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Research
Cite this article: Kitamura T, Imafuku M.
2015 Behavioural mimicry in flight path
of Batesian intraspecific polymorphic butterfly
Papilio polytes. Proc. R. Soc. B 282: 20150483.
http://dx.doi.org/10.1098/rspb.2015.0483
Received: 2 March 2015
Accepted: 7 May 2015
Subject Areas:
behaviour, biomechanics
Keywords:
Batesian mimic butterfly, behavioural mimicry,
flight behaviour, flight path, intraspecific
polymorphism, Papilio polytes
Author for correspondence:
Tasuku Kitamura
e-mail: [email protected]
Behavioural mimicry in flight path
of Batesian intraspecific polymorphic
butterfly Papilio polytes
Tasuku Kitamura1,2 and Michio Imafuku1
1
2
Department of Zoology, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto 606-8502, Japan
Graduate School of Bioresources, Mie University, 1577 Kurimamachiya-cho, Tsu, Mie 514-8507, Japan
Batesian mimics that show similar coloration to unpalatable models gain a
fitness advantage of reduced predation. Beyond physical similarity, mimics
often exhibit behaviour similar to their models, further enhancing their protection against predation by mimicking not only the model’s physical appearance
but also activity. In butterflies, there is a strong correlation between palatability
and flight velocity, but there is only weak correlation between palatability and
flight path. Little is known about how Batesian mimics fly. Here, we explored
the flight behaviour of four butterfly species/morphs: unpalatable model
Pachliopta aristolochiae, mimetic and non-mimetic females of female-limited
mimic Papilio polytes, and palatable control Papilio xuthus. We demonstrated
that the directional change (DC) generated by wingbeats and the standard
deviation of directional change (SDDC) of mimetic females and their models
were smaller than those of non-mimetic females and palatable controls.
Furthermore, we found no significant difference in flight velocity among all
species/morphs. By showing that DC and SDDC of mimetic females resemble
those of models, we provide the first evidence for the existence of behavioural
mimicry in flight path by a Batesian mimic butterfly.
1. Introduction
Mimicry, in which a colour pattern of palatable individuals closely resembles that of
unpalatable individuals of other species phylogenetically separated, has long
attracted evolutionary biologists, mainly regarding two aspects. One aspect is its biological significance addressing whether the resemblance is actually in effect or not
[1–4], and the other is the genetic basis that supports the resemblance. In the latter
aspect, a ‘supergene’, a tightly linked cluster of loci on a chromosome, was hypothesized in butterflies [5,6], and the molecular architecture of the supergene has
progressively been disclosed for Müllerian [7–11] and Batesian mimicry [12–14].
Attention to mimicry was first paid on colour patterns which are readily perceived, and then directed to similarity of movements between mimics and their
models and to wing and body morphologies that support behavioural similarity.
Movement is important for prey to avoid attacks by predators. Some animals
move rapidly to escape from predators, whereas others remain motionless to
avoid detection by predators [15]. It is thought that sluggish movement exhibited by many unpalatable animals is also a strategy for avoiding attacks [15–17].
Sherratt et al. [18] showed in experiments with human predators attacking
computer-simulated prey that unprofitable prey evolved slower movement behaviour than profitable prey if they were readily recognized as unprofitable and
survived predatory attacks. This is presumably because if unprofitable prey are
slow-moving, they can be more readily recognized as being unprofitable.
In butterflies, it has been thought that there are correlations between palatability and flight-related characters. Palatable species fly fast and erratically, a flight
pattern that would make it difficult for predators to predict the flight path, reducing the frequency of successful attacks by predators. By contrast, unpalatable
species tend to fly slowly and regularly. This flight pattern would make it easy
for predators to recognize the prey as being unpalatable. Srygley and colleagues
demonstrated in neotropical butterflies that unpalatable species have relatively
& 2015 The Author(s) Published by the Royal Society. All rights reserved.
