Blackwell Publishing LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066© 2007 The Linnean Society of London? 2007
904
573581
Original Article
DEVELOPMENTAL VARIABILITY IN GENITALIA
H. TATSUTA
ET AL.

Biological Journal of the Linnean Society, 2007, 90, 573–581. With 1 figure

Distinctive developmental variability of genital parts inthe sexually dimorphic beetle, Prosopocoilus inclinatus(Coleoptera: Lucanidae)
HARUKI TATSUTA1*, KATSUFUMI FUJIMOTO2, KOJI MIZOTA3, KLAUS REINHARDT4and SHIN-ICHI AKIMOTO2
1

Center for Biodiversity and Conservation, School of Biology, The University of Leeds, Leeds LS2 9JT, UK
Department of Ecology and Systematics, Graduate School of Agriculture, Hokkaido University, Sapporo
060-8589, Japan
3
Environmental Education Center, Miyagi University of Education, Sendai 980-0845, Japan
4
Department of Animal and Plant Sciences, The University of Sheffield, Sheffield S10 2TN, UK
2

Received 18 August 2005; accepted for publication 20 June 2006

Recent comparative studies have revealed that the rapid diversity of genitalia is closely related to sexual selection
and that genital development interacts with the development of different body parts. Hypotheses about developmental stability due to selection to genital parts were tested by estimating allometric relations in a sexually dimorphic stag beetle Prosopocoilus inclinatus. All genital parts of males scaled to body size with a slope of less than 1 andall but the median lobe (male intromittent organ) showed smaller variability than other body parts. This supportedthe ‘one-size-fits-all’ hypothesis, which suggests broad copulation opportunity by males of any size with females
within a population. Nevertheless, we found large variation among different genital parts in coefficients of variationand in values of the switch point where the allometric relations varied significantly. These results strongly support
the view that developmental trajectories of genital traits are not necessarily integrated. Among the genitalic traits,
male intromittent organ and female genitalia exhibited large variability, suggesting a high responsiveness to theselective regimes and physical interaction during copulation. This may account for rapid diversification of genitalmorphology, even in closely-related populations in beetle species. © 2007 The Linnean Society of London, Biological
Journal of the Linnean Society, 2007, 90, 573–581.

ADDITIONAL KEYWORDS: allometry – genitalia – one-size-fits-all hypothesis – sexual selection.

INTRODUCTION
Most recent studies on genital variation agree thatsexual selection processes such as female choice andmale–female interaction, rather than traditional ‘lockand-key’ or pleiotropy mechanisms, play an importantrole in the divergence of genital shape and functions(for a review, see Hosken & Stockley, 2004). The best
way to unravel the pathway of genital evolution will be
to measure selective pressures acting directly on the*Corresponding author. Current address: Laboratory of Ecological Risk Assessment, National Institute for Environmental
Studies, Tsukuba, Ibaraki 305-8506, Japan.
E-mail: htatsuta@nies.go.jp

genitalia. However, this approach is restricted to very
few species because of the difficulty in rearing large
amounts of animals. Instead, comparative morphological studies on genital features have been applied toindirectly infer the relationship between genital characteristics and selective regimes. For example, comparison of variation in genital features has revealed
that genitalia of males were more diverged within apolyandrous clade than those within a monoandrous
clade, suggesting that selective opportunity differs
between the two clades (Arnqvist, 1998).
A further indirect tool to disentangle hypotheses on
the evolution of genital structures is to study theallometry of genitalia. Two existing hypotheses basedon sexual selection (i.e. the good genes hypothesis and© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90, 573–581

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H. TATSUTA ET AL.

