doi: 10.1111/j.1420-9101.2009.01870.x
Alternative reproductive tactics and the propensity of hybridization
K. TYNKKYNEN*, K. J. RAATIKAINEN*, M. HÄKKILÄ*, E. HAUKILEHTO* & J. S. KOTIAHO* *Centre of Excellence in Evolutionary Research, Department of Biological and Environmental Sciences, University of Jyväskylä, Jyväskylä, Finland
Natural History Museum, University of Jyväskylä, Jyväskylä, Finland
Keywords:
Abstract
adaptive hybridization;
Calopteryx damselflies;
fluctuating selection;
reinforcement;
reproductive isolation;
secondary sexual ornaments;
territoriality.
One explanation for hybridization between species is the fitness benefits it
occasionally confers to the hybridizing individuals. This explanation is possible
in species that have evolved alternative male reproductive tactics: individuals
with inferior tactics might be more prone to hybridization provided it increases
their reproductive success and fitness. Here we experimentally tested whether
the propensity of hybridization in the wild depends on male reproductive
tactic in Calopteryx splendens damselflies. Counter to our expectation, it was
males adopting the superior reproductive tactic (territoriality) that had greatest
propensity to hybridize than males adopting the inferior tactics (sneakers and
floaters). Moreover, among the territorial males, the most ornamented males
had greatest propensity to hybridize whereas the pattern was reversed in the
sneaker males. Our results suggest that there is fluctuating selection on male
mate discrimination against heterospecific females depending on both ornament size and the male’s reproductive tactic.
Introduction
Hybridization between species is considered maladaptive
when it lowers the fitness of the parents. When
maladaptive hybridization occurs, a selection pressure
can arise leading to reinforcement of premating
reproductive isolation between hybridizing species
(Dobzhansky, 1951; Sætre et al., 1997a; Higgie et al.,
2000; Coyne & Orr, 2004; Pfennig, 2007). However, in
some cases hybridization does confer fitness benefits and
thus may give rise to adaptive heterospecific mating
decisions (Nuechterlein & Buitron, 1998; Veen et al.,
2001; Pfennig, 2007; Reyer, 2008). In such a case
hybridization should be under positive selection provided
that the fitness of the fertile hybrids compensate for the
costs instigated by hybridization.
Within a species, males frequently employ different
tactics to compete for mates (Gross, 1996; Tomkins &
Brown, 2004; Tomkins & Hazel, 2007). These tactics
usually arise because some males are inferior in compeCorrespondence: Katja Tynkkynen, Centre of Excellence in Evolutionary
Research, Department of Biological and Environmental Sciences,
PO Box 35, University of Jyväskylä, FI-40014 Jyväskylä, Finland.
Tel.: +358 14 2602311; fax: +358 14 2602321;
e-mail: [email protected]
2512
tition for mates, and they have to engage in an alternative reproductive tactic to gain some fitness return. It has
been suggested that male alternative reproductive tactics
combined with adaptive mating decisions can lead to
hybridization, especially if there are substantial differences in the tactics in terms of reproductive success
(Lamb & Avise, 1986; Wirtz, 1999; Garcia-Vazquez et al.,
2002). Although it is well known that males of many
species court and mate with heterospecific females
(Coyne & Orr, 2004; Mallet, 2005), there are only
few empirical studies addressing the role of male reproductive tactic on hybridization (Garcia-Vazquez et al.,
2002; Jennings & Philipp, 2002; see also Frisch & Van
Herwerden, 2006).
Calopteryx splendens Harris and C. virgo L. (Odonata:
Calopterigidae) are two congeneric damselfly species,
that hybridize in nature at low frequency (Tynkkynen
et al., 2008a). Male Calopteryx damselflies display three
alternative reproductive tactics. There are territorial,
sneaker and floater males, of which the latter two do
not defend territories of their own (see Pajunen, 1966;
Forsyth & Montgomerie, 1987; Plaistow, 1997; Corbet,
1999). Sneakers act as satellites sneaking copulations
with females arriving to the territory of the territorial
males. Floaters, instead, patrol along a river. The
ª 2009 THE AUTHORS. J. EVOL. BIOL. 22 (2009) 2512–2518
JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Male tactics and hybridization propensity
adoption of different tactics is conditional (Pajunen,
1966; Forsyth & Montgomerie, 1987; Corbet, 1999), and
the reproductive success of non-territorial sneaker and
floater males is substantially lower (up to 1000 times)
than that of the territorial males (Plaistow & Siva-Jothy,
1996). The territorial tactic is energetically costly, and the
tactic a particular individual adopts is related to male age
and energy reserves (Plaistow & Siva-Jothy, 1996;
Plaistow, 1997; Corbet, 1999).