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(a) Subjects
We used three species of Papilioninae, Pap. polytes (Papilionini),
Pach. aristolochiae (Troidini) and Papilio xuthus (Papilionini). Papilio
polytes is a palatable swallowtail butterfly commonly found
throughout the Oriental tropics. Males of this butterfly are monomorphic, whereas females are polymorphic. Pachliopta aristolochiae
is an unpalatable toxic butterfly found throughout the Oriental
tropics. It has warning red spots on its hindwings. Poisonous substances are resorbed from the food plant by the larva and stored by
the organism during pupation and metamorphosis [25]. Papilio
xuthus, which is not known to be either an unpalatable species
or a mimic, is a swallowtail butterfly found throughout the temperate region of East Asia. Papilio polytes and Pap. xuthus use the
Rutaceae group as host plants, whereas Pach. aristolochiae uses
the Aristolochiaceae group.
Adults of Pap. polytes and Pach. aristolochiae were collected
on Ishigaki Island, Okinawa, Japan (248260 N; 124880 E) and
were brought to Minoh Park Insectary, Osaka, Japan (348500 N;
1358280 E). Adults of Pap. xuthus were brought to the Insectary
from Osaka Prefecture. Eggs of these butterflies were collected in
the Insectary and were raised in a temperature-controlled room
at 238C. Butterflies that emerged from pupae were released
into the insectary. We performed behavioural observations on
butterflies kept in the insectary for at least one generation.
(b) Wing stroke records
During July 2007 to April 2008 and May 2009 (from 10.00 to
16.00), we recorded the flight behaviour of butterflies with two
2
L
1
7
a
2 a
2
c
b
FV1–2
3
FV2–3
6
a3
a6
5 a5
4
FV5–6 FV6–7
(b)
2
a2
3
1
8
9 a
9
FV1–2 FV2–3
FV8–9
10
FV9–10
Figure 1. A scheme showing (a) one-wingbeat and (b) nine-wingbeat analysis of flight path. Solid circles indicate thoracic position of a butterfly. Top
diagrams show lateral views of a butterfly. We used 6.60 + 0.96
(mean + s.d.) images in one-wingbeat analysis. Numbers indicate coordinate
of a butterfly. a, b and c indicate distances between coordinates 1 –2, 2 – 3
and 1 – 3, respectively. a2 indicates external angle of coordinate 2 on triangle
formed by coordinate 1, 2 and 3. Bottom figures show top views of a
wing-closed posture of a butterfly.
fixed digital video cameras while they were flying freely in a
large cage (13 14 m, 10 m high) in the insectary. We constructed a rectangular framework (1.5 2 m, 3.5 m high) with
pipes in the cage. One video camera (Sony DCR-SR100, Japan,
aspect ratio 4 : 3) was placed at the centre of the ceiling of the
framework with the lens side down to obtain a vertical view.
Another video camera (Canon DM-FV M100, Japan, aspect
ratio 4 : 3) mounted on a tripod was placed on the side of the
framework at a position 1.5 m high to obtain a horizontal view.
When a butterfly had passed through the framework, it was captured and the ambient temperature was immediately measured
(range: 19.6 – 33.68C). For synchronization of respective images
from the two video cameras, the shrinking motion of a spring
was recorded after every recording of butterflies. Flying behaviour of butterflies in the framework was analysed. Butterflies
were used only once.
(c) Analysis of images
We traced the centre of the thoracic position of butterflies on
images from the two video cameras (60 images per second), and
the data obtained were transformed into three-dimensional coordinates, using eight reference points on the framework, by an image
analysis software (FRAME-DIAS II, DKH, Japan). The change in position over time was low-pass filtered at 20 Hz. Gliding flight was
excluded from the analyses. We conducted two types of analyses:
one-wingbeat analysis and nine-wingbeat analysis.
One-wingbeat analysis was used to examine the up–down
movement generated by wingbeats. For this analysis, we used
every frame within one wingbeat (from a wing-closed posture to
the next wing-closed posture) when butterflies flew linearly in a
horizontal plane (figure 1a). Horizontal flight was defined as
flight in which the angle between the horizontal plane (line L)
and a straight line connecting the starting point (point 1) with
the ending point (e.g. point 7 in figure 1a) was less than or equal
to 58. Flight in a vertical plane was defined as change in heading
direction of a butterfly frame to frame of less than or equal to 58
on average. We calculated four variables from the coordinates:
Proc. R. Soc. B 282: 20150483
2. Material and methods
(a)
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smaller thoraces and longer bodies, and they fly more slowly
[19–21]. By contrast, palatable species have relatively wider
thoraces and shorter bodies, and they have higher manoeuvrability and fly faster. However, the correlation between
palatability and irregularity of flight path was very weak
[19]. Flight path is still poorly investigated, and skepticism
remains over whether a difference in flight path exists between
palatable and unpalatable species.
