigments are red or yellow and thus absorb the
short wavelength end of the light spectrum. The rhabdoms of these butterflies
are narrow and function as wave-guides, in which a fraction of the wave energy
travels outside the rhabdom surface
(Nilsson et al., 1988). It is
this fraction of light that can be absorbed by the perirhabdomal filter
pigment. Since the spatial distribution of light across the rhabdom and
surround is not affected, this influences the spectral composition of the
light traveling inside the rhabdom that can be absorbed by the opsin pigment.
If they absorb light in an appropriate short-wavelength range, perirhabdomal
pigments can shift the sensitivity of the photoreceptor into the longer
wavelengths (Stavenga 2002;
Warrant et al., 2007), which
has been shown electrophysiologically in Papilio xuthus
(Arikawa et al., 1999) and
Pieris rapae crucivora (Wakakuwa
et al., 2004). In Heliconius erato, electrophysiological
data revealed the existence of a red-sensitive receptor over 30 years ago
(Struwe, 1970;
Swihart and Gordon, 1971;
Swihart, 1972). These
butterflies are now known to express only one LW opsin pigment in the eye.
They possess perirhabdomal filter pigments that most likely shift the
sensitivity peak of receptors in a sub-set of ommatidia
(Zaccardi et al., 2006).
If signals from two receptors with different spectral sensitivity are
compared neurally, color vision is possible. For H. erato only,
behavioral evidence has been obtained demonstrating that photoreceptors
expressing the same opsin pigment but differing in sensitivity as a result of
perirhabdomal filter pigment are used for color vision
(Zaccardi et al., 2006). More
behavioral evidence is needed to better understand the evolution of such
systems, particularly since it has been suggested that variation of ommochrome
pigments in butterfly wings may be genetically linked to variation in lateral
filtering pigments in the eyes, thus co-evolution of mating signals and
photoreceptors may have occurred
(Kronfrost et al., 2006).
|
; Sison-Mangus
et al., 2006). 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,
producing visual pigments with max corresponding to 360 nm,
437 nm, 500 nm and 568 nm, respectively
(Fig. 1). The ommatidia of the
lycaenid compound eye contain nine photoreceptor cells, R1–9
(Fig. 2). The ventral eye of
Lycaena rubidus contains six classes of ommatidia that differ
according to the opsins expressed in the R1 and R2 cells: UV-UV, UV-B1, UV-B2,
B1-B2, B1-B1 or B2-B2 (Fig.
2C). The R3–8 cells of the ventral retina express the LW
opsin. In addition, L. rubidus eyes contain a red filtering pigment
that is found exclusively in the ventral area and is located in the R5–8
cells, but only in ommatidia in which B2 is also present
(Sison-Mangus et al., 2006).
Thus, it is possible that in addition to the four purely opsin-based
photoreceptor classes just described, there is a fifth class in the ventral
eye that is based upon the LW opsin together with the red filtering pigment.
This additional spectral class could, in principle, extend color vision
abilities of the animal in the long wavelength range.
|
). The highly territorial male L. rubidus probably
use their dorsal eye for dichromatic color vision and the detection of
sympatric males (Bernard and Remington,
1991).
Like L. rubidus, P. icarus males are highly territorial and engage
in intense male–male interactions
(Lundgren, 1977). Their eyes
also express the duplicate blue opsins, B1 and B2, found in L.
rubidus (Sison-Mangus et al.,
2006). In addition, there is sufficient evidence that P.
icarus use ultraviolet signals to select their mates
(Burghardt et al., 2000;
Knüttel and Fiedler,
2001) but proof of color vision is lacking.
In the present study, we examined color vision in Polyommatus icarus in the long-wavelength range. First, we asked whether P. icarus extends its color vision in the red range, possibly via the effects of a perirhabdomal filtering pigment. Secondly, we asked whether the putatively blue-green-absorbing visual pigment encoded by the duplicate blue opsin, B2, is used for color vision in the context of feeding.
|
MATERIALS AND METHODS |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
). The
eyes were oriented sideways such that the first few cuts showed tangential
sections of the ommatidia in the lateral part of the eye and the later cuts
were longitudinal sections of the frontal part of the eye. Some eyes were also
sectioned more frontally to obtain tangential sections of ommatidia in this
part of the eye.
