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Evolution, 59(8), 2005, pp. 1838–1843
INTERSPECIFIC AGGRESSION CAUSES NEGATIVE SELECTION ON SEXUAL CHARACTERS
1 Department
KATJA TYNKKYNEN,1,2 JANNE S. KOTIAHO,1,3 MARI LUOJUMÄKI,1 AND JUKKA SUHONEN1
of Biological and Environmental Science, P.O. Box 35, FIN-40014, University of Jyväskylä, Finland
2 E-mail: [email protected]
3 Natural History Museum, P.O. Box 35, FIN-40014, University of Jyväskylä, Finland
Abstract. Interspecific aggression originating from mistaken species recognition may cause selection on secondary
sexual characters, but this hypothesis has remained untested. Here we report a field experiment designed to test directly
whether interspecific aggression causes selection on secondary sexual characters, wing spots, in wild damselfly populations. Males of Calopteryx virgo are more aggressive toward males of C. splendens with large than with small wing
spots. This differential interspecific aggression may cause negative selection on wing spot size. Indeed, our results
show that directional survival selection on wing spot size of C. splendens males was changed by experimental removal
of C. virgo males. Without removal, directional selection went from positive to negative with increasing relative
abundance of C. virgo males. In populations where C. virgo males were removed, this relationship disappeared. These
results verify that interspecific aggression can cause negative selection on sexual characters. Thus, interspecific aggression has the potential to cause divergence on these characters between two species offering an alternative explanation for reinforcement for generating character displacement in secondary sexual characters.
Key words.
sympatry.
Calopteryx, character displacement, interspecific interactions, reinforcement, selection gradient, survival,
Received November 30, 2004.
Secondary sexual characters are conventionally considered
to evolve as a result of selection operating within the species
through female choice (Andersson 1982, 1994; Kirkpatrick
and Ryan 1991; Kokko et al. 2002) or male-male competition
(Arak 1983; Andersson 1994). It has also been recognized
that interspecific interactions, mainly avoidance of maladaptive hybridization (Waage 1975, 1979; Sætre et al. 1997;
Marshall and Cooley 2000; Höbel and Gerhardt 2003) and
predation (Endler 1980; Zuk et al. 1998; Stoddard 1999), can
cause selection on sexual characters. For example, similarity
of sexual characters of two species may lead to hybridization
(e.g., Sætre et al. 1997; Pfennig 2000). If hybridization is
maladaptive, that is, has a negative fitness consequence, selection against interspecific matings arises where divergence
of sexual characters between the species can be selected for.
The process is referred to as reinforcement, since it strengthens the premating reproductive isolation between the species,
and resulting divergence in sexual characters is referred to
as reproductive character displacement (Dobzhansky 1951;
Waage 1975, 1979; Howard 1993; Sætre et al. 1997; Marshall
and Cooley 2000; Höbel and Gerhardt 2003; Lemmon et al.
2004). In addition to reinforcement and predation, however,
interspecific aggression may have an effect on sexual characters, but this possibility has rarely been studied (Butcher
and Rohwer 1989; Sætre et al. 1993; Alatalo et al. 1994;
Seehausen and Schluter 2004; Tynkkynen et al. 2004).
Interspecific aggression may depend on the expression of
male sexual characters and thus cause selection on them. This
may happen when sexual characters of two species resemble
each other, leading to misdirected aggression toward heterospecifics (Alatalo et al. 1994; Tynkkynen et al. 2004). Interspecific aggression is likely to have an effect on male
fitness. For example, interspecific aggression can force males
into less preferred habitats (Alatalo et al. 1994; Nomakuchi
and Higashi 1996; Martin and Martin 2001; Melville 2002),
reduce the ability of a male to obtain or keep a territory
(Rowland 1983; Gaudreault and Fitzgerald 1985; Tynkkynen
et al. 2005), or reduce the survival of individuals (e.g., Eccard
and Ylönen 2002). If males with the most exaggerated sexual
characters are those that most resemble heterospecifics, interspecific aggression may lead to negative selection on the
expression of sexual characters.