Golding et al. [22] showed that a Batesian mimic dronefly
resembles a honeybee in its flight behaviour as well as in
appearance. In butterflies, Srygley [23] found that Batesian
mimics and their models perform wingbeats with slower
angular velocity compared with palatable species to enhance
the colour signal. Kitamura & Imafuku [24] demonstrated in a
female-limited Batesian mimic butterfly, Papilio polytes, that
mimetic females mimic their models in the minimum positional
angle of their wings. As far as we know, however, there are no
studies of flight path of Batesian mimic butterflies.
Papilio polytes is a female-limited Batesian mimic butterfly
(refer to [24] for a picture of the species and morphs being
investigated). Females of this butterfly show polymorphism
in coloration. Non-mimetic females (Pap. polytes form. cyrus)
have black wing and white spots on the hindwing, and they
resemble conspecific males. Mimetic females (form. polytes)
have black wing and white and red spots on the hindwing,
and resemble an unpalatable sympatric toxic butterfly,
Pachliopta aristolochiae [25], and thus are thought to be a Batesian mimic of this species [4,26,27]. The purpose of this study
was to determine whether behavioural mimicry in flight
path exists in Pap. polytes, on the assumption that the mimetic form shows a flight path similar to that of the model and
different from that of the non-mimetic form.
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(d) Statistical analysis
Correlation of all variables and ambient temperature was not
found among species/morphs for each of sexes ( p . 0.1136).
Three species were compared for males. We used Bartlett’s
test to test for homogeneity of variances. If we found no significant difference in the test ( p . 0.05), we conducted one-way
ANOVA (three-levels for the independent variable in the
ANOVA) and when we found a significant difference in oneway ANOVA ( p , 0.05), we conducted multiple comparisons
(Tukey’s honestly significant difference test). If we found a significant difference in Bartlett’s test ( p , 0.05), we conducted
Welch’s ANOVA and when we found a significant difference
in Welch’s ANOVA ( p , 0.05), we conducted multiple comparisons (Holm test). The significance level for experiment-wise error
rate was set at p ¼ 0.05. The females for two morphs within one
species and two additional species (four levels in the ANOVA)
were compared in the same manner as the males. All analysis
was conducted using R (v. 3.0.2).
3. Results
In one-wingbeat analysis, 60 butterflies were used in males
(Pap. xuthus n ¼ 20, Pach. aristolochiae n ¼ 13, Pap. polytes n ¼
27) and 66 butterflies in females (Pap. xuthus n ¼ 9, Pach.
aristolochiae n ¼ 13, non-mimetic form of Pap. polytes n ¼ 20,
mimetic form of Pap. polytes n ¼ 24). In nine-wingbeat analysis,
61 butterflies were used in males (Pap. xuthus n ¼ 20, Pach.
aristolochiae n ¼ 13, Pap. polytes n ¼ 28) and 75 butterflies in
(b)
(c)
Figure 2. Example of flight path of female butterflies in a vertical plane in onewingbeat analysis. Solid circles indicate vertical position of the thorax in successive frames. Butterflies fly from left to right. (a) Pap. polytes non-mimetic form,
(b) Pap. polytes Batesian mimetic form, (c) Pach. aristolochiae.
females (Pap. xuthus n ¼ 14, Pach. aristolochiae n ¼ 16, nonmimetic form of Pap. polytes n ¼ 20, mimetic form of Pap.
polytes n ¼ 25). An example from a typical tracing of a
non-mimetic and mimetic female, and the model, is shown in
figure 2.
In one-wingbeat analysis, statistically significant effects of
species/morph were found for DCone and SDDCone in both
sexes, but not for FVone or SDFVone (table 1). In nine-wingbeat analysis, we found statistically significant effects of
species/morph for SDFVnine in females and VI in males,
but not for FVnine or SDFVnine in males, nor for DCnine,
SDDCnine or VI in females (table 1).