the weapon hypothesis) were tested by Eberhard et al.
(1998) using 20 species of insects and spiders. They
found that the allometric slopes of male genitalia
tended to be lower than the slopes of nongenital parts.
Consequently, an alternative hypothesis was proposed, namely the one-size-fits-all hypothesis. Thishypothesis predicts that females perceive tactile signals from the male genitalia and bias their fertilization decision accordingly. Selection therefore tends todecouple genitalia from the development of other general body parts (Eberhard et al., 1998).
Accordingly, stabilizing selection results in a similar
size of male genitalia regardless of the body size ofmales. As a result, low variation should be expectedacross males, implying that stabilizing selection itself
cannot explain why genital parts have acquired complicated shapes. Recent evolutionary studies on sexual
selection have provided an insight into this puzzle:
some genitalic traits may evolve independently fromone another (i.e. mosaic evolution) by way of male andfemale interactions (Cordoba-Aguilar, 2002; Cordero
Rivera et al., 2004; Hosken, Minder & Ward, 2005).
Moreover, although allometric coefficient of the genitalia as a whole is constant and lower than 1 in manycases (Eberhard et al., 1998; Tatsuta, Mizota & Akimoto, 2001; Bernstein & Bernstein, 2002; Mutanen &Kaitala, 2006), a positive allometry is sometimes
found in a part of genitalia, presumably due to postcopulatory sexual selection (Lupold, Mcelligott &Hosken, 2004; Hosken, Minder & Ward, 2005). These
facts lead to a contradiction in terms of developmental
stability and rapid diversification of genital structures. Comparative studies on phenotypic variation
would contribute to distinguishing these conjectures.
In the present study, comparison of phenotypic variability is attempted using the external morphology ofmale and female body parts of a lucanid beetle, Prosopocoilus inclinatus. In this species, male genitalia
consist of four fundamental parts: sternite IX andtergite IX, which constitute the abdominal plate, andthe aedeagus and the median lobe (penis), which show
a complex structure and are directly related to the copulatory process (Fig. 1). Female genitalia are relatively simple and consist of bursa copulatrix andspermatheca (Fig. 1). Males of the P. inclinatus species group often show dimorphism in mandible size
(Tatsuta, Mizota & Akimoto, 2004). Because such adimorphism can result in different behavioural tactics(Gage, Stockley & Parker, 1995; Shiokawa & Iwahashi, 2000), the alternative behaviour may exert different selective pressures on different body parts. The
developmental threshold at which allometric relations
switch can be analysed from allometric equations(Kotiaho & Tomkins, 2001). Comparison of the inflection points on the allometric curve between different
body parts will provide valuable insights that allow

assessment of the selective regimes and developmental constraints in a particular character set (Knell,
Pomfret & Tomkins, 2004). If traits are under selection
and tend to be subject to physiological constraint, thedevelopmental patterns would be similar with eachother. By contrast, if sexual selection (i.e. antagonistic
sexual selection; Arnqvist & Rowe, 2002) drives genitalia evolution, not only the inflection points on the
allometric curve differ across genitalic parts, but also
the disparity pattern around the character mean
would differ. Finally, comparing how the respective
variability of male and female genital parts matches
may also allow functional considerations (Hosken &Stockley, 2004; Mendez & Cordoba-Aguilar, 2004).

MATERIAL AND METHODS
MATERIALS AND MEASUREMENTS OF BODY PARTS
A total of 133 males and 142 females of P. inclinatusfrom a locality in Hidaka region, Hokkaido, northern
Japan was used for the analysis. All specimens werecollected by light trap in the summers of 1998 and1999 and killed immediately by ethyl acetate. Prior tothe measurement of each body part in males andfemales, five parts of each individual were separated
at the membranous joints: left and right mandible,
head, prothorax, fused segments of mesothorax-abdomen (SMA) (sensu Tatsuta, Mizota & Akimoto, 2001,
2004) (Fig. 1). Previous studies adopted morphometricanalysis to evaluate shapes of body parts, but thismethod is not always feasible, especially when bodyparts have a three-dimensional shape and tend to
induce substantial measurement errors due to small
size (cf. Bernstein & Bernstein, 2002). Thus, eachshape feature is represented as the weight of dry
mass, except female genitalia whose majority are constituted by membrane. Male genitalia were partitioned into the four fundamental parts: tergite IX,
sternite IX, the tegmen (comprising the parameres
and the basal piece), and the median lobe (Fig. 1). To
measure each part, after softening the whole genitalia
in hot water (95 °C) for a few minutes, each part was
separated and then dried at 65 °C for 24 h using a drying oven and weighed on a 1.0 × 10−5 g scale using afine electric balance (ISO9001, Sartorius). The dryweight of a character was shown to be governed by the
resource allocation during development (Tatsuta,
Mizota & Akimoto, 2001, 2004), and also reduces scaledifferences between body parts and overcomes difficulties in measuring dimensional complex body parts. We
eliminated damaged body parts from the subsequent
analysis.
For analysis of female genitalia, the sperm storage
organs, comprising the bursa copulatrix and the spermatheca (Fig. 1), were surgically removed from SMA
that had been softened in hot water (95 °C) before© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90, 573–581