Eye-shine photographs
Two dark-adapted female P. icarus eyes were photographed using the
method described earlier (Zaccardi et al.,
2006) to look at the eye-shine of different ommatidial types.
Eye-shine is light that initially passes through the rhabdom and is not
absorbed by the visual pigments. Once the light reaches the tapetum basal to
the rhabdom, it is reflected back to be absorbed by the visual pigments. Any
unabsorbed light leaving the eye is seen as eye-shine. All butterfly eyes
examined so far reflect eye-shine (Miller and Bernard, 1968;
Bernard and Miller, 1970;
Stavenga, 2002), except for
those in the most basal family, the Papilionidae
(Miller, 1979) and in the
pierid genus, Anthocharis
(Takemura et al., 2007).
Animals were immobilized with wax and placed with the centre of curvature of
one eye in the centre of a goniometer. This way, eye-shine of ommatidia
looking dorsally (D), laterally (L) or anteriorly (A) could be taken as well
as pictures of ommatidia looking into intermediate directions. Light from a 45
W xenon lamp was focused on the centre of curvature of the eye for
illumination of a large patch of ommatidia. A microscope cover glass was used
as a semi-transparent mirror to allow observation from the direction of the
incident light (orthodromic illumination). Photographs were taken with the
shutter open for 0.1 s with intervals of 10 s to avoid pupil closure. Pictures
were taken using a digital camera and a Zeiss Luminar 25 mm objective.
PCR, cloning and sequencing of opsin genes
A cDNA library was synthesized from the total RNA of three female P.
icarus heads and screened for opsin transcripts following the procedures
described (Sison-Mangus et al.,
2006). Briefly, 3'RACE (rapid amplification of cDNA ends)
products were amplified using the degenerate primer (5' GAA CAR GCW AAR
AAR ATG A 3') and cloned. Then, 95 plasmids were screened by
EcoRI digestion. 24 plasmids with inserts were sequenced.
Gene-specific reverse primers (UV, 5' TTT GCA AGT CAC GGC TGG TAT C
3'; LW, 5' GCT CGG TAC TTA GGA TGG CTT ATG 3' and 5'
AAT GTG CAA CTT CTA ACC CGA TAC 3') were then designed and used to
amplify 5'RACE products. The remaining 3'RACE plasmid clones were
further screened for opsin-specific gene inserts via multiplex PCR.
Three opsin-specific primer pairs were mixed in one PCR cocktail and plasmids
that did not amplify any product were sequenced.
Phylogeny reconstruction
P. icarus opsin genes were aligned with other homologous
lepidopteran opsins downloaded from GenBank in Mega 3.0
(Kumar et al., 2004). The gene
trees were reconstructed by neighbor-joining analysis of nucleotides using
Tamura–Nei distance, heterogeneous pattern of nucleotide substitution
among lineages and complete deletions of gaps. The reliability of the tree was
sampled with 1000 bootstrap replicates.
Animals, training and test conditions
Two behavioural experiments were performed for this study. The first
experiment (red color vision) was performed during September 2001, the second
experiment (green color vision) during July and August 2006. For the red color
vision experiment, 122 pupae of P. icarus were obtained from the
offspring of four females from the same wild population in Bavaria, Germany,
using breeding methods described by Burghardt and Fiedler
(Burghardt and Fiedler, 1996).
For the green color discrimination experiment, two groups of P.
icarus animals obtained from pupae were used, the F1
generation of butterflies caught in Lund, Sweden and those of P.
icarus butterflies from Bavaria, Germany. Butterflies caught in Lund were
placed in a butterfly cage and allowed to lay eggs on bird's foot trefoil
Lotus corniculatus. Caterpillars were collected and fed ad
libitum with young L. corniculatus leaves. They were grown in a
high humidity chamber above 25°C, and food was changed daily until
pupation. Pupae from both groups were kept in an open plastic box maintained
at high humidity with 16 h:8 h light:dark photoperiod inside the butterfly
cage.
The experimental cage for behavioral testing was 70 cm wide, 60 cm deep and 50 cm high. For the red color vision test, the cage was illuminated from above by two 18 W Osram Biolux tubes (Osram, Hamburg, Germany) and one 40 W Philips 09N tube (Philips Lighting, Hamburg, Germany), in a 14 h:10 h light:dark regime. For the green color tests, three 18 W Osram Biolux tubes were used. The light intensity during training and tests corresponded to 100 cd m–2. After lights on in the morning, the temperature in the cage increased from 22°C to 30°C within 1 h.