In C. splendens there is a curious asymmetry between
the sexes in premating reproductive isolation against
C. virgo: C. splendens females display strong discrimination
against C. virgo males, while C. splendens males very often
court C. virgo females (Svensson et al., 2007; Tynkkynen
et al., 2008a,b). This asymmetry, together with the fact
that males can force females to copulate (Cordero, 1999),
implies that males are responsible for the hybridization
between these two species (Tynkkynen et al., 2008a).
This is against the view that females, who are usually the
more discriminating sex and whose cooperation is often
needed for a successful copulation, are mainly responsible for copulations leading to hybridization (e.g. Ryan &
Wagner, 1987; Wirtz, 1999; Malmos et al., 2001; Randler,
2002; but see Peterson et al., 2005). However, when
females are highly discriminating, males may be relieved
from selection to become more discriminating. There can
be even costs for males to be more discriminating, as
conspecific mates may be missed if males discriminate
females too much (Parker, 1983; Sætre et al., 1997b;
Parker & Partridge, 1998; Peterson et al., 2005). Nevertheless, males can discriminate against females provided
there are fitness benefits to be gained from the discrimination (Byrne & Rice, 2006; Servedio & Lande, 2006;
Clutton-Brock, 2007; Servedio, 2007; Bel-Venner et al.,
2008; Rowell & Servedio, 2009). Furthermore, male
competitive ability can affect their mate choice: at least in
some cases males with poorer competitive ability can
mate more opportunistically than males with better
competitive ability (Bel-Venner et al., 2008). Thus, in
addition to females it can also be males who initiate the
behavior leading to copulation between heterospecific
individuals.
Here we report a replicated field experiment designed
to determine the role of male alternative reproductive
tactics on the propensity of hybridization in wild
C. splendens males. We predict that males engaging in
non-territorial tactics (sneakers and floaters) should have
greater propensity to hybridize with C. virgo females than
territorial males. In addition, we investigated the role of
male ornament size (i.e. wing spot size) and age on the
propensity of hybridization. There are some indications
that ornament size of Calopterygid damselflies is positively related to their competitive ability, as territorial
males have larger ornament size than non-territorial
males (Siva-Jothy, 1999; Córdoba-Aguilar, 2002;
Contreras-Garduño et al., 2006, 2008). Thus, it might
be that males with smaller ornament size are less
2513
selective and thus have greater propensity to hybridize
than males with larger ornaments. It is also possible, that
when males get older, their residual reproductive value
declines, and as a consequence, propensity to hybridize
increases.
Materials and methods
Study species
Calopteryx splendens and C. virgo are two congeneric
damselfly species which resemble each other ecologically
and phenotypically (Askew, 1988). The distribution of
the species overlap in a large part of Europe, and this is
also the case in Finland (Askew, 1988). As secondary
sexual characters or ornaments, males of C. splendens
have pigmented, blue reflecting wing spots in the middle
of the wings and these ornaments are displayed to
females during courtship flight (Pajunen, 1966; Askew,
1988; Siva-Jothy, 1999). The flying pattern of the
courtship flight differs substantially from that of normal
flight, and is easy to observe. Most strikingly, wing stroke
frequency during courtship flight is four times faster than
normal flight, and wings are moved asynchronously. In
addition, male courtship often includes short landings on
water surface and floating a few centimetres with the
current (Pajunen, 1966; Corbet, 1999). The wing spot
size of C. splendens males may indicate male quality and
competitive ability to conspecifics, as in Calopteryx damselflies wing spot size is positively related to immunocompetence (Rantala et al., 2000; Siva-Jothy, 2000),
survival (Tynkkynen et al., 2005; see also Grether,
1996) and territoriality (Siva-Jothy, 1999; CórdobaAguilar, 2002). In Calopteryx damselflies both sexes
can mate with several partners during their lifetime
(Siva-Jothy & Hooper, 1995; Plaistow & Siva-Jothy,
1996; Siva-Jothy, 1999; Córdoba-Aguilar, 2002).
Experimental design
The study was performed between 20th of June and 19th
of July 2006 at the River Niemenjoki in Central Finland
(6215¢N, 2619¢E). C. splendens and C. virgo were sympatric at the study site, but the latter was less abundant
(7% of all males were C. virgo). At the river, we
established a 100 m section where the experiment was
conducted. As we wanted to know the age of males in
days (i.e. the number of days a male has been mature),
we captured all males when they first time entered to the
river after short teneral phase between emergence and
sexual maturity. To be sure that the newly captured
males were freshly matured, wing stiffness of each of the
males was assessed; young freshly matured males have
clearly less stiff wings than old males (see Plaistow &
Siva-Jothy, 1996). Later, only males which were just
matured when first appeared to the river, and thus from
which we were able to know their age, were accepted to
ª 2009 THE AUTHORS. J. EVOL. BIOL. 22 (2009) 2512–2518
JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
2514
K. TYNKKYNEN ET AL.
the experiment. At the first capture, males were marked
uniquely on their hind wings with a silver marking pen
(Artline EK-999XF; Shachihata, Japan), and the wing
spot width was measured from the left hind wing with a
digital caliper to the nearest 0.01 mm. Males were
measured only once because in our previous study
measurement of the size of wing spots has been highly
repeatable (R = 0.96 in the study of Tynkkynen et al.