In both sexes, DCone and SDDCone of palatable butterflies
were significantly larger than those of the unpalatable species
and mimetic females (figure 3e–h). In females, SDFVnine of
the non-mimetic form of Pap. polytes was significantly larger
than that of the mimetic form of Pap. polytes (figure 3l ). For
VI of males, we found statistically significant effects of
species/morph between palatable species and unpalatable
species in multiple comparisons (figure 3q).
In nine-wingbeat analysis, wingbeat frequency was
10.4 + 0.84 (mean + s.d., Pap. xuthus), 11.5 + 0.88 (Pach.
aristolochiae) and 10.4 + 0.92 (Pap. polytes) for males, and
10.8 + 1.20 (Pap. xuthus), 10.9 + 0.69 (Pach. aristolochiae),
11.1 + 1.00 (non-mimetic form of Pap. polytes) and 10.7 +
0.92 (mimetic form of Pap. polytes) for females. Significant
difference in wingbeat frequency was not found among
species/morphs for each of sexes. This result coincides with
that obtained previously [24].
4. Discussion
From one-wingbeat analysis, clear-cut results were obtained:
the flight path, but not the flight velocity, of the control (nontoxic) species was clearly different from that of the model
(toxic) species. Moreover, the flight paths of mimetic females
and non-mimetic females of a Batesian intraspecific polymorphic butterfly were different from each other, and that of
mimetic females was not significantly different from that
of their models. This is the first evidence that shows the
existence of behavioural mimicry in flight path.
As shown by the large DCone values, butterflies of the
control and non-mimetic groups performed flight characterized by large changes in heading direction. A large DC
with nonlinear path could be produced by a large angular
3
Proc. R. Soc. B 282: 20150483
where t indicates time spent from coordinate 1– 3 of a butterfly.
DCone and SDDCone were, respectively, the mean and the standard
deviation of all DCs within a wingbeat. Chai and Srygley [19] used
DC as the index value of irregularity, but in this study we used DC
as the index value of nonlinearity and SDDC as the index value
of irregularity.
Nine-wingbeat analysis was considered to examine the movement of a butterfly without wingbeat effects. For this analysis, we
used 10 successive frames (totalling about 1 s, roughly
corresponding to the time a butterfly stayed within the framework) that showed the butterfly with wings closed (figure 1b).
We separated the three-dimensional component into an xy-plane
component and a z-axis component. Four variables—flight velocity (FVnine), standard deviation of flight velocity (SDFVnine),
time variation of directional change (DCnine) and standard deviation of directional change (SDDCnine)—were calculated from the
xy-coordinates. Thus, we used the component of each vector in
the horizontal plane. FVnine and SDFVnine were, respectively, the
mean and the standard deviation of all FVs (FV1 – 2, FV2 – 3, . . . ,
FV9 – 10; figure 1b). DCnine and SDDCnine were, respectively, the
mean and the standard deviation of all DCs in the nine wingbeats.
The vertical interval (VI) was defined as the vertical distance
between the highest and lowest values of the z-coordinate in the
nine wingbeats.
All variables were defined as the mean value, respectively,
for each species/morph.
(a)
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flight velocity (FVone), standard deviation of flight velocity
(SDFVone), directional change (DCone) and standard deviation of
directional change (SDDCone). FVone was a mean value of velocities
calculated from two successive frames (FV1 – 2, FV2 – 3, . . . , FV6 – 7).
SDFVone was the standard deviation of all FVs within a wingbeat.
Directional change (DC) was defined as the time variation of difference of heading directions in two successive frames (an 2 an21).
DCa2 in figure 1a is given by
2
180
a þ b 2 c2
1
DCa2 ¼ 180 ,
arccos
t
p
2ab
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Table 1. The result of analysis (ANOVA) about nine parameters (FVone, SDFVone, DCone, SDDCone, FVnine, SDFVnine, DCnine, SDDCnine and VI).