In the damselfly Calopteryx splendens, males have pigmented wing spots with blue reflections as sexual characters,
the size of which exhibit continuous variation (Rantala et al.
2000; Tynkkynen et al. 2004; Svensson et al. 2004). Interestingly, large-spotted males of C. splendens are the target
of higher interspecific aggression than small-spotted males.
This is because males of another damselfly species, Calopteryx virgo, attack large-spotted C. splendens males more frequently and from longer distances than small-spotted males
(Tynkkynen et al. 2004). This aggression is likely to be
caused by mistaken species recognition since large-spotted
C. splendens males resemble C. virgo males, which have almost completely pigmented wings (Tynkkynen et al. 2004).
If interspecific aggression causes differential mortality on C.
splendens males depending on their wing spot size, this effect
is likely to be amplified when the relative abundance of C.
virgo males in the population increases. This is because C.
splendens males spend more time in interspecific contests
when relative abundance of C. virgo males increases (Tynkkynen et al. 2005). In addition, it seems that interspecific
aggression has had evolutionary consequences for wing spots,
since character displacement exists such that wing spot size
is negatively correlated with the relative abundance of C.
virgo males across populations (Tynkkynen et al. 2004).
In this study, we aimed to determine whether interspecific
aggression can cause negative survival selection on wing spot
size of C. splendens. To do this, we performed a removal
experiment in the field in which the relative abundance of
C. virgo males was manipulated.
1838
q 2005 The Society for the Study of Evolution. All rights reserved.
Accepted June 6, 2005.
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MATERIALS
AND
METHODS
Study Populations
The study was performed on seven rivers between 26 June
and 22 August 2001 near the city of Jyväskylä, central Finland (628159N, 258259E). Four of the rivers (River Neulajoki,
River Niemenjoki, River Myllyjoki, and Piikakoski in River
Isojoki) were controls (no manipulation) and three of the
rivers were treatments (River Janholanjoki, River Mustajoki,
and Outinen in River Isojoki). Only data collected before 28
July (first four weeks) were included in our analyses, because
at that time, the main flying season of C. splendens had finished and there were too few individuals to allow reliable
estimation of survival selection.
Treatments and Recapturing
Well-defined sections of the rivers (length: 111 6 20 m
[mean 6 SE]) were used to carry out our study. These sections
were bordered both up- and downstream by an unsuitable
habitat for C. splendens (e.g., lake, forested river banks, etc.),
with the exception of one river. All rivers were visited once
a week, every seven days, provided the weather was adequate
for damselflies to be flying. When the weather was cold,
rainy, or very cloudy, visits were shifted by a maximum of
one day.
In each population, male survival was monitored in sampling periods of one week (three to four sampling periods
per population), because the relative abundance of the two
species may not be stable over long periods and changes in
this variable may affect the intensity of survival selection.
To determine the relative abundance of C. virgo and C. splendens, we caught all males of both species during each visit.
If there were too many individuals and we were not able to
catch them all, we caught all males during approximately two
hours (which was the case in two controls and in one treatment population). The relative abundance of C. virgo males
was estimated by dividing the total number of C. virgo males
by the total number of both species. In the treatment populations, we measured the relative abundance of C. virgo males
on the last day of each sampling period, by which time new
C. virgo males had appeared in the populations. Note that
immediately after the removal, the relative abundance of C.
virgo males was near zero but increased as new C. virgo
appeared into the population. Thus, the estimates for the treatment populations are the highest relative abundance experienced by these populations. In addition, after the removal,
the relative abundance was near zero, causing greater reduction on this variable when natural relative abundance of C.
virgo was high.
In all populations, the hind wings of C. splendens males
were measured and marked with a unique three-letter code
with silver marking pen, after which the males were released.