(2004)). All males were measured by one person (K.J.R.).
During the day, we walked along the river, and the
reproductive tactic of each observed male was determined from their behavior (see Pajunen, 1966). Territorial males perch close to the water and defend territories,
whereas sneaker males perch higher in the vegetation
and do not defend the territory. Floater males are very
mobile and fly around most of the time. From the
observational data a daily tactic was determined for each
male. From 226 males individually marked for the study,
157 were observed to perform at least one tactic.
The propensity of C. splendens males to hybridize was
determined by moving mature, live C. virgo females
towards known territorial, sneaker and floater males of
C. splendens. Before the presentation of the heterospecific
females, possible tactic-dependent differences in sexual
activity were removed by presenting a live conspecific
female to each experimental male. The presentation of
C. virgo female was done only if a male courted or tried to
mate with the conspecific female (ranks 5–7 in the
category of reactions; see below the classification of
reactions). Due to this procedure, there were no differences between tactics in male reactions towards conspecific females among experimental males to which
heterospecific females were presented (one way A N O V A ,
F2,59 = 1.04, P = 0.361). Presentation of females was
done by moving and presenting them 30 sec to males
with the aid of fishing line (length c. 150 cm, diameter
0.11 mm) and a rod (length 4 m) so that a female was
constantly flying preventing her to perform rejection or
acceptance signals which she is known to perform while
perched (see Corbet, 1999). The presentation of females
started always when a male was perched. Before the
presentation, the end of the fishing line was attached to
the thorax of the females just in front of the wings with a
small droplet of glue (Super Attack; Loctite Corp. 1999,
Henkel, Düsseldorf, Germany) and a small piece (c.
3 · 3 mm) of white paper tape (MicroporeTM; 3M Company, St Paul, MN, USA) to ensure that the line attached
firmly. To make the tape more cryptic, we dyed it black
with a permanent drawing pen (Textmark 500, Japan)
after the glue had dried. A small lead weight was attached
to the fishing line, c. 20 cm above a female allowing us to
manipulate the female flying direction (for further details
see Tynkkynen et al., 2008). This treatment did not have
any obvious adverse effects on the flying ability of the
females. However, the fishing line disturbed tandem
formation, and thus copulations were not observed
directly. Instead, reactions of C. splendens males were
ranked into seven categories of increasing interest to
mate with the presented female. These categories were
from the highest interest: an attempted tandem (7),
courting more than 5 s (6), courting less than 5 s (5),
interested gesture (e.g. flying around a female) (4), a
non-aggressive reaction (e.g. evasive movement) (3), no
reaction (2), an aggressive reaction (attack against a
female or warning signaling) (1) (see also Pajunen,
1966). In the case of heterospecific females, this classification of male interest was interpreted to be indicative
of males’ propensity to hybridize.
Twelve males changed their tactic during the experiment after the initial female presentation. For these 12
males, a new heterospecific female was presented. From
these 12 males only the reaction to the initial presentation was included into the main analysis in which we
analysed the effect of male reproductive tactic on the
propensity of hybridization. In addition, we conducted a
second analysis for the 12 males to determine if their
reaction to the heterospecific female was different during
the different tactics. Each of the tactic changes included a
territorial tactic either during or after the initial female
presentation. However, because we only had 12 males
that changed their tactic, we pooled the two nonterritorial tactics for this analysis and compared male
reactions to the heterospecific female between territorial
and non-territorial tactics.
Females used in the experiments were caught from
two sympatric populations: all C. virgo females were
caught from the River Vispiläjoki (6214¢N, 2529¢E) and
all C. splendens females were caught from the River
Pitkäjoki (627¢N, 263¢E). In the field, females were kept
individually in small plastic containers in a cooler box. If
they had to overnight in the laboratory, they were kept
at +4.5 C. Each female was used in the experiment a
maximum of two times; when a female was used two
times, it was presented to males exhibiting different
tactics.
