BRIEF COMMUNICATIONS

BRIEF COMMUNICATIONS 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 LUOJUMA¨KI,1 AND JUKKA SUHONEN1 of Biological and Environmental Science, P.O. Box 35, FIN-40014, University of Jyva¨ skyla¨, Finland 2 E-mail: [email protected] 3 Natural History Museum, P.O. Box 35, FIN-40014, University of Jyva ¨ skyla¨, 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; Ho¨bel 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; Ho¨bel 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 Ylo¨nen 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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BRIEF COMMUNICATIONS

MATERIALS

AND

METHODS

Study Populations The study was performed on seven rivers between 26 June and 22 August 2001 near the city of Jyva¨skyla¨, 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. Va¨a¨na¨nen, 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; Ho¨bel 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. Ha¨kkila¨ for assistance in field. Special thanks to M. Bjo¨rklund, R. Brooks, J. Jokela, K. Lindstro¨m, 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. Ylo¨nen. 2002. Direct interference or indirect exploitation? An experimental study of fitness costs of interspecific competition in voles. Oikos 99:580–590.

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