575

DEVELOPMENTAL VARIABILITY IN GENITALIA

A
30
35

Frequency

30

Mandible-left

25
20
15
10

Frequency

Frequency

30

Mandible-right

20

20

Sternite IX

10

10

5
0
0.00

0.05

0.10

0.15

0
0.00

0.05

0.10

0
0.3

0.15

0.4

0.5

0.6

0.7

0.8

40

Frequency

35

Frequency

30
25

Head

20
15

30

Tergite IX

20

10

10
5
0
0.0

0.1

0.2

0
0.1

0.3

0.3

0.4

40

30

Frequency

Frequency

40

0.2

Prothorax

20

10

30

Tegmen

20

10
0
0.0

0.1

0.2

0.3
0
0.1

0.2

0.3

0.4

0.5

30

SMA

20

40

Frequency

Frequency

40

10

0
0.1 0.2 0.3 0.4 0.5 0.6 0.7

30Median lobe

20

10

0
0.0

0.1

0.2

0.3

0.0
0.4

B
30

0
0.0010.0020.0030.0040.0050.0060.007

Mandible-right

20

30
10

Frequency

Mandible-left
10

Frequency

Frequency

30

20

0
0.001 0.002 0.003 0.004 0.005 0.006

Frequency

40

30

20

10

0

Head

20

2

3

4

5

6

7

Spermatheca

1000.010.020.030.040.050.060.070.08

Frequency

50
40
30

Prothorax

20
10
0
0.00

0.05

0.10

0.15

0.20

40

Frequency

20

SMA

Frequency

30

30

20

10

10
0
3.0
0
0.1 0.2 0.3 0.4 0.5 0.6

3.5

4.0

4.5

5.0

5.5

0.7

Bursa copulatrix
Figure 1. Characters measured in males (A) and females (B) and their frequency distributions. The unit of measurement
is grams for nongenital parts in both sexes and genital parts in males and pixel for genital parts in females, respectively.
Landmarks for the length of female genitalia are indicated by the overlays.
© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90, 573–581

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H. TATSUTA ET AL.

surgery. Because the genital parts of females are madeof thin membrane and are not suitable for weighing,
we quantified the length of genital organs (Fig. 1). For
the length measurement of female genitalia, the whole
genitalia, comprising the bursa copulatrix and spermatheca, was mounted in Hoyer’s medium on a grassslide and then spread by careful placement of a coverslip so as not to deform original features. Images foreach part of genitalia were captured using a digital
camera (TK-1283, Victor) linked to a stereoscope(SZH-ILLD, Olympus, Japan). For all characters,
images were magnified to the exact same scale on acomputer screen to minimize measurement errors.
The measurement (where the scale unit was one pixel)of female genitalia was conducted using Scion Images
for Windows, version 4, (Scion Corp., 2000) as shownin Figure 1. To determine measurement precision ofeach part, measurements were repeated three times
in each character and the proportion of within-individual variance to the total variance was estimated usinga nested analysis of variance model. The proportion ofwithin-individual variance to the total variance wasconspicuously small (< 1% in nongenital characters inmales and females, < 4% in genital characters inmales, < 2% in genital characters in females). Because
this indicates that our measures of each character
were highly repeatable, the mean weights or lengthsof characters for each individual were used in the subsequent analysis.