Statistical analyses
In analysing the reactions of males an analysis of
covariance (A N C O V A ) was used; a parametric analysis of
variance is appropriate also for rank transformed data
(Zar, 1996). In the A N C O V A the dependent variable was
male reaction to the heterospecific female (i.e. the
propensity to hybridize). Male mating tactic was entered
as a fixed factor, and the ornament (i.e. wing spot) size
and male age as covariates. The model was built to
consider all possible main effects and interaction terms
between the variables. The non-significant interaction
terms were removed from the model one by one starting
from the highest order interaction, that is the three-way
interaction and proceeding with the two-way interactions. The criterion for removal was that at each step the
least significant interaction was removed first. Removal
was stopped when the first significant independent
ª 2009 THE AUTHORS. J. EVOL. BIOL. 22 (2009) 2512–2518
JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Male tactics and hybridization propensity
Results
7
6
Propensity to hybridize
variable was established. Because of the interaction
between a factor and a covariate, the covariate (wing
spot size) was standardized to mean of zero and variance
of one to make the main effect of the tactic interpretable
and meaningful (Hendrix et al., 1982). All statistical
analyses were conducted with S P S S (version 14.0),
except non-parametric pairwise comparison for
Kruskall–Wallis test, which was calculated by hand
using formulas presented in Zar (1996). All statistical
tests were two-tailed.
2515
5
4
3
2
1
There was a significant interaction between male reproductive tactic and the ornament size of the male on the
propensity of C. splendens males to hybridize with C. virgo
females (Table 1; Fig. 1). A closer analysis revealed that
there was a positive relationship between ornament size
and the propensity of the male to hybridize in territorial
males (linear regression, y = )0.06 + 0.40x, n = 25,
P = 0.026, R2 = 0.20) and a negative relationship in
sneaker males (y = 14.34 – 0.70x, n = 17, P = 0.027,
R2 = 0.29). In floater males there was no relationship
(y = 3.26 + 0.06x, n = 20, P = 0.864, R2 < 0.01). However, there was heterogeneity in the error variances
across the tactics (Levene’s test F2, 59 = 8.05, P = 0.001).
As we can see from Fig. 1 the heterogeneity arises from
floater males having greater variance than the other two
tactics. If the analysis is run without the floater males the
error variances are no longer heterogeneous (Levene’s
test F1, 40 = 1.63, P = 0.209), and the interaction
between male tactic and ornament size is much stronger
(F1, 37 = 12.45, P = 0.001).
In addition to the interaction, the reproductive tactic
had a main effect on the propensity of C. splendens males
to hybridize with C. virgo females (Table 1). Territorial
males had greater propensity to hybridize than sneakers
or floaters (pairwise comparisons, LSD, P = 0.017 and
P = 0.003, respectively), but there was no difference
between sneakers and floaters (P = 0.606). During the
experiment we observed 12 males switching their tactic.
We compared the propensity of these 12 males to
hybridize with heterospecific females during both tactics
and these comparisons confirmed the above results:
Table 1 Analysis of covariance testing the effect of male tactic,
ornament (i.e. wing spot) size and age on the propensity of Calopteryx
splendens males to hybridize with C. virgo females.
Source
SS
df
MS
F
P
Tactic
Ornament size
Age
Tactic · ornament size
Error
33. 43
0.72
0.40
22.13
158.78
2
1
1
2
55
33.43
0.72
0.40
11.06
2.89
5.79
0.25
0.14
3.83
0.005
0.621
0.710
0.028
R2 = 0.25 (R2 = proportion of variance explained by the model).
0
9.0
11.0
13.0
15.0
Wing spot size (mm)
17.0
19.0
Fig. 1 Propensity of Calopteryx splendens males to hybridize with
C. virgo females in relation to his ornament size (i.e. wing spot size).
d — = territorial males, s - - - = sneaker males, h — - — = floater
males. Reactions of C. splendens males were ranked into seven
categories of increasing propensity of hybridization.
C. splendens males have a higher propensity to hybridize
when displaying territorial tactic than when displaying
non-territorial tactic (Wilcoxon test, Z = )2.038, n = 12,
P = 0.042).
From all individual daily observations of male reproductive tactic (nterritorial = 150, nsneaker = 47, nfloater =
122), we investigated whether there is ornament size or
age differences between males engaging in different
tactics. There was no difference in ornament size of
territorial, sneaker and floater males (one way A N O V A ,
F2, 316 = 0.16, P = 0.984). Instead, there was an age
difference between males of different reproductive tactics
(Kruskall–Wallis test, v2 = 9.99, df = 2, P = 0.007). Territorial males were most abundant at the age of three
days, while sneaker males were most abundant at the age
of 1 and 2 days, and floater males were most abundant at
the age of one day (non-parametric pairwise comparison,
territorial vs. sneaker males: Q = 2.177, 0.05 < P < 0.10,
territorial vs. floater males: Q = 2.854, P < 0.05 and
sneaker vs. floater males: Q = 0.093, P > 0.50). These
apparently small age differences between the tactics are
nevertheless likely to be biologically import since the
overall survival of mature males was on average only
5.5 ± 0.3 days (mean ± SE, n = 226). However, male age
had no effect on his propensity of hybridization
(Table 1).