4
p-value
FVone (m s21)
SDFVone
one-way
Welch’s
f2, 57 ¼ 0.328
f2, 34.256 ¼ 1.008
p ¼ 0.722
p ¼ 0.376
DCone (8 s21)
SDDCone
Welch’s
Welch’s
f2, 37.331 ¼ 19.539
f2, 37.401 ¼ 13.813
p , 0.0001
p , 0.0001
FVone (m s21)
SDFVone
one-way
Welch’s
f3, 62 ¼ 0.667
f3, 24.152 ¼ 1.023
p ¼ 0.576
p ¼ 0.400
DCone (8 s21)
Welch’s
f3, 26.202 ¼ 24.507
p , 0.0001
SDDCone
Welch’s
f3, 25.483 ¼ 19.085
p , 0.0001
FVnine (m s21)
SDFVnine
Welch’s
one-way
f2, 38.274 ¼ 2.611
f2, 58 ¼ 0.866
p ¼ 0.087
p ¼ 0.426
DCnine (8 s21)
one-way
f2, 58 ¼ 2.321
p ¼ 0.107
SDDCnine
VI (m)
one-way
Welch’s
f2, 58 ¼ 2.494
f2, 37.138 ¼ 9.885
p ¼ 0.091
p , 0.001
FVnine (m s21)
SDFVnine
one-way
Welch’s
f3, 71 ¼ 0.921
f3, 33.032 ¼ 4.217
p ¼ 0.435
p ¼ 0.012
DCnine (8 s21)
SDDCnine
one-way
Welch’s
f3, 71 ¼ 1.044
f3, 34.778 ¼ 2.566
p ¼ 0.378
p ¼ 0.070
VI (m)
Welch’s
f3, 33.256 ¼ 2.096
p ¼ 0.119
one wingbeat
male
female
nine wingbeat
male
female
velocity of wing and large stroke amplitude—angular difference between the most closed (wmax) and opened (wmin:
minus values in many case) wing positions (see fig. 3.2 in
[28])—or produced by a pause at the top of the wing stroke
which causes the insect drop (flight pattern of many satyrids
[29,30]). However, we found no pause in our butterflies. In
another study of wing motion, we found that angular velocity of wing and wmax were not different among these
species/morphs, but wmin of the mimetic females and their
models was larger than that of the control and the nonmimetic groups [24]. Presumably, a large wmin of the former
group is one of the factors that cause small DCs, whereas a
small wmin of the control and non-mimetic groups is one of
the factors that cause large DCs. Further, the standard deviation of DC of the control and the non-mimetic groups was
larger than those of the model and the mimicry group. This
means that the former groups fly not only in a nonlinear
path but also in a linear path, thus in an irregular flight
path. By contrast, butterflies of the latter group continuously
fly in a regular flight pattern with a linear path.
It is thought that nonlinear and irregular flight is one of
the defence strategies of butterflies against aerial predation.
In one classical explanation, the flight pattern functions as a
warning signal indicating difficulty of capture and associated
prey unprofitability [31]. However, this hypothesis has never
been tested experimentally. Another explanation is that the
flight pattern functions as a tactic for avoiding attack rather
than as a warning signal before birds attack them. Because
birds attack taking the motion of prey into consideration, a
flight pattern of butterflies that makes the flight path hard
to predict and makes it hard for the bird to catch them [15]
will be useful for survival of butterflies. On the other hand,
it is thought that linear and regular flight, characteristic
of unpalatable butterflies and their mimics, increases the
conspicuous effect of their warning coloration to enhance
learning and avoid confusion with palatable butterflies,
and decreases the chance of mistaken attacks by potential
predators [19,32– 34].