All wing measurements (length of left and right wing, width
of left and right wing spot) were taken from hind wings with
digital calipers to the nearest 0.01 mm. If the wing was broken, measurements were not taken. Repeatabilities of measurements are high, being equal to or greater than 0.96 (Tynkkynen et al. 2004). A total of 801 C. splendens males was
marked during the first four weeks (114.4 6 38.5 [mean 6
SE] males from each population), but because males that
survived were treated as newly marked individuals in the
next period, there were 993 individuals in the statistical analyses. Survival and recapture probabilities were estimated by
an open population capture-recapture model using MARK
software (version 4.0; White and Burnham 1999). Survival
probability (6 SE) from first capture to first recapture occasion was 0.33 6 0.03, 0.32 6 0.07 from first to second
recapture occasion, and 0.16 6 0.05 from second to third
recapture occasion. Recapture probability (6 SE), (i.e., probability that a live male is recaptured), was 0.62 6 0.06 for
the first, 0.64 6 0.13 for the second, and 1.0 6 0.00 for the
third recapture occasion.
In control populations, we did not manipulate relative
abundance. Thus, to simplify estimation of relative abundance in these populations, C. virgo males were marked, tallied, and released. In treatment populations where we manipulated the relative abundance of C. virgo males, we removed all C. virgo males that we were able to find. Removal
was repeated once a week, and in total we removed 524 males.
On average, we removed 175 6 72 (mean 6 SE) males from
each treatment population.
Selection and Statistical Analyses
Estimates of survival selection on wing measurements are
based on recapture data under the assumption that males not
recaptured have died. This assumption is likely to be justified
because in our data the recapture probability was 62–100%
(see above). Moreover, C. splendens is a poor disperser (Stettmer 1996; Schutte et al. 1997): in sympatric population less
than 15% of C. splendens dispersed 150 m or more (Stettmer
1996). Note also that in our study area all potential places
where dispersing C. splendens males could settle are inhabited by C. virgo (K. Tynkkynen, pers. obs.). In addition, with
the exception of one river, our study sections were selected
such that they were bordered by unsuitable habitat for C.
splendens. However, we made an effort to detect possibly
dispersed individuals and searched approximately 50 m of
river outside both ends of our study section. Only 5.4% of
marked males were found in these areas and they were included in the analyses.
Directional selection was estimated by means of standardized selection differentials (s, measures total selection) and
by standardized selection gradients (b, measures direct selection). Before analyses, traits before selection were standardized (mean 5 0; variance 5 1) for each sampling period
after which all sampling periods within a population were
pooled. Directional selection differentials were estimated as
the difference in standardized trait means before and after
the selection. Statistical significance of standardized selection
differentials were calculated using independent samples ttests (Endler 1986). To estimate direct survival selection acting on absolute wing spot size and wing length, we performed
multivariate analysis using logistic regression (Janzen and
Stern 1998). Statistical significance of selection gradients was
estimated using analysis of deviance (Hardy and Field 1998).
Statistical analyses of the removal experiment were performed with analysis of covariance (ANCOVA) using population-level selection coefficients and mean of relative abun-
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TABLE 1. Population-level statistics of standardized selection differentials (s) and standardized selection gradients (b) for Calopteryx
splendens wing spot size and wing length. Populations within treatments are arranged in ascending order according to the relative
abundance of C. virgo males. C/T indicates control (C) and treatment (T) populations. Degrees of freedom (df) indicated with decimals
reveals adjusted degrees of freedom, and they were used in t-test when the assumption of equality of variances was not met.