Discussion
We hypothesised that male alternative reproductive
tactics combined with adaptive mating decisions can lead
to hybridization: individuals with inferior tactics might
be prone to hybridize to gain even some reproductive
success and fitness. However, our results were in stark
ª 2009 THE AUTHORS. J. EVOL. BIOL. 22 (2009) 2512–2518
JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
2516
K. TYNKKYNEN ET AL.
contrast to this hypothesis. It was the territorial
C. splendens males, i.e. males with the superior reproductive tactic, which had the greatest propensity to hybridize
with the heterospecific females. In addition, males which
changed their reproductive tactic also changed their
behaviour such that the propensity of hybridization was
greater when a male displayed the territorial tactic.
There are several kinds of possible costs for males from
hybridization. These include energetic costs of courtship,
risk to be predated during courtship, sperm depletion,
intruders to a territory while mating with a heterospecifics and thus fighting costs afterwards, and reduced
opportunity to mate with conspecifics females (see e.g.
Kotiaho, 2001; Kotiaho & Simmons, 2003; Peterson et al.,
2005). In our study species, there is a discrepancy
between number of observed matings between heterospecifics and number of observed hybrid offspring in the
wild, indicating that females are either not using the
heterospecific sperm or that the hybrids are partially
unviable (Tynkkynen et al., 2008a; see also Marshall
et al., 2002). Since low reproductive output seems likely
from matings between heterospecifics, the possible benefits from hybridization may be too small to allow the
adaptive hybridization to evolve. Therefore, there may
also be selection on C. splendens males to be discriminating and to avoid matings with heterospecifics. Selection
on males to avoid hybridization has been suggested to
occur in other systems as well (Waage, 1975; Peterson
et al., 2005). However, C. splendens males may also benefit
from courting C. virgo females because high courtship
activity may insure high reproductive success with
conspecific females; conspecific females appear to prefer
actively courting males (see Hooper & Siva-Jothy, 1997).
We found an interaction effect between the male
reproductive tactic and his ornament size on his propensity of hybridization. This interaction suggests, that in this
system hybridization may be a by-product of intraspecific
fluctuating selection on male mate discrimination within
an individual, which is dependent on male tactic and
ornament size. Indeed, in territorial C. splendens males,
there is a positive relationship and in sneaker males
negative relationship between ornament size and propensity of hybridization. Defending a territory is energetically expensive (Plaistow & Siva-Jothy, 1996), and
more ornamented territorial males are likely to have
more energy reserves than less ornamented males, as has
been observed in territorial males of another Calopterygid damselfly, Hetaerina americana (Contreras-Garduño
et al., 2006, 2008). By being less discriminating and
presenting courtship also to heterospecific females, territorial males may benefit through being more perceptible and thus attractive also for conspecifics females (see
Hooper & Siva-Jothy, 1997). In addition, it may be that
costs of courtship and mating with heterospecific females
are less for the more ornamented territorial males than
for the less ornamented territorial males. Thus, it seems
that in territorial males the cost:benefit-ratio of the
behaviour leading to mating with heterospecific females
may be negatively related to male ornament size, making
less ornamented territorial males more selective.
In contrast to territorial males, for sneaker C. splendens
males the relationship between the ornament size and
the probability of hybridization was negative: most
ornamented sneaker males avoided heterospecific
females, whereas least ornamented sneaker males were
not so discriminating. The sneaking tactic involves
stealing matings from the territorial males. Increasing
ornament size makes males more visible (Tynkkynen
et al., 2004; Svensson & Friberg, 2007), and is likely to
increase the risk of attack by the territorial males (see
Tynkkynen et al., 2004). Therefore, it seems that in
sneaker males the cost:benefit-ratio of the behaviour
leading to mating with heterospecific females may be
positively related to male ornament size, making more
ornamented sneaker males more selective.
In contrast to territorial and sneaker males, wing spot
size of floater males was not related to their propensity of
hybridization. This may be due to the mobile and less
hiding behaviour of floater males when compared to the
sneaker males (K. Tynkkynen, personal observation),
probably reducing the role of their ornament visibility
and thus likelihood of attacks from other males.
Males have been suggested to be able to allocate their
courting efforts strategically over available classes of
females when females differ in their value for males
(Rowell & Servedio, 2009). Such a strategic allocation
may give rise to a stable polymorphism in male mate
preference (Rowell & Servedio, 2009). Our results,
although from the context of interspecific interactions
rather than intraspecific interactions, are in agreement
with the above model because it is likely that heterospecific females are of lower value than conspecifics ones
(see Tynkkynen et al., 2008a). Our results suggest that
male C. splendens may strategically allocate courtship
towards heterospecific females depending on the tactic
the male is displaying and on his ornament size.