Red color discrimination test
To establish color vision, the animal must be able to detect differences in
the spectral composition of two stimuli irrespective of the relative
intensities (Kelber et al.,
2003). To test if the butterflies had color vision abilities in
general, and whether they could discriminate colors in the red range,
naïve (newly eclosed) animals were trained on an array of 18 feeders that
were positioned on a 10 cmx10 cm horizontal black board. A feeder
consisted of a light emitting diode (LED) surrounded by a short piece of
transparent tubing that served as reservoir for 10% (w:w) sucrose solution.
For an exact description and picture of the feeder board, see Kelber and Pfaff
(Kelber and Pfaff, 1999). Only
the six yellow (590 nm) feeders contained sucrose solution, and the six red
(640 nm) and six blue (430 nm) feeders were empty. The butterflies easily
learned to land on the feeder tubes and extend their proboscis into the
feeders. Although all animals were trained and tested together, for individual
identification each animal was marked by a number on the wing. During tests,
only two colors (yellow and either red or blue) were used; LEDs of the third
color were switched off. Each landing of a butterfly on a feeder was counted
as a choice. Landings on feeders where another butterfly was sitting were
avoided by gently removing butterflies from feeders after landing. The
intensities of the rewarded color (yellow) and the unrewarded color (red or
blue, in respective tests) were adjusted such that the ratio of the
intensities of rewarded (+) and unrewarded color ranged from 0.1 to 4. Animals
were tested for ca. 1 h per day, and tests with different colors and intensity
ratios were performed in a random order. Not all animals survived long enough
to be tested. Data from the entire population were pooled, and G-tests
(Sokal and Rohlf, 1995)
performed to test for statistical significance of results.
Green color discrimination test
We wished to investigate whether P. icarus uses one of its
duplicated blue opsins (BRh2, encoding a visual pigment with possibly
a max 
500 nm as in Lycaena rubidus) in
discriminating colors in the green part of the light spectrum (see
Fig. 1). Since P.
icarus only possesses one LW opsin (that may produce a visual pigment
with a max 568 nm as in L. rubidus), we
hypothesized that the animal utilizes its BRh2 visual pigment to
extend its color discrimination in the green range.
In these experiments, animals were also trained to discriminate a rewarded
(+) color from an unrewarded color. Each stimulus was produced by light from a
lamp with adjustable intensity, passed through a narrow-band (10 nm)
interference filter and presented on a feeder of 20 mm diameter. Both feeders
were presented on the same feeder plate. The behavioral apparatus and
experimental method we used are described in more detail elsewhere
(Zaccardi et al., 2006), but
there were some differences. In the present study, the feeder plate was
oriented horizontally instead of vertically, which allowed the small
butterflies to land more easily on the feeders. Additionally, the floor of the
cage was covered with black paper, which dissuaded the animals from perching
on the floor. Naïve butterflies were trained to find 10% sugar solution
on the positive feeder 6–8 h after eclosion. The naïve butterflies
were first offered cotton soaked in sugar solution. Once their proboscis was
extended, the animals were brought to the positive feeder and allowed to feed
ad libitum. Training continued for 3–7 days until the animals
flew freely toward the positive feeder (supplementary material Movie 1). The
light intensity ratio of 0.1 was used in training the butterflies.
Four colors were used in the experiments. These were produced using filters transmitting light at 450 nm, 560 nm, 570 nm and 590 nm, respectively. In each experiment, two color stimuli with varying light intensity combinations were presented simultaneously to the animals. We used three different ratios of 0.1, 1 and 10 between the light intensity of the rewarded and unrewarded stimulus for the two color stimuli, ranging between 9x1015 and 1.2x1017 photons sr–1 cm–2 s–1.
We first trained the animals to discriminate between 450 nm (blue) and 590 nm (yellow), with the latter designated as the rewarded (+) stimulus. Only one individual at a time was allowed to approach the feeder. A choice was registered if the animal extended its proboscis. The animal was allowed to feed for 3 s and then gently removed from the feeder. Tarsus extension was not counted as a choice and, if displayed, the animal was gently removed from the feeder. Between choices, the feeders were covered with black cardboard and the side and light intensity ratio between rewarded (+) and unrewarded (–) stimuli changed in a pseudorandom manner. The feeders were cleaned with water after each individual session to remove sugar or odor traces. An individual must have made a minimum of ten choices for each of three intensity combinations before being trained for the next experiment.