River
C/T
s
SE
t
df
P
b
SE
x21
P
Wing spot size
Neulajoki
Niemenjoki
Myllyjoki
Piikakoski
Janholanjoki
Mustajoki
Outinen
C
C
C
C
T
T
T
0.31
0.20
20.25
20.43
0.02
0.06
0.17
0.10
0.12
0.23
0.10
0.09
0.14
0.30
22.58
21.44
0.73
2.11
20.15
20.32
20.49
92.0
278
52
20.4
121.1
134
44
0.011
0.152
0.471
0.048
0.878
0.752
0.628
0.35
0.19
20.27
20.85
0.03
0.05
0.15
0.14
0.11
0.33
0.76
0.12
0.10
0.30
7.23
2.87
0.70
1.48
0.07
0.25
0.25
0.007
0.090
0.402
0.223
0.792
0.616
0.617
Wing length
Neulajoki
Niemenjoki
Myllyjoki
Piikakoski
Janholanjoki
Mustajoki
Outinen
C
C
C
C
T
T
T
20.13
0.16
20.41
1.02
20.29
20.04
0.30
0.13
0.13
0.39
0.40
0.10
0.15
0.26
0.87
21.10
1.12
21.77
2.20
0.25
20.86
342
278
52
31
348
134
44
0.388
0.274
0.269
0.087
0.029
0.804
0.392
20.15
0.12
20.43
1.48
20.33
20.03
0.31
0.12
0.11
0.31
0.75
0.12
0.10
0.31
1.46
1.31
2.03
5.89
7.77
0.12
1.07
0.228
0.253
0.154
0.015
0.005
0.731
0.302
dances of C. virgo males over each sampling period. Error
variances were equal except for the case of wing spot size
(Levene’s test F1,5 5 14.73, P 5 0.012 for selection differentials and F1,5 5 13.71, P 5 0.014 for selection gradients).
All statistical analyses were conducted with SPSS (SPSS
11.0.1, standard version 2001).
RESULTS
AND
DISCUSSION
When the relative abundance of C. virgo males was low
in control populations, large-spotted C. splendens males were
at a selective advantage under survival selection (Table 1).
However, the selective advantage of the large-spotted males
decreased with increasing relative abundance of C. virgo
males (filled circles in Fig. 1A,B). Finally, when the relative
abundance of C. virgo males was high there was negative
survival selection on wing spot size in C. splendens (Table
1). The decline in selection coefficients with increasing relative abundance of C. virgo is likely to be a consequence of
differential interspecific aggression (Tynkkynen et al. 2004).
This is because the time that C. splendens males spend fighting with C. virgo increases with increasing relative abundance
of C. virgo males (Tynkkynen et al. 2005). In treatment populations, a similar decline in selection coefficients was not
detected (open circles in Fig. 1A,B). This suggests that when
relative abundance of C. virgo males was high, the manipulation was effective in reducing interspecific aggression towards large-spotted C. splendens males to a level at which
their survival was not negatively affected.
There was a significant interaction effect between the treatment and the relative abundance of C. virgo males on the
selection differentials for wing spot size of C. splendens
males (Table 2; Fig. 1A). This means that directional survival
selection on wing spot size in relation to relative abundance
of C. virgo depended on the treatment. The difference in the
strength of selection on wing spot size between control and
treatment populations was highest when the relative abundance of C. virgo was high (see Fig. 1A,B). This is an expected consequence of the removal of C. virgo males if sur-
vival selection is affected by interspecific aggression. This
is because our manipulation caused a greater reduction in
relative abundance of C. virgo and thus interspecific aggression when the natural relative abundance of C. virgo in the
population was high. There was no interaction effect between
the treatment and the relative abundance of C. virgo on the
selection coefficients for wing length (Table 2; Figs. 1C,D),
suggesting that interspecific aggression does not cause selection on male size.
Our results suggest that interspecific aggression has caused
the previously-described pattern of character displacement in
C. splendens males, in which wing spot size is inversely
related to the relative abundance of C. virgo males in populations (Tynkkynen et al. 2004). This is apparently because
survival advantage of large-spotted C. splendens males decreases with increasing relative abundance of C. virgo males.
Another possible explanation for character displacement in
wing spot size is the avoidance of maladaptive hybridization.
Hybrids between C. virgo and C. splendens occur in nature
(assessed by randomly amplified polymorphic DNA technique), but the fitness of hybrids is unknown (K. Tynkkynen,
A. Grapputo, J. S. Kotiaho, M. J. Rantala, S. Väänänen, and
J. Suhonen, unpubl. data; see also De Marchi 1990; Corbet
1999). However, according to our personal observation, matings between heterospecifics are rare (less than 3% of matings), indicating that interspecific aggression is a much more
prevalent phenomenon in nature than hybridization (see
Tynkkynen et al. 2004). This suggests that although our result
does not exclude the possibility of the existence of reinforcement, interspecific aggression should have a greater role than
avoidance of maladaptive hybridization in the origin of character displacement in wing spot size of C. splendens males.
Our results provide direct evidence that interspecific aggression is able to cause phenotypic selection on sexual characters. This finding may aid the future development of sexual
selection theory, since interspecific aggression may be a more
common mechanism explaining variation in sexual characters
among populations than has previously been realized. For
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FIG. 1. Patterns of survival selection for wing spot size and wing length in relation to the relative abundance of Calopteryx virgo males.
(A) Standardized selection differentials and (B) gradients for wing spot size. (C) Standardized selection differentials and (D) gradients
for wing length. In both panels filled circles and solid line indicate control populations with natural relative abundance of C. virgo males.
Open circles and broken line indicate treatment populations where relative abundance of C. virgo was manipulated via removals. In
treatment populations, the relative abundance of C. virgo males was estimated by using the number of C. virgo males on the last day of
each sampling period. Note that immediately after the removal, the relative abundance of C. virgo was near zero (for further details see
Materials and Methods). Standardized selection differentials and gradients significantly different from zero are indicated with an asterisk:
* P , 0.05, ** P , 0.01.
TABLE 2. Analysis of covariance testing the effect of treatment and relative abundance of Calopteryx virgo males on standardized
selection differentials and gradients for C. splendens wing spot size and wing length. Eta2 refers to the proportion of variance explained.
Trait
Selection differentials
Wing spot size1
Wing length2
Selection gradients
Wing spot size3
Wing length4
1
R2
R2
3 R2
4 R2
2
5
5
5
5
0.90.
0.24.
0.79.
0.26.
Source
SS
df
MS
F
P
Eta2
Treatment
Abundance
Treatment 3 abundance
Error
Treatment
Abundance
Treatment 3 abundance
Error
0.15
0.09
0.22
0.04
0.01
0.28
0.00
1.04
1
1
1
3
1
1
1
3
0.15
0.09
0.22
0.01
0.01
0.28
0.00
0.35
11.13
7.15
17.05
0.045
0.076
0.026
0.79
0.70
0.85
0.02
0.80
0.01
0.899
0.437
0.943
0.01
0.21
0.00
Treatment
Abundance
Treatment 3 abundance
Error
Treatment
Abundance
Treatment 3 abundance
Error
0.22
0.24
0.38
0.20
0.00
0.49
0.01
1.84
1
1
1
3
1
1
1
3
0.22
0.24
0.38
0.06
0.00
0.49
0.01
0.61
3.29
3.54
5.67
0.167
0.157
0.097
0.52
0.54
0.65
0.00
0.79
0.02
0.997
0.439
0.910
0.00
0.21
0.01
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example, character displacement in sexual characters of two
species between allopatric and sympatric populations has often been interpreted to result from reinforcement (e.g., Waage
1975, 1979; Sætre et al. 1997; Marshall and Cooley 2000;
Höbel and Gerhardt 2003). Some alternative explanations for
the pattern have been suggested, although experimental evidence is scarce (Noor 1999; Servedio 2001; Coyne and Orr
2004). However, because interspecific aggression can cause
strong selection on sexual characters even during short periods of time, its effect on sexual characters may be even
greater than the effect of reinforcement. In the famous example of reinforcement, it has been concluded that divergence
in plumage coloration of collared and pied flycatchers (Ficedula albicollis and F. hypoleuca, respectively) in sympatric
populations is caused by the avoidance of hybridization
(Sætre et al. 1997). However, Sætre et al. (1993) and Alatalo
et al. (1994) have already suggested that the character displacement in the plumage coloration may also be caused by
interspecific aggression. In the face of our result, the possibility that interspecific aggression can indeed cause selection on secondary sexual characters and thus have potential
to cause character displacement can no longer be neglected.