Additionally, Kassarov [35] considered the relationship
between flight pattern of butterflies and predation by birds
as follows. It is thought that aerial hawking birds are the
main predators of flying butterflies. If birds find a butterfly at
a distance, they must make a decision to attack or not within
seconds before it flies away. At a distance, birds can differentiate the characteristic flight pattern but not the colour
pattern. Thus, characteristic flight pattern becomes the factor
that renders the prey ‘conspicuous’ and becomes a useful cue
that signals profitability or unprofitability. Actually, at a
distance, we can easily differentiate whether a butterfly is palatable or unpalatable and whether it belongs to the mimicry
group by the flight pattern rather than the colour pattern in
our species/morph (T.K. 2007, personal observations). When
a chromatically mimetic butterfly mimics the flight pattern of
its model well, it is difficult to differentiate at a distance. On
the other hand, when close to the butterfly, we can first differentiate butterflies as mimics or their models by their colour
pattern and morphological characteristics. Thus, at a distance
from predators, unpalatable and mimic species may gain protection against aerial predation by their conspicuous flight
pattern rather than by their coloration. Flight pattern may
thus function as a primary defence, like aposematic coloration,
for unpalatable species [15]. Further, Kassarov [35] argued that
birds are not the primary selective force leading to evolution of
mimicry and aposematism in butterflies, because birds are able
Proc. R. Soc. B 282: 20150483
f-value
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ANOVA
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one-wingbeat analysis
(b)
male
nine-wingbeat analysis
(i)
female
FVnine (m s–1)
FVone (m s–1)
1.5
1.0
0.5
1.0
0.5
(d)
(k)
(l)
0.3
0.2
0.2
SDFVnine
0.3
0.1
Proc. R. Soc. B 282: 20150483
SDFVone
1.5
0
0
(c)
*
0.1
0
0
(f)
(e)
**
(m)
***
***
(n)
80
***
***
***
DCnine (° s–1)
600
DCone (° s–1)
5
female
2.0
2.0
400
200
0
60
40
20
0
(h)
(g)
400
*
(o)
**
***
***
***
(p)
60
***
SDDCnine
SDDCone
( j)
male
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(a)
300
200
40
20
100
0
0
20
13
27
9
13
20
24
(r)
(q)
0.4
*
*
0.3
VI (m)
Pap. xuthus
Pach. aristolochiae
Pap. polytes
non-mimetic form
Pap. polytes
mimetic form
0.2
0.1
0
20
13
28
14
16
20
25
Figure 3. Comparisons of (a,b,i,j ) FV, (c,d,k,l ) SDFV, (e,f,m,n) DC, (g,h,o,p) SDDC and (q,r) VI among butterfly species/morphs during (a –h) one wingbeat and (i – r)
nine wingbeats. Papilio xuthus ( palatable control), Pap. polytes (males: palatable non-mimetic form; females: non-mimetic form, Batesian mimetic
form), Pach. aristolochiae (unpalatable model). Bars show standard error. Numbers at the bottom are the sample size of butterfly species/morphs, respectively.
*p , 0.05, **p , 0.01, ***p , 0.001.
to recognize the profitability of prey by their flight pattern not
their colour pattern. However, birds attack not only flying butterflies but also butterflies landing on plants, especially in the
early morning (N. Osaki & M. Ohata 2004, personal observation). They come into action earlier than butterflies, which
enables them to approach butterflies closely with time
enough to differentiate them by the colour pattern. It may be
that aposematic coloration evolves for protection against predation in the early morning, whereas a characteristic flight
pattern evolves for protection against predation in the daytime.
In the nine-wingbeat analysis, which explored horizontal movement, we found no statistically significant effects.
Insectivorous birds tend to attack from a position level with
the prey, and thus vertical movements of the potential prey
would be easily recognized by the attacker.
It is well known that palatable butterflies generally fly fast,
whereas unpalatable species fly slowly [19,32–36]. However,
we could not confirm this for our species, as shown by the
lack of a significant difference in FVone or FVnine among these
species/morph. As energetic cost of fast and irregular flight
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Data accessibility. The database for all data in this article is publicly
available at Dryad http://dx.doi.org/10.5061/dryad.60bd8.
Authors’ contributions. T.K. and M.I. conceived of and designed the study.
T.K. carried out the data collection and data analysis. T.K. wrote the
manuscript and M.I. improved it. Both authors gave final approval
for publication.
Competing interests. We declare we have no competing interests.
Funding. This study was supported in part by Grants for Global COE
Program for Biodiversity and Evolution (A06) to Kyoto University.
Acknowledgements. We thank the staff of Minoh Park Museum of Insects
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6
rspb.royalsocietypublishing.org
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In the one-wingbeat analysis, which explored the effect of
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difference between the two morphs of the Batesian mimetic
species. As flight patterns are known to be related to wing
and body morphologies [19,38,39], the different flight paths
found in our mimetic species may be caused by different
morphologies of wing and body. This is an interesting possibility to be addressed in a future study. A possibility that the
supergene responsible for colour patterns is associated with
wing shape variation is suggested [40]. The results obtained
for intraspecific variation in flight behaviour in our species
will contribute to studies of supergenes.
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