VARIABILITY AND ALLOMETRY OF BODY PARTS
To assess the relationship between body parts, we first
calculated Pearson’s product-moment correlation coefficients between SMA and other body parts for eachsex. The trend of relative growth of a body part wasevaluated using the least-square fitting of the secondorder polynomial (Eberhard & Gutierrez, 1991). If thepartial regression coefficient of the quadratic term ( b2in Table 1) significantly deviated from zero, this partwas considered as having at least one inflection pointon allometric curve. We then searched for the switch
point of the allometric coefficient. In general, to determine the optimal switch point in the allometry of acharacter, a conditional regression model with leastsquare fashion (Eberhard & Gutierrez, 1991), in which
the dependent variable is regressed on the independent variable (i.e. body size), was adopted. However, as
noted by Kotiaho & Tomkins (2001), the accuracy ofthe model estimate is questionable when substantial
variance is primarily induced by environmental and/or genetic origin around the ‘realized’ switch point.
Therefore, we first estimated the switch point in thedimorphic parts (instead of finding the switch point inbody size first) by use of the modified least-squaremodel implemented by Kotiaho & Tomkins (2001):

ln X = a + b1 ◊ ln Y (1 - D) + b2(ln Y - ln YD ) D + e

in which ln X is log-transformed body size; ln Y is the
log-transformed response variable; ln YD is a logtransformed optimal switch point where the total
residual variance (1 − R2) of the above equation is thesmallest; D = 0 if Y < YD, D = 1 if Y > YD; α is a constant; β is the partial regression coefficient; and ε isthe error term. Based on the value of YD, the data werepartitioned into subsets and the range of SMA (shownas an untransformed scale; Table 1) of each subset wasestimated. We finally estimated regression slope of atrait on SMA. For comparison of regression coefficients estimated by different methods (for a detailed
discussion, see Green, 1999), ordinary least-square(OLS) regression and major axis (MA) regression wereused to estimate the allometry slope. Confidence intervals were also given to test the regression slope for aparticular allometric coefficient.
The coefficient of variation (CV) is entangled withthe change of allometric slope and the increase of variability (Eberhard et al., 1998: fig. 1A, B). To distinguish between the two, a modified estimator CV′,calculated as CV(Y) × (1 − r2)1/2 (Eberhard et al., 1998),
was estimated for each regression line when significant switching of allometric curve was found.
Correlation coefficients of residuals around the OLS
regression lines were also calculated between characters. All calculations were implemented using codedeveloped for statistical program R, version 1.90 (RDevelopment Core Team, 2004) and JMP for windows,
version 5.01 (SAS Institute Inc., 2002).

RESULTS
Figure 1 shows the frequency distribution of each bodypart. In males, most body parts showed a significant
departure from normality (Table 1). By contrast,
although all nongenital parts of the females conformed to normality, two genital parts were significantly deviated from normality (Table 1).
Basic statistics and allometric relations of each bodypart are summarized in Table 1. Because the correlation between the length of spermatheca (with a verylarge CV of 86.451%) and SMA was not significant(F = 2.93, P = 0.091), further analysis of allometry was
not carried out. In males and females, all body parts,
except the median lobe, had at least one inflection
point on the allometric curve. Two meaningful switch
points were found only in sternite IX.
Overall, although allometric coefficients calculated
from OLS regression tended to be smaller than thosefrom MA regression, the results were consistent irrespective of regression methods. In males, allometricslopes for the left and right mandible changed at avery similar body size (left = 0.253; right = 0.254):© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90, 573–581

© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90, 573–581

40.73333.20432.25531.98643.617280.27 ± 118.47
0.497 ± 0.101

0.242 ± 0.046

0.290 ± 0.054

0.175 ± 0.055

133

124

124

124

122

SMA‡
Genital parts
Sternite IX

Tergite IX

TegmenMedian lobe

0.088*

0.145**

0.175**

0.159**

0.113**

0.114**

0.118**

0.133**

0.137**

Dmax

0.447

0.651

0.700

0.794

0.961

0.962

0.907

0.907

r

0.084

0.114**

0.139**

0.160**

0.392**

0.510**

0.622**

0.626**b2> 0.266< 0.266> 0.201< 0.201> 0.187

0.172–0.187< 0.172> 0.270< 0.270> 0.252< 0.252> 0.254< 0.254> 0.253< 0.253

Range of SMA

0.045(0.028, 0.061)
0.033(0.029, 0.037)
0.343(0.328, 0.357)
0.191(0.178, 0.204)
0.084(0.054, 0.114)
0.131(0.118, 0.144)
0.189(0.175, 0.203)
0.262(0.154, 0.371)

1.400(1.361, 1.439)
0.418(0.374, 0.462)
1.428(1.388, 1.468)
0.402(0.359, 0.444)
0.435(0.396, 0.473)
1.224(1.203, 1.244)
0.845(0.828, 0.862)
0.374(0.342, 0.407)

OLS (CI)

0.048(−0.094, 0.192)
0.033(0.002, 0.064)
0.374(0.307, 0.444)
0.212(0.139, 0.288)
0.097(−0.073, 0.272)
0.136(0.068, 0.206)
0.201(0.142, 0.263)
0.390(0.236, 0.562)

1.978(1.675, 2.379)
0.527(0.364, 0.715)
2.063(1.742, 2.494)
0.497(0.342, 0.673)
0.900(0.508, 1.541)
1.320(1.212, 1.440)
0.991(0.852, 1.152)
0.440(0.320, 0.571)

MA (CI)

42.70011.644

8.304

8.154

11.82415.090

2.136

6.828

22.82625.16233.33932.14125.98047.09227.20246.139CV′†*P < 0.05, **P < 0.001.
†Modified coefficient of variation (see text).
‡Segments of mesothorax-abdomen (SMA) (see text) was used as an indicator of body size, and thus information on allometry was not obtained.
§Measurements cubed were used for allometric analysis.
¶No significant correlation with SMA (F = 1.964, P = 0.147), and thus further analysis was not implemented.
N, number of individuals; SS, standard deviation; CV, coefficient of variation; Dmax, statistic of Kolmogorov–Smirnov test for normality; r, Pearson’s product-moment

44.196105.99 ± 46.80

133

Prothorax

57.60790.89 ± 52.39

133

Head

68.17139.43 ± 26.90

133

Mandible: rightCV

68.094133

Male
Nongenital parts
Mandible: left

Mean ± SD

39.93 ± 27.21

N

Character

Allometric coefficients

Table 1. Basic statistics and allometric relationships for genitalic and nongenitalic body parts for male and female stag beetles, Prosopocoilus inclinatus

DEVELOPMENTAL VARIABILITY IN GENITALIA

577

29.90734.51386.451320.05 ± 95.72
4.33 ± 0.39

4.35 ± 0.59

142

128

83

SMA‡
Genital parts
Bursa copulatrix‡

Spermatheca§¶

0.292**

0.302**

0.049

0.053

0.074

0.049

0.063

Dmax

0.155

0.121

0.940

0.970

0.840

0.836

r

−0.193**−0.259**−0.142*−0.349**−0.389**b2> 0.163< 0.163> 0.503< 0.503> 0.450< 0.450> 0.417< 0.417> 0.467< 0.467

Range of SMA

0.046(0.012, 0.079)
0.061(0.033, 0.090)

0.699(0.682, 0.716)
0.212(0.246, 0.278)
0.680(0.663, 0.696)
0.265(0.238, 0.291)
0.935(0.925, 0.945)
0.511(0.469, 0.554)
0.877(0.866, 0.888)
0.391(0.366, 0.415)

OLS (CI)

0.050(−0.133, 0.237)
0.159(−0.277, 0.664)

0.802(0.712, 0.901)
0.278(−0.033, 0.650)
0.769(0.673, 0.875)
0.360(0.156, 0.595)
0.979(0.926, 1.034)
0.575(0.313, 0.912)
0.927(0.871, 0.987)
0.413(0.223, 0.631)

MA (CI)

Allometric coefficients

6.121

2.902

6.651

25.345

11.26225.766

11.61620.8488.512

22.711

CV′†*P < 0.05, **P < 0.001.
†Modified coefficient of variation (see text).
‡Segments of mesothorax-abdomen (SMA) (see text) was used as an indicator of body size, and thus information on allometry was not obtained.
§Measurements cubed were used for allometric analysis.
¶No significant correlation with SMA (F = 1.964, P = 0.147), and thus further analysis was not implemented.
N, number of individuals; SS, standard deviation; CV, coefficient of variation; Dmax, statistic of Kolmogorov–Smirnov test for normality; r, Pearson’s product-moment
correlation coefficient with SMA; b2, partial regression; coefficient of quadratic term in second-order polynormial (see text); OLS, cefficient estimated by ordinary
least-square regression; MA, coefficient estimated by major-axis regression; CI, 95% confidence interval of each coefficient.

27.66386.60 ± 23.96

142

Prothorax

29.58637.62 ± 11.13

142

Head

28.434

3.49 ± 0.99

142

Mandible: rightCV

28.119142

FemaleNongenital parts
Mandible: left

Mean ± SD

3.53 ± 0.99

N

Character

Table 1. Continued

578
H. TATSUTA ET AL.

© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90, 573–581

DEVELOPMENTAL VARIABILITY IN GENITALIA
individuals with relatively smaller body size developed disproportionately larger mandibles but the allometric slope changed into ‘negative’ in males withrelative large body size. By contrast, the allometry of
the head was slightly negative when SMA was small,but was positive when SMA was larger than a threshold (> 0.252, Table 1). The prothorax showed an almost
isometric relationship to small SMA, but strongly
negative relationships to large SMA. All allometriccoefficients of genital parts were negative and did
not contradict the prediction of a one-size-fits-all hypothesis. However, compared with nongenital parts,
genital parts showed a wider range of switch points(0.253–0.270 in nongenital parts vs. 0.172–0.266 ingenital parts). Among genital parts, the tergite IX
showed the opposite pattern to these parts: a relatively large allometry coefficient was found in smaller
individuals, whereas sternite IX and tegmen tended tobe larger in allometry as the body size increased.
In females, all body parts tended to show ‘negative’
allometry despite the existence of dimorphism. Moreover, a decrease of the relative growth of genital parts
was observed in individuals with a larger body size. As
in males, large variation in switch point of allometry
was found between genital and nongenital parts.
In both sexes, dispersion around the mean (CV′) was
relatively larger in nongenital parts than in genital
parts, except for the median lobe that showed substantial large variation around the mean (Table 1). Residuals between nongenitalic traits showed significant
correlations in both sexes (Table 2). Significant correlation between genitalic and nongenitalic traits wasfound only in females (mandible right–bursa copula-579

trix and prothorax–bursa copulatrix) whereas no correlation was significant in males.

DISCUSSION
The present study revealed that most genital parts
possessed much lower allometric coefficients thannongenital parts. This is consistent with the prediction by Eberhard et al. (1998), in which individuals
with intermediate genital size are favourably selectedby stabilizing sexual selection. Stabilizing selection
appears to play an important role in maintaining
restricted size of genitalia in many organisms (Eberhard et al., 1998; Bernstein & Bernstein, 2002). Under
this hypothesis, a unimodal distribution and a small
amount of variation were predicted in the frequency
distribution of characters. However, in P. inclinatus,
the variation in genitalia did not agree with the
expectations.
If developmental pattern of each genital part is canalized by stabilizing selection, the range of inflection
points, as well as phenotypic variation, would be more
restricted in genital parts than in nongenital parts
that are considered to be free from such a selective
regime. Indeed, the present study showed that genitalia were much less variable than other body parts as
a whole, but also revealed that ranges of inflection
points on allometric curve varied more in genital parts
than in nongenital parts. To our knowledge, these are
the first findings of this kind. Furthermore, the deviations from the expected mean (CV′) varied in both
genital and nongenital parts. The latter two findings
cannot be reconciled with stabilizing selection and

Table 2. Correlations of residuals of ordinary least-square regression between genitalic and nongenitalic body parts ofmale and female stag beetles, Prosopocoilus inclinatus
Mandible left