ACKNOWLEDGMENTS
We thank M. Vaittinen and M. Häkkilä for assistance in
field. Special thanks to M. Björklund, R. Brooks, J. Jokela,
K. Lindström, L. W. Simmons, E. I. Svensson, J. L. Tomkins,
and T. Tregenza for comments on the manuscript. The manuscript was further improved by the comments of M. Peterson
and two anonymous reviewers. The study was funded by a
grant from the Alfred Kordelin Foundation, the Jenny and
Antti Wihuri Foundation, and the Finnish Cultural Foundation (Keski-Suomi) to KT, the Finnish Biodiversity Research
Programme to JS, the Academy of Finland to JSK, and the
Academy of Finland under the Finnish Centre of Excellence
Programme during 2000–2005 (project 44878) to JS.
LITERATURE CITED
Alatalo, R. V., L. Gustafsson, and A. Lundberg. 1994. Male coloration and species recognition in sympatric flycatchers. Proc.
R. Soc. Lond. B 256:113–118.
Andersson, M. 1982. Female choice selects for extreme tail length
in a widowbird. Nature 299:818–820.
———. 1994. Sexual selection. Princeton Univ. Press, Princeton,
NJ.
Arak, A. 1983. Sexual selection by male–male competition in natterjack toad choruses. Nature 306:261–262.
Butcher, G. S., and S. Rohwer. 1989. The evolution of conspicuous
and distinctive coloration for communication in birds. Curr. Ornithol. 6:51–108.
Corbet, P. S. 1999. Dragonflies: behaviour and ecology of Odonata.
Harley Books, Essex, U.K.
Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer Associates,
Sunderland, MA.
De Marchi, G. 1990. Precopulatory reproductive isolation and wing
colour dimorphism in Calopteryx splendens females in southern
Italy (Zygoptera: Calopterygidae). Odonatologica 19:243–250.
Dobzhansky, T. 1951. Genetics and the origin of species. 3rd ed.
Columbia Univ. Press, New York.
Eccard, J. A., and H. Ylönen. 2002. Direct interference or indirect
exploitation? An experimental study of fitness costs of interspecific competition in voles. Oikos 99:580–590.
Endler, J. A. 1980. Natural selection on colour patterns in Poecilia
reticulata. Evolution 34:76–91.
———. 1986. Natural selection in the wild. Princeton Univ. Press,
Princeton, NJ.
Gaudreault, A., and G. J. Fitzgerald. 1985. Field observations of
intraspecific and interspecific aggression among sticklebacks
(Gasterosteidae). Behaviour 94:203–211.
Hardy, I. C. W., and S. A. Field. 1998. Logistic analysis of animal
contests. Anim. Behav. 56:787–792.
Höbel, G., and H. C. Gerhardt. 2003. Reproductive character displacement in the acoustic communication system of green tree
frogs (Hyla cinerea). Evolution 57:894–904.
Howard, D. J. 1993. Reinforcement: origin, dynamics and fate of
an evolutionary hypothesis. Pp. 46–69 in R. G. Harrison, ed.
Hybrid zones and the evolutionary process. Oxford Univ. Press,
Oxford, U.K.
Janzen, F. J., and H. S. Stern. 1998. Logistic regression for empirical
studies of multivariate selection. Evolution 52:1564–1571.
Kirkpatrick, M., and M. J. Ryan. 1991. The evolution of mating
preferences and the paradox of the lek. Nature 350:33–38.
Kokko, H., R. Brooks, J. M. McNamara, and A. I. Houston. 2002.
The sexual selection continuum. Proc. R. Soc. Lond. B 269:
1331–1340.
Lemmon, A. R., C. Smadja, and M. Kirkpatrick. 2004. Reproductive
character displacement is not the only possible outcome of reinforcement. J. Evol. Biol. 17:177–183.
Marshall, D. C., and J. R. Cooley. 2000. Reproductive character
displacement and speciation in periodical cicadas, with description of a new species, 13-year Magicicada neotredecim. Evolution 54:1313–1325.
Martin, P. R., and T. E. Martin. E. 2001. Ecological and fitness
consequences of species coexistence: a removal experiment with
wood warblers. Ecology 82:189–206.