In the subsequent tests, we wanted to determine the color vision limit of
the animal between the green and yellow colors. The same individuals that were
able to discriminate colors in the first experiment were continuously trained
to 590 nm as the rewarded (+) stimulus. They were then tested for their
ability to discriminate this wavelength from either 560 nm (–) or 570 nm
(–). The number of choices made by an individual for each intensity
combination was tested for statistical significance using the test of binomial
proportions of P=0.5, compared in the table of critical values for
tests of proportions [table Q (Rohlf and
Sokal, 1995) p. 107] using the two-tailed significance level
(
) of 0.05.
|
RESULTS |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
) and we were interested in whether or not P. icarus
eyes contain a filtering pigment like Lycaena rubidus that could
possibly extend its color vision capability into the red range. Indeed, we
found a red filtering pigment in the P. icarus eye which was also
present proximally in the R5–8 photoreceptor cells and only expressed
exclusively in a sub-set of ommatidia in the ventral eye
(Fig. 2B). In tangential
sections, the distance between pigment spots was 0.9±0.15 µm
(Fig. 2B). No pigment was seen
over the most distal 30 µm of the rhabdom, pigmentation extended over a
length of 55 µm, and the basal 45 µm were pigment free again (see
supplementary material Fig. S3). We also noticed a difference in the
distribution of these pigment granules between the lateral and anterior sides
of the eye. More ommatidia with red pigmentation were observed in the latter
than in the former (data not shown). Another pigment, the purple pupillary
pigment, which regulates the amount of light entering the ommatidium, was seen
in all ommatidia and was present more distally (data not shown) in the
R1–8 photoreceptor cells.
Red-reflecting ommatidia in the ventral retina
There was a notable heterogeneity of eye-shine color in the retina of
P. icarus (Fig. 3).
Most remarkable was the difference between dorsal and ventral eye-shine. The
dorsal retina was dominated by yellow-reflecting ommatidia while the ventral
retina exhibited yellow- and red-reflecting ommatidia. Interestingly, the
red-reflecting ommatidia were much more abundant in the anterior (frontal)
part of the eye than in the lateral side of the eye. These eye-shine data
correspond rather well with the location and frequency of filtering pigment
granules observed from the Epon eye section in
Fig. 2. Undoubtedly,
red-reflecting ommatidia contain the filtering pigment whereas yellow ones do
not. The presence of red ommatidial eye-shine suggested that the animal may
have red-sensitive photoreceptors in the ventral retina.
|
). To
identify other candidate photoreceptors in the P. icarus retina, we
screened head-specific cDNA. We cloned two more full-length opsin encoding
cDNAs which, based upon phylogenetic analysis, represent UV- and LW-absorbing
pigments (see supplementary material Figs S1, S2;
Fig. 4). The four opsins in
P. icarus were found to be orthologous to those of L.
rubidus, whose gene sequence similarity ranges from 86–89%. Since
P. icarus contains the same four opsin genes as found in L.
rubidus, we assume that the pattern of opsin expression in the adult
compound eye of both lycaenids is similar. Namely, in the ventral retina, the
R3–8 cells likely express the LW opsin while the R1 and R2 cells likely
express either UV-UV, UV-B1, UV-B2, B2-B1, B1-B1 or B2-B2
(Fig. 2C). Together with the
red filtering pigment, it is therefore possible that the P. icarus
ventral eye contains five spectral classes of receptor suitable for color
vision.
|
Red color discrimination is absent in P. icarus
In an experiment where the butterflies were allowed to feed ad
libitum from yellow (590 nm) feeders but did not find any food in red or
blue feeders, they learned to reliably discriminate yellow from blue,
independent of intensities. The animals did not learn to visit the yellow
feeders very well. In tests with the training intensities, they chose the
yellow color in about 70% of the landings (70 animals, G-test,
P<0.05 for all intensity ratios). This choice frequency did not
change with changing intensity ratios (Fig.
5A) and was similar for both sexes (not shown). In tests with
yellow (590 nm) versus red (640 nm) (Fig.
5B), the choice frequency changed dramatically, if the intensity
ratio was changed. From this result, we conclude that the animals use color
vision to discriminate yellow of 590 nm from blue of 430 nm but not to
discriminate yellow from red of 640 nm. For this latter task, the animals
obviously use a brightness cue for discrimination, a cue that does not allow
them to choose the correct color when intensities are changed.
|
|
The results of the behavioural experiments show clearly that P. icarus can use color vision to discriminate rewarding from unrewarding stimuli. The differences in choice frequencies between both color discrimination experiments (70% correct choices in the first set of experiments and 90% correct choices in the second) are most certainly due to the differences in training and testing methods, in which a large number of animals were tested in the first experiment and the motivated specimens were selected during individual training in the second experiment. Together, both experiments show that P. icarus can discriminate colors and that the long-wavelength limit of color vision lies between 560 and 570 nm.
|
DISCUSSION |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
), and
from Pieris rapae, where electrophysiology proved two long-wavelength
receptor types with different spectral sensitivities (620 nm and 640 nm)
(Wakakuwa et al., 2004).
Second, gene duplication of opsins, followed by the gain of new function,
serves as a powerful evolutionary mechanism in fine-tuning the color vision
capability of the animal.
Our eye-shine and anatomical data suggested that P. icarus may
have color vision in the red range. The eye possesses several classes of
ommatidia, one of which is widely distributed in the ventral retina and is
red-reflecting. The red reflection from this class of ommatidia is most likely
produced by the red filtering pigment, which is also found in the ventral
retina. The red reflection could not result from another LW opsin because we
found only one LW opsin transcript. Our hypothesis that the red-reflecting
ommatidia might have contained a red-sensitive photoreceptor is based upon the
interpretation of Stavenga (Stavenga,
2002). If their signals were compared neurally, the receptor with
red filtering pigment, and the receptor without it, could allow the animal to
extend its color vision into the red range.
Our behavioral tests, however, reveal that P. icarus has no color
vision in the red range because it could not distinguish yellow from red.
There are several possible explanations for this finding. First, the lateral
filtering pigment may not in fact shift the sensitivity of the LW receptors as
much as it does in other butterfly eyes. The pigment is only expressed along
55 µm of the rhabdom length, beginning 30 µm proximal from the rhabdom
tip, and it is possible that most light is absorbed by the visual pigment in
the distal-most part of the rhabdom. Second, the lateral filtering pigment
could change the sensitivity of the photoreceptors, but the signals for
different ommatidia are not compared neurally. Neural lateral connections that
are specific for different ommatidial types have so far only been studied in
the lamina of Papilio (Takemura
et al., 2005). Signals from R3–8 photoreceptors of
neighboring ommatidia may be pooled such that the pigment-induced spectral
information is equalized and thereby rendered useless. Another possibility is
that pigment-induced spectral information is preserved in another behavioral
context, such as in the discrimination of oviposition substrates or mate
detection. A color vision channel using this information would have to compare
signals from both types of ommatidia. While there is no direct proof of such a
neural process at present, the possibility is viable.
Lateral filtering pigments have long been described as spectral filters
(Ribi, 1978). In
Papilio and Pieris, filtering pigments come in different
colors and spatial distributions (Arikawa,
2003; Wakakuwa et al.,
2004), and in Papilio, are coordinately expressed with
particular opsins. The effect of these pigments in Pieris as spectral
filters has been demonstrated by electrophysiology
(Wakakuwa et al., 2004). In
Papilio, red receptors are used for color vision in both the context
of oviposition and food choice (Kelber,
1999; Kelber and Pfaff,
1999). It is difficult to test, however, the behavioral effects of
the filtering pigments in Papilio independently from that of the
co-ordinately expressed opsin. Behavioral and electrophysiological studies on
other butterfly species known to have lateral filtering pigments in the retina
(e.g. Wakakuwa et al., 2004;
Sauman et al., 2005) are
needed to confirm the difference between our result in this study and our
previous findings in Heliconius erato
(Zaccardi et al., 2006).
Our results also show that the visual pigments encoded by the blue opsin
duplicate gene, BRh2, and the LW opsin gene, LWRh, function
together for green color discrimination in P. icarus. Elucidating the
function of the B2 pigment is of interest because this is a unique case of a
visual pigment in insects that evolved from a blue opsin gene and is
red-shifted by 63 nm compared to its 437 nm paralogue
(Fig. 1). Because lycaenids
only have one LW opsin transcript that may also be somewhat red-shifted in
peak absorbance (568 nm as in L. rubidus) compared to their estimated
540±10 nm (mean ± s.e.m.) ancestral pigment
(Frentiu et al., 2007), we
hypothesize that the B2 receptor, after gene duplication, co-evolved with the
LW-absorbing visual pigment to shift the limit of color discrimination
capability of the animal towards longer wavelengths. Color discrimination in
this range of the spectrum may not only facilitate flower discrimination, but
it may also help detect suitable oviposition substrates (e.g.
Kelber, 1999;
Kelber, 2001).
It is of interest to note that the only other butterfly we are aware of
whose eye contains a visual pigment with a peak absorbance similar to B2 is
the riodinid Apodemia mormo
(Bernard et al., 1988). Unlike
the 500 nm (B2) pigment of Lycaena, however, the 505 nm pigment of
A. mormo is produced by a duplicate LW opsin, LWRh1
(Frentiu et al., 2007).
Intriguingly, the LW opsins of L. rubidus and P. icarus are
homologous to the LWRh2 opsin of A. mormo, which encodes a
600 nm pigment (Bernard 1979;
Frentiu et al., 2007), but a
homolog of the A. mormo 505 nm (LWRh1) pigment in lycaenids
is missing. The convergent evolution of two visual pigments with
max in the 500 nm range implies strong selection for this
trait.
It is intriguing that butterflies from different lineages, such as the
papilionids and lycaenids, follow a different manner of modifying their color
vision system to achieve good color discrimination in the green range.
Papilionids use duplicated LW opsins, one of which is a red receptor, to have
a better green color discrimination for the purpose of oviposition
(Kelber, 1999) while the
lycaenids have a duplicated blue opsin, that is maximally sensitive in the
blue-green (at least in L. rubidus), to be able to discriminate green
colors. Hence, we conclude that natural selection has hit upon alternative
strategies for producing color vision in the green part of the visible
spectrum in butterflies.
|
Acknowledgments |
|---|
|
Footnotes |
|---|
|
References |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Arikawa, K. (2003). Spectral organization of the eye of a butterfly, Papilio. J. Comp. Physiol. A 189,791 -800.[CrossRef][Medline]
Arikawa, K., Scholten, D. G. W., Kinoshita, M. and Stavenga, D. G. (1999). Tuning of photoreceptor spectral sensitivities by red and yellow pigments in the eye of the butterfly Papilio. Vision Res. 39,1 -8.[CrossRef][Medline]
Arikawa, K., Wakakuwa, M., Qiu, X., Kurasawa, M. and Stavenga,
D. G. (2005). Sexual dimorphism of short-wavelength
photoreceptors in the small white butterfly, Pieris rapae crucivora.J. Neurosci. 25,5935
-5942.
Bernard, G. D. (1979). Red-absorbing visual
pigments of butterflies. Science
203,1125
-1127.
Bernard, G. D. and Miller, W. H. (1970). What does antenna engineering have to do with insect eyes? IEEE Stud. J. 8,2 -8.
Bernard, G. D. and Remington, C. L. (1991).
Color vision in Lycaena butterflies: spectral tuning of receptor
arrays in relation to behavioral ecology. Proc. Natl. Acad. Sci.
USA 88,2783
-2787.
Bernard, G. D., Douglass, J. K. and Goldsmith, T. H. (1988). Far-red sensitive visual pigment of a metalmark butterfly. Invest. Ophthalmol. 29, 350.
Briscoe, A. D. (1998). Molecular diversity of visual pigments in the butterfly Papilio glaucus.Naturwissenschaften 85,33 -35.[CrossRef][Medline]
Briscoe, A. D. and Bernard, G. D. (2005).
Eye-shine and spectral tuning of long wavelength-sensitive rhodopsins: no
evidence for red-sensitive photoreceptors among five Nymphalini butterfly
species. J. Exp. Biol.
208,687
-696.
Briscoe, A. D. and Chittka, L. (2001). The evolution of color vision in insects. Annu. Rev. Entomol. 46,471 -510.[CrossRef][Medline]
Briscoe, A. D., Bernard, G. D., Szeto, A. S., Nagy, L. M. and White, R. H. (2003). Not all butterfly eyes are created equal: rhodopsin absorption spectra, molecular identification and localization of ultraviolet-, blue-, and green-sensitive rhodopsin-encoding mRNAs in the retina of Vanessa cardui. J. Comp. Neurol. 458,334 -349.[CrossRef][Medline]
Burghardt, F. and Fiedler, K. (1996). The influence of diet on growth and secretion behaviour of myrmecophilous Polyommatus icarus caterpillars (Lepidoptera: Lycaenidae). Ecol. Entomol. 21,1 -8.
Burghardt, F., Knüttel, H., Becker, M. and Fiedler, K. (2000). Flavonoid wing pigments increase attractiveness of female common blue (Polyommatus icarus) butterflies to mate-searching males. Naturwissenschaften 87,304 -307.[CrossRef][Medline]
Frentiu, F. D., Bernard, G. D., Sison-Mangus, M. P., Brower, A.
V. Z. and Briscoe, A. D. (2007). Gene duplication is an
evolutionary mechanism for expanding the spectral diversity in the
long-wavelength photopigments of butterflies. Mol. Biol.
Evol. 24,2016
-2028.
Kelber, A. (1999). Ovipositing butterflies use a red receptor to see green. J. Exp. Biol. 202,2619 -2630.[Abstract]
Kelber, A. (2001). Receptor based models for spontaneous colour choices in flies and butterflies. Entomol. Exp. Appl. 99,231 -244.[CrossRef]
Kelber, A. (2006). Invertebrate colour vision. In Invertebrate Vision (ed. E. J. Warrant and D.-E. Nilsson), pp. 250-290. Cambridge: Cambridge University Press.
Kelber, A. and Pfaff, M. (1999). True colour vision in the orchard butterfly, Papilio aegeus.Naturwissenschaften 86,221 -224.[CrossRef]
Kelber, A., Vorobyev, M. and Osorio, D. (2003). Animal colour vision-behavioural tests and physiological concepts. Biol. Rev. 78,81 -118.[Medline]
Kinoshita, M., Shimada, N. and Arikawa, K. (1999). Colour vision of the foraging swallowtail butterfly Papilio xuthus. J. Exp. Biol. 202,95 -102.[Abstract]
Kitamoto, J., Sakamoto, K., Ozaki, K., Mishina, Y. and Arikawa, K. (1998). Two visual pigments in a single photoreceptor cell: identification and histological localization of three mRNAs encoding visual pigment opsins in the retina of the butterfly Papilio xuthus.J. Exp. Biol. 201,1255 -1261.[Abstract]
Knüttel, H. and Fiedler, K. (2001). Host-plant-derived variation in ultraviolet wing patterns influences mate selection by male butterflies. J. Exp. Biol. 204,2447 -2459.[Medline]
Kronfrost, M. R., Young, L. G., Kapan, D. D., McNeely, C.,
O'Neill, R. J. and Gilbert, L. E. (2006). Linkage of
butterfly mate preference and wing color preference cue at the genomic
location of wingless. Proc. Natl. Acad. Sci. USA
103,6575
-6580.
Kumar, S., Tamura, K. and Nei, M. (2004).
MEGA3: an integrated software for molecular evolutionary genetics analysis and
sequence alignment. Brief Bioinformatics
5, 150-163.
Lundgren, L. (1977). Role of intra and interspecific male-male interactions in Polyommatus icarus Rott and some other species of blues (Lycaenidae). J. Res. Lepid. 16,249 -264.
Miller, W. H. (1979). Ocular optical filtering. In Handbook of Sensory Physiology. Vol.VII /6A (ed. H. Autrum), pp.69 -143. Berlin, Heidelberg, New York: Springer-Verlag.