Mandible right

Head

Prothorax

Sternite IX

Tergite IX

TegmenMandible right
Head
Prothorax
Sternite IX
Tergite IX
TegmenMedian lobe

0.962*
0.621*
0.812*
0.088
0.251
0.126
−0.1540.611*
0.785*
0.134
0.277
0.173
−0.1880.613*−0.0020.218
0.097−0.154

0.231
0.171
0.150
−0.0480.202
0.321*
0.267

0.095
0.139

−0.107

Female†Mandible right
Head
Prothorax
Bursa copulatrix

0.493*
0.512*
0.705*
0.203

0.342*
0.485*
0.271*

0.771*
0.177

0.268**Significant at 5% level after Bonferroni correction.
†Female spermatheca did not correlate with the size of the segments of mesothorax-abdomen (SMA) and thus the residuals
were not estimated. Further details are provided in the text.
© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90, 573–581

580

H. TATSUTA ET AL.

physiological constraints on genitalia. Recent theoretical and empirical studies have highlighted the importance of complex mating systems being associatedwith a change in genital morphology (Arnqvist, 1998;
Cordoba-Aguilar, 2002). Provided that the functional
differentiation of genital parts during or after couplingcauses the difference in their relative growth patterns,
the developmental mechanisms inducing this differential variability among genitalic parts are mostinteresting.
In the present study, although all allometric coefficients of genital parts were less than 1, some criticaldifferences were found among genital parts. Relatively
large CV and CV′ were found in the median lobe (43.62
and 42.70, respectively) compared with other genital
parts (31.99–33.20). Interestingly, a large CV was also
found in female genitalia (spermatheca: 86.45).
Because the median lobe is inserted into the female
genital opening, these two organs are very likely tointeract mechanically and/or sensory during copulation. Such an interaction has been suggested to involvea coevolutionary arms race between sexes (Hosken &Stockley, 2004). A large CV, which might result fromdirectional sexual selection (Pomiankowski & Moller,
1995), provides substantial potential for a rapidchange that is necessary to cope with coadaptation of
the opposite sex (Arnqvist & Rowe, 2002). Furthermore, the allometric curve of the median lobe did nothave any inflection point whereas the spermatheca did
not correlate with body size (SMA). These lines of evidence underpin the potential for a unique change by
sexual selection in any of these characters.
The phenotypic correlations demonstrated that the
male sternite and tergite, which belong to abdominal
plates, were more strongly associated with body size
than other genital parts such as the median lobe.
Experimental evidence suggests that the presence/
absence of an adjacent character affects the fate of thedevelopmental pattern of other characters because of
trade-offs in resource allocation (Nijhout & Wheeler,
1996; Klingenberg & Nijhout, 1998; Nijhout & Emlen,
1998). However, the results of the present study suggest that the growth of genitalic parts is not necessarily phenotypically correlated and support the viewthat resource competition for development is notnecessarily restricted between traits developing fromspatially close areas of the epithelium (for further
discussion, see Moczek & Nijhout, 2004; Pigliucci &Preston, 2004; Tomkins, Kotiaho & LeBas, 2005).
Another finding worthy of note is that developmental patterns expressed as an allometric curve are moresimilar among male nongenital parts than female nongenital parts. One possible interpretation for such asexual difference may be that the genetic architecturenecessary for developing organs is different between
sexes, and thus the pattern and timing of consuming

nutritional resources are consequently different(Tatsuta, Mizota & Akimoto, 2004). Incorporative
studies of developmental and genetic architecture ofmorphology will be useful to assess the prospects ofthe evolution of phenotypic integration.

ACKNOWLEDGEMENTS
We are grateful to M. Maruyama for kindly providing
several specimens, H. Kishino for valuable advice on
statistics, and an anonymous referee for thoughtfulcomments on earlier version of the manuscript.
H.T. was funded by a Japan Society for the Promotionof Science (JSPS) Research Fellowship for JapaneseYoung Scientists (No. 08608) and the British Council
grant for JSPS fellows.

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