An alternative explanation for the greater propensity
of territorial males to hybridize with C. virgo females
could be that they have smaller residual reproductive
value than other males. This is because territorial
C. splendens males were older than non-territorial males.
This kind of increase in mating effort when a male
becomes older or when survival probability diminishes,
or so called ‘terminal investment’, has been reported in
other organisms (e.g. Candolin, 1999; Velando et al.,
2006; Weil et al., 2006). However, in our analysis age had
no effect on male propensity of hybridization, and thus
this explanation is unlikely in our case.
In conclusion, when a male changes his reproductive
tactic, his mate discrimination changes accordingly.
However, optimal behavior of a male is not depending
only on the tactic he is displaying, but also on the size
of his sexual ornaments. In other words, there is
fluctuating selection on male mate discrimination
ª 2009 THE AUTHORS. J. EVOL. BIOL. 22 (2009) 2512–2518
JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Male tactics and hybridization propensity
against heterospecific females depending simultaneously
on the ornament size and the reproductive tactic the
male has adopted. Indeed, in this system hybridization
may be a by-product of varying selection pressures
operating within C. splendens males. An important
implication of our results is that all individuals are not
equal in their propensity of hybridization. Consequently, depending on the relative number of individuals with different reproductive tactics, the prevalence
of hybrids may vary between populations. Given that
reproductive tactics are involved, the variation in
propensity of hybridization can influence the strength
of processes depending on frequency of hybridization,
such as the reinforcement of premating reproductive
isolation.
Acknowledgments
We thank K. Emily Knott for comments to manuscript,
Hanna Kokko for valuable discussion with us about the
topic, and Kari Nissinen and Harri Högmander from the
Department of Mathematics and Statistics in University
of Jyväskylä for statistical advice. The study was funded
by the Academy of Finland, Centre of Excellence in
Evolutionary Research, The Kuopio Naturalists’ Society,
Societas Biologica Fennica Vanamo and Societas pro
Fauna et Flora Fennica.
References
Askew, R.R. 1988. The Dragonflies of Europe. B. H & A. Harley Ltd,
Colchester.
Bel-Venner, M.C., Dray, S., Allainé, D., Menu, F. & Venner, S.
2008. Unexpected male choosiness for mates in a spider. Proc.
R. Soc. Lond. B 275: 77–82.
Byrne, P.G. & Rice, W.R. 2006. Evidence for adaptive male mate
choice in the fruitfly Drosophila melanogaster. Proc. R. Soc. Lond.
B 273: 917–922.
Candolin, U. 1999. The relationship between signal quality and
physical condition: is sexual signalling honest in the threespined stickleback? Anim. Behav. 58: 1261–1267.
Clutton-Brock, T. 2007. Sexual selection in males and females.
Science 318: 1882–1885.
Contreras-Garduño, J., Canales-Lazcano, J. & Córdoba-Aguilar,
A. 2006. Wing pigmentation, immune ability, fat reserves and
territorial status in males of the rubuspot damselfly, Hetaerina
americana. J. Ethol. 24: 165–173.
Contreras-Garduño, J., Buzatto, B.A., Serrano-Meneses, M.A.,
Nájera-Cordero, K. & Córdoba-Aguilar, A. 2008. The size of
the red wing spot of the American rubyspot as a heightened
condition-dependent ornament. Behav. Ecol. 19: 724–732.
Corbet, P.S. 1999. Dragonflies: Behaviour and Ecology of Odonata.
Harley Books, Essex.
Cordero, A. 1999. Forced copulations and female contact
guarding at a high male density in a Calopterygid damselfly.
J. Insect Behav. 12: 27–37.
Córdoba-Aguilar, A. 2002. Wing pigmentation in territorial male
damselflies, Calopteryx haemorrhoidalis: a possible relation to
sexual selection. Anim. Behav. 63: 759–766.
2517
Coyne, J.A. & Orr, H.A. 2004. Speciation. Sinauer Associates,
Sunderland, MA.
Dobzhansky, T. 1951. Genetics and the Origin of Species, 3rd edn.
Columbia University Press, New York.
Forsyth, A. & Montgomerie, R.D. 1987. Alternative reproductive
tactics in the territorial damselfly Calopteryx maculata: sneaking
by older males. Behav. Ecol. Sociobiol. 21: 73–81.
Frisch, A. & Van Herwerden, L. 2006. Field and experimental
studies of hybridization between coral trouts, Plectropomus
leopardus and Plectropomus maculatus (Serranidae), on the Great
Barrier Reef, Australia. J. Fish Biol. 68: 1013–1025.