Miller, W. H. and Bernard, G. D. (1970). Butterfly glow. J. Ultrastruct. Res. 24,286 -294.[CrossRef]
Nilsson, D.-E., Land, M. F. and Howard, J. (1988). Optics of the butterfly eye. J. Comp. Physiol. A 162,341 -366.[CrossRef]
Ômura, H. and Honda, K. (2005). Priority of color over scent during flower visitation by adult Vanessa indica butterflies. Oecologia 142,588 -596.[CrossRef][Medline]
Palacios, A. G., Bernard, G. D. and Goldsmith, T. H. (1996). Sensitivity of cones from a cyprinid fish (Danio aequipinnatus) to ultraviolet and visible light. Vis. Neurosci. 13,411 -421.[Medline]
Ribi, W. A. (1978). Ultrastucture and migration of screening pigments in retina of Pieris rapae L (Lepidoptera, Pieridae). Cell Tissue Res. 191, 57-73.[Medline]
Ribi, W. A. (1979). Coloured screening pigments cause red eye glow hue in pierid butterflies. J. Comp. Physiol. A 132,1 -9.[CrossRef]
Rohlf, F. J. and Sokal, R. R. (1995). Statistical Tables. New York: Freeman and Co.
Sauman, I., Briscoe, A. D., Zhu, H., Shi, D. D., Froy, O., Stalleicken, J., Yuan, Q., Casselman, A. and Reppert, S. M. (2005). Connecting the navigational clock to sun compass input in monarch butterfly brain. Neuron 46,457 -467.[CrossRef][Medline]
Seki, T. and Vogt, K. (1998). Evolutionary aspects of the diversity of visual pigment chromophores in the Class Insecta. Comp. Biochem. Physiol. 119B,53 -64.[CrossRef]
Sison-Mangus, M. P., Bernard, G. D., Lampel, J. and Briscoe, A.
D. (2006). Beauty in the eye of the beholder: the two blue
opsins of lycaenid butterflies and the opsin gene-driven evolution of sexually
dimorphic eyes. J. Exp. Biol.
209,3079
-3090.
Smith, W. C. and Goldsmith, T. H. (1990). Phyletic aspects of the distribution of 3-hydroxyretinal in the Class Insecta. J. Mol. Evol. 30,72 -84.[CrossRef][Medline]
Sokal, R. R. and Rohlf, F. J. (1995). Biometry. New York: Freeman and Co.
Stavenga, D. G. (2002). Reflections on
colourful ommatidia of butterfly eyes. J. Exp. Biol.
205,1077
-1085.
Struwe, G. (1970). Spectral sensitivity of the compound eye in butterflies (Heliconius). J. Comp. Physiol. 79,191 -196.[CrossRef]
Swihart, S. L. (1972). The neural basis of color vision in the butterfly, Heliconius erato. J. Insect Physiol. 18,1015 -1025.[CrossRef]
Swihart, S. L. and Gordon, W. C. (1971). Red receptors in butterflies. Nature 231,126 -127.[CrossRef][Medline]
Takemura, S.-Y., Kinoshita, M. and Arikawa, K. (2005). Photoreceptor projection reveals heterogeneity of lamina cartridges in the visual system of the Japanese yellow swallowtail butterfly, Papilio xuthus. J. Comp. Neurol. 483,341 -350.[CrossRef][Medline]
Takemura, S.-Y., Stavenga, D. G. and Arikawa, K.
(2007). Absence of eye shine and tapetum in the heterogeneous eye
of Anthocharis butterflies (Pieridae). J. Exp.
Biol. 210,3075
-3081.
Wakakuwa, M., Stavenga, D. G., Kurasawa, M. and Arikawa, K.
(2004). A unique visual pigment expressed in green, red and
deep-red receptors in the eye of the small white butterfly, Pieris rapae
crucivora. J. Exp. Biol.
207,2803
-2810.
Warrant, E., Kelber, A. and Frederiksen, R. (2007). Ommatidial adaptations for spatial, spectral, and polarization vision in arthropods. In Invertebrate Neurobiology (ed. G. North and R. J. Greenspan), pp.123 -154. Cold Spring Harbor, NY: CSHL Press.
Weiss, M. R. and Papaj, D. (2003). Colour learning in two behavioral contexts: how much can a butterfly keep in mind? Anim. Behav. 65,425 -434.[CrossRef]
Zaccardi, G., Kelber, A., Sison-Mangus, M. P. and Briscoe, A.
D. (2006). Color discrimination in the red range with only
one long-wavelength sensitive opsin. J. Exp. Biol.
209,1944
-1955.
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
This article has been cited by other articles:
|
|
 |
|
  A. D. Briscoe Reconstructing the ancestral butterfly eye: focus on the opsins J. Exp. Biol., June 1, 2008; 211(11): 1805 - 1813. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