Melville, J. 2002. Competition and character displacement in two
species of scincid lizards. Ecol. Lett. 5:386–393.
Nomakuchi, S., and K. Higashi. 1996. Competitive habitat utilization in the damselfly, Mnais nawai (Zygoptera: Calopterygidae) coexisting with a related species, Mnais pruinosa. Res. Popul. Ecol. 38:41–50.
Noor, M. A. F. 1999. Reinforcement and other consequences of
sympatry. Heredity 83:503–508.
Pfennig, K. S. 2000. Female spadefoot toads compromise on mate
quality to ensure conspecific matings. Behav. Ecol. 11:220–227.
Rantala, M. J., J. Koskimäki, J. Taskinen, K. Tynkkynen, and J.
Suhonen. 2000. Immunocompetence, developmental stability
and wingspot size in the damselfly Calopteryx splendens. L. Proc.
R. Soc. Lond. B 267:2453–2457.
Rowland, W. J. 1983. Interspecific aggression and dominance in
Gasterosteus. Environ. Biol. Fish. 8:269–277.
Sætre, G-P., M. Král, and V. Bičı́k. 1993. Experimental evidence
for interspecific female mimicry in sympatric Ficedula flycatchers. Evolution 47:939–945.
Sætre, G.-P., T. Moum, S. Bureš, M. Král, M. Adamjan, and J.
Moreno. 1997. A sexually selected character displacement in
flycatchers reinforces premating isolation. Nature 387:589–592.
Schutte, G., M. Reich, and H. Plachter. 1997. Mobility of the rheobiont damselfly Calopteryx splendens (Harris) in fragmented
habitats (Zygoptera: Calopterygidae). Odonatologica 26:
317–327.
Seehausen, O., and D. Schluter. 2004. Male-male competition and
nuptial-colour displacement as a diversifying force in Lake Victoria cichlid fishes. Proc. R. Soc. Lond. B 271:1345–1353.
Servedio, M. R. 2001. Beyond reinforcement: the evolution of premating isolation by direct selection on preferences and postmating, prezygotic incompatibilities. Evolution 55:1909–1920.
Stettmer, C. 1996. Colonisation and dispersal patterns of banded
(Calopteryx splendens) and beautiful demoiselles (C. virgo)
(Odonata: Calopterygidae) in southeast German streams. Eur. J.
Entomol. 93:579–593.
Stoddard, P. K. 1999. Predation enhances complexity in the evolution of electric fish signals. Nature 400:254–256.
Svensson, E. I., L. Kristoffersen, K. Oskarsson, and S. Bensch.
2004. Molecular population divergence and sexual selection on
BRIEF COMMUNICATIONS
morphology in the banded demoiselle (Calopteryx splendens).
Heredity 93:423–433.
Tynkkynen, K., M. J. Rantala, and J. Suhonen. 2004. Interspecific
aggression and character displacement in the damselfly Calopteryx splendens. J. Evol. Biol. 17:759–767.
Tynkkynen, K., J. S. Kotiaho, M. Luojumäki, and J. Suhonen. 2005.
Interspecific territoriality between Calopteryx splendens and Calopteryx virgo damselflies: the role of secondary sexual characters. Anim. Behav. In press.
Waage, J. K. 1975. Reproductive isolation and the potential for
character displacement in the damselflies, Calopteryx maculata
1843
and C. aequabilis (Odonata: Calopterygidae). Syst. Zool. 24:
24–36.
———. 1979. Reproductive character displacement in Calopteryx
(Odonata: Calopterygidae). Evolution 33:104–116.
White, G. C., and K. P. Burnham. 1999. Program MARK: survival
estimation from populations of marked animals. Bird Study
46(Supp.):120–139.
Zuk, M., J. T. Rotenberry, and L. W. Simmons. 1998. Calling songs
of field crickets (Teleogryllus oceanicus) with and without phonotactic parasitoid infection. Evolution 52:166–171.
Corresponding Editor: M. Peterson