Garcia-Vazquez, E., Moran, P., Perez, J., Martinez, J.L,
Izquierdo, J.I., de Gaudemar, B. & Beall, E. 2002. Interspecific
barriers between salmonids when hybridisation is due to
sneak mating. Heredity 89: 288–292.
Grether, G.F. 1996. Sexual selection and survival selection on
wing coloration and body size in the rubyspot damselfly
Hetaerina americana. Evolution 50: 1939–1948.
Gross, M.R. 1996. Alternative reproductive strategies and tactics:
diversity within sexes. Trends Ecol. Evol. 11: 92–98.
Hendrix, L.J., Carter, M.W. & Scott, D.T. 1982. Covariance
analyses with heterogeinity of slopes in fixed models. Biometrics 38: 641–650.
Higgie, M., Chenoweth, S. & Blows, M.W. 2000. Natural
selection and the reinforcement of mate recognition. Science
290: 519–521.
Hooper, R.E. & Siva-Jothy, M.T. 1997. ‘‘Flybys’’: A prereproductive remote assessment behavior of female Calopteryx
splendens xanthostoma (Odonata: Calopterygidae). J. Insect
Behav. 10: 165–175.
Jennings, M.J. & Philipp, D.P. 2002. Alternative mating tactics in
sunfishes (Centrarchidae): a mechanism for hybridization?
Copeia 2002(4): 1102–1105.
Kotiaho, J.S. 2001. Costs of sexual traits: a mismatch between
theoretical considerations and empirical evidence. Biol. Rev.
76: 365–376.
Kotiaho, J.S. & Simmons, L.W. 2003. Longevity cost of reproduction for males but no longevity cost of mating or courtship
for females in the male-dimorphic dung beetle Onthophagus
binodis. J. Insect Physiol. 49: 817–822.
Lamb, T. & Avise, J.C. 1986. Directional introgression of
mitochondrial DNA in a hybrid population of treefrogs: the
influence of mating behaviour. Proc. Nat. Acad. Sci. USA 83:
2526–2530.
Mallet, J. 2005. Hybridization as invasion of the genome. Trends
Ecol. Evol. 20: 229–237.
Malmos, K.B., Sullivan, B.K. & Lamb, T. 2001. Calling behavior
and directional hybridization between two toads (Bufo microscaphus · B. woodhousii) in Arizona. Evolution 55: 626–630.
Marshall, J.L., Arnold, M.L. & Howard, D.J. 2002. Reinforcement: the road not taken. Trends Ecol. Evol. 17: 558–563.
Nuechterlein, G.L. & Buitron, D. 1998. Interspecific mate choice
by late-courting male western grebes. Behav. Ecol. 9: 313–
321.
Pajunen, V.I. 1966. Aggressive behaviour and territoriality in a
population of Calopteryx virgo L. (Odon., Calopterygidae). Ann.
Zool. Fennici 3: 201–214.
Parker, G.A. 1983. Mate quality and mating decisions. In: Mate
Choice (P. Bateson, ed), pp. 141–164. Cambridge University
Press, Cambridge.
Parker, G.A. & Partridge, L. 1998. Sexual conflict and speciation.
Phil. Trans. R. Soc. Lond. B 353: 261–274.
ª 2009 THE AUTHORS. J. EVOL. BIOL. 22 (2009) 2512–2518
JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
2518
K. TYNKKYNEN ET AL.
Peterson, M.A., Honchak, B.M., Locke, S.E., Beeman, T.E.,
Mendoza, J., Green, J., Buckingham, K.J., White, M.A. &
Monsen, K.J. 2005. Relative abundance and the speciesspecific reinforcement of male mating preference in the
Chrysochus (Coleoptera: Chrysomelidae) hybrid zone. Evolution
59: 2639–2655.
Pfennig, K.S. 2007. Facultative mate choice drives adaptive
hybridization. Science 318: 965–967.
Plaistow, S.J. 1997. Variation in non-territorial behaviour in
male Calopteryx splendens xanthostoma (Charpentier) (Zygoptera: Calopterygidae). Odonatologica 26: 171–181.
Plaistow, S. & Siva-Jothy, M.T. 1996. Energetic constraints and
male mate-securing tactics in the damselfly Calopteryx splendens
xanthostoma (Charpentier). Proc. R. Soc. Lond. B 263: 1233–1238.
Randler, C. 2002. Avian hybridization, mixed pairing and female
choice. Anim. Behav. 63: 103–109.
Rantala, M.J., Koskimäki, J., Taskinen, J., Tynkkynen, K. &
Suhonen, J. 2000. Immunocompetence, developmental stability and wingspot size in the damselfly Calopteryx splendens L.
Proc. R. Soc. Lond. B 267: 2453–2457.
Reyer, H.-U. 2008. Mating with wrong species can be right.
Trends Ecol. Evol. 23: 289–292.
Rowell, J.T. & Servedio, M.R. 2009. Gentlemen prefer blondes:
The evolution of mate preference among strategically allocated males. Am. Nat. 173: 12–25.
Ryan, M.J. & Wagner, W.E. Jr 1987. Asymmetries in mating
preferences between species: female swordtails prefer heterospecific males. Science 236: 595–597.
Sætre, G.-P., Moum, T., Bures, S., Kral, M., Adamjan, M. &
Moreno, J. 1997a. A sexually selected character displacement
in flycatchers reinforces premating isolation. Nature 387: 589–
592.
Sætre, G.-P., Král, M. & Bures, S. 1997b. Differential species
recognition abilities of males and females in a flycatcher
hybrid zone. J. Avian Biol. 28: 259–263.
Servedio, M.R. 2007. Male versus female mate choice: sexual
selection and the evolution of species recognition via reinforcement. Evolution 61: 2772–2789.
Servedio, M.R. & Lande, R. 2006. Population genetic models of
male and mutual mate choice. Evolution 60: 674–685.
Siva-Jothy, M.T. 1999. Male wing pigmentation may affect
reproductive success via female choice in a calopterygid
damselfly (Zygoptera). Behaviour 136: 1365–1377.
Siva-Jothy, M.T. 2000. A mechanistic link between parasite
resistance and expression of a sexually selected trait in a
damselfly. Proc. R. Soc. Lond. B 267: 2523–2527.
Siva-Jothy, M.T. & Hooper, R.E. 1995. Disposition and genetic
diversity of stored sperm in the damselfly Calopteryx splendens
xanthostoma (Charpentier). Proc. R. Soc. Lond. B 259: 313–318.
Svensson, E.I. & Friberg, M. 2007. Selective predation on wing
morphology in sympatric damselflies. Am. Nat. 170: 101–112.
Svensson, E.I., Karlsson, K., Friberg, M. & Eroukhmanoff, F.
2007. Gender differences in species recognition and the
evolution of asymmetric sexual isolation. Curr. Biol. 17:
1943–1947.
Tomkins, J.L. & Brown, G.S. 2004. Population density drives the
local evolution of a threshold dimorphism. Nature 431: 1099–
1103.
Tomkins, J.L. & Hazel, W. 2007. The status of the conditional evolutionarily stable strategy. Trends Ecol. Evol. 22:
522–527.
Tynkkynen, K., Rantala, M.J. & Suhonen, J. 2004. Interspecific
aggression and character displacement in the damselfly Caloperyx splendens. Evol. Biol. 17: 759–767.
Tynkkynen, K., Kotiaho, J.S., Luojumäki, M. & Suhonen, J.
2005. Interspecific aggression causes negative selection on
sexual characters. Evolution 59: 1838–1843.
Tynkkynen, K., Grapputo, A., Kotiaho, J.S., Rantala, M.J.,
Väänänen, S. & Suhonen, J. 2008a. Hybridization in Calopteryx damselflies: the role of males. Anim. Behav. 75: 1431–
1439.
Tynkkynen, K., Kotiaho, J.S. & Svensson, E.I. 2008b. Interspecific interactions and premating reproductive isolation. In:
Dragonflies: Model Organisms for Ecological and Evolutionary
Research (A. Cordoba-Aguilar, ed), pp. 139–152. Oxford
University Press, Oxford.
Veen, T., Borge, T., Griffith, S.C., Sætre, G.-P., Bures, S.,
Gustafsson, L. & Sheldon, B.C. 2001. Hybridization and
adaptive mate choice in flycatchers. Nature 411: 45–50.
Velando, A., Drummond, H. & Torres, R. 2006. Senescent birds
redouble reproductive effort when ill: confirmation of the
terminal investment hypothesis. Proc. R. Soc. Lond. B 273:
1443–1448.
Waage, J.K. 1975. Reproductive isolation and the potential for
character displacement in the damselflies, Calopteryx maculata
and C. aequabilis (Odonata: Calopterygidae). Syst. Zool. 24:
24–36.
Weil, Z.M., Martin, L.B., Workman, J.L. & Nelson, R.J. 2006.
Immune challenge retards seasonal reproductive regression in
rodents: evidence for terminal investment. Biol. Lett. 2: 393–
396.
Wirtz, P. 1999. Mother species–father species: unidirectional
hybridization in animals with female choice. Anim. Behav. 58:
1–12.
Zar, J.H. 1996. Biostatistical Analysis, 3rd edn. Prentice Hall, Upper
Saddle River.
Received 5 June 2009; accepted 25 September 2009
ª 2009 THE AUTHORS. J. EVOL. BIOL. 22 (2009) 2512–2518
JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY