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Intrasexual selection favors an immune-correlated color ornament in a dragonfly


Abstract and Figures

Sexual signaling is predicted to shape the evolution of sex-specific ornamentation, and establishing the costs and benefits of ornamentation and the information that ornamentation provides to receivers is necessary to evaluating this adaptive function. Here, we assessed the adaptive function of a common color ornament in insects, melanin wing ornamentation, using the dragonfly Pachydiplax longipennis. We hypothesized that greater ornamentation would improve territory holding success by decreasing aggression that males receive from territorial rivals, but that more ornamented males may have shorter lifespans. Using mark-recapture field observations, we found that more ornamented males had greater territory holding success, and that viability selection did not act on wing melanization. We then compared the aggression of territorial rivals to decoy males before and after experimentally augmenting wing melanization, finding that males significantly reduced aggression following the manipulation. We next hypothesized that wing melanization would signal fighting ability to territorial rivals by reflecting condition via investment in the costly melanin-synthesis pathway. We observed a positive relationship between ornamentation and the likelihood of winning territorial disputes, suggesting that wing melanization provides information about fighting ability to rivals. We also found a positive relationship between melanin-based immune defense and ornamentation, supporting a link between the signal and condition. We conclude that wing melanization is a condition-related signal of fighting ability, and suggest that this may be a common mechanism promoting the evolution of melanin ornamentation. This article is protected by copyright. All rights reserved.
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Intrasexual selection favours an immune-correlated colour
ornament in a dragonfly
Department of Biology, Case Western Reserve University, Cleveland, OH, USA
malemale competition;
sexual selection;
sexual signal;
viability selection.
Sexual signalling is predicted to shape the evolution of sex-specific orna-
mentation, and establishing the costs and benefits of ornamentation and the
information that ornamentation provides to receivers is necessary to evalu-
ating this adaptive function. Here, we assessed the adaptive function of a
common colour ornament in insects, melanin wing ornamentation, using
the dragonfly Pachydiplax longipennis. We hypothesized that greater orna-
mentation would improve territory-holding success by decreasing aggression
that males receive from territorial rivals, but that more ornamented males
may have shorter lifespans. Using markrecapture field observations, we
found that more ornamented males had greater territory-holding success
and that viability selection did not act on wing melanization. We then com-
pared the aggression of territorial rivals to decoy males before and after
experimentally augmenting wing melanization, finding that males signifi-
cantly reduced aggression following the manipulation. We next hypothe-
sized that wing melanization would signal fighting ability to territorial rivals
by reflecting condition via investment in the costly melanin synthesis path-
way. We observed a positive relationship between ornamentation and the
likelihood of winning territorial disputes, suggesting that wing melanization
provides information about fighting ability to rivals. We also found a posi-
tive relationship between melanin-based immune defence and ornamenta-
tion, supporting a link between the signal and condition. We conclude that
wing melanization is a condition-related signal of fighting ability and suggest
that this may be a common mechanism promoting the evolution of melanin
Sex-specific ornamentation is predicted to affect repro-
ductive success through sexual signalling (Darwin,
1871; Andersson, 1994; Maynard Smith & Harper,
2003). Specifically, sexual signals in animals function-
ally shape mating success by providing information
about the individual to rivals or potential mates,
thereby directly moderating the outcomes of beha-
vioural interactions over territories or copulation oppor-
tunities (Maynard Smith & Harper, 2003; Searcy &
Nowicki, 2005; Lailvaux & Irschick, 2006). For exam-
ple, sex-specific ornamentation may influence
competition over territories by signalling the bearer’s
fighting ability to rivals and facilitating the resolution of
disputes quickly and without injury (Maynard Smith &
Harper, 2003; Arnott & Elwood, 2009). As sexual selec-
tion should therefore strongly favour individuals with
large, conspicuous ornaments, the adaptive value and
evolutionary maintenance of signal function crucially
depends on its ability to convey reliable information
(Maynard Smith & Harper, 2003). Understanding the
adaptive function of sex-specific ornaments thus neces-
sitates directly evaluating the relationship between
ornamentation and components of reproductive suc-
cess, as well as characterizing the information being sig-
nalled to rivals and potential mates. However,
investigations of the adaptive function of sex-specific
ornamentation rarely integrate both approaches (Lail-
vaux & Irschick, 2006).
Correspondence: Michael P. Moore, Department of Biology, Case Western
Reserve University, 2080 Adelbert Road, Cleveland, OH 44106, USA.
Tel.: +1 216 368 2177; fax: +1 216 368 4672;
doi: 10.1111/jeb.12953
Melanin is a phylogenetically widespread pigment
underlying sex-specific ornaments in many animals, yet
its role in sexual signalling has been relatively contro-
versial (Stoehr, 2006; Roulin, 2016). While any positive
covariance between ornamentation and aspects of con-
dition may promote sexual signalling functions, insects
use the melanin synthesis enzymatic pathway not only
for colouration but also for directly mounting immune
responses and repairing wounds (Schmid-Hempel,
2005; Siva-Jothy et al., 2005), providing a strong proxi-
mate link by which ornamentation may intrinsically
reflect aspects of condition (Hill, 2011; Roulin, 2016).
For instance, allocation trade-offs of melanin precursors
(e.g. tyrosine) may promote signal reliability such that
only males in the best condition can invest precursors
in both immunocompetence and ornamentation (i.e. Y-
shaped acquisitionallocation model; Stoehr, 2006; Hill,
2011). Additionally, the high energetic costs of melanin
synthesis may maintain signal reliability (e.g. Moret &
Schmid-Hempel, 2000; Fedorka et al., 2004; Schwarzen-
bach & Ward, 2006), whereby only males with the
greatest energetic reserves can activate and maintain
high overall levels of melanin synthesis (Gonz
toyo & C
ordoba-Aguilar, 2012). As a consequence of
this proximate link, melanin ornamentation may often
reliably signal information about an individual’s condi-
tion, directly moderating the outcomes of interactions
with rivals or potential mates, and causally shaping
reproductive outcomes (Hooper et al., 1999; Siva-Jothy,
2000; Wittkopp & Beldade, 2009). However, the rela-
tively few tests of this sexually selected function of mel-
anin colouration in insects have been equivocal
(Lawniczak et al., 2007; Punzalan et al., 2008b; Izzo &
Tibbetts, 2012), and its explicit function in intrasexual
selection has received little attention in particular.
Given this, and the growing recognition of similar
pleiotropic effects in invertebrates and vertebrates
(Ducrest et al., 2008; Roulin, 2016), studies that directly
estimate phenotypic selection on, and the information
content of, melanin ornaments remain critical to
understanding the adaptive function of this widespread
Using the sexually dimorphic dragonfly, Pachydiplax
longipennis (Burmeister), we tested the adaptive
function of a common melanin ornament in arthro-
pods, wing melanization (Fig. 1). Similar to damselflies
that display red wing ornaments (e.g. Hetaerina ameri-
cana, Grether, 1996b), we hypothesized that wing
melanization improves territory-holding success, a vital
component of mating success in odonates (reviewed in
Koenig, 2008; Suhonen et al., 2008), by decreasing
energetically costly and potentially injurious aggressive
interactions with rivals. We also predicted that males
with greater wing melanization would be more suscep-
tible to predators and have higher mortality (e.g.
Grether, 1997; Kuchta & Svensson, 2014) and therefore
have shorter reproductive lifespans. We further hypoth-
esized that wing melanization signals fighting ability to
rivals by proximately reflecting energetic reserves via
the shared melanin synthesis pathway. We thus pre-
dicted that ornamentation would be positively associ-
ated with the likelihood of winning territorial contests
and with melanin-based immune defence.
Materials and methods
Study system
Pachydiplax longipennis (Burmeister) is a medium-sized
dragonfly distributed broadly across North America.
Females are brown with longitudinal yellow stripes,
whereas males have blue abdomens and, in the eastern
extent of their range where our study was conducted,
express melanin colouration on the distal portion of
their wings (Fig. 1; Paulson, 2012). Detailed descriptions
of the mating system can be found elsewhere (Johnson,
1962; Robey, 1975; Fried & May, 1983; Sherman,
1983). Briefly, on sunny days between mid-June and
early August, males arrive at the pond between 0800
and 0900 EST and defend territories on emergent vege-
tation around the perimeter of the pond until approxi-
mately 1530 EST. Males spend time in their territories
perching on emergent vegetation and patrolling. Males
frequently encroach upon rivals’ territories, engaging in
aggressive disputes where the winner retains the terri-
tory and the loser either searches for a new territory or
leaves the pond entirely. Once males have established at
a pond for breeding, they rarely disperse (McCauley,
(a) (b)
Fig. 1 Wings of two mature males with
relatively low (a) and high (b) wing
melanization. Note that the
pigmentation at the base of the wing is
less variable among males and is also
expressed in females. Pigmentation in
the distal portion of the wing is
sexually dimorphic and highly variable
among males.
2010). Females arrive at the pond throughout the day,
mate with a male, and then oviposit in his territory
while he hovers above her (Sherman, 1983). There are
seldom more than one or two females on a pond at a
given time, and copulations are very short, rarely lasting
more than 2 min (Sherman, 1983; Paulson, 2012).
Study site, population monitoring and phenotypic
We conducted this study at a small (perime-
ter =140.2 m) research pond at Case Western Reserve
University’s Squire Valleevue Farm (Hunting Valley,
OH, USA). Males defend territories along two regions of
emergent vegetation on opposite sides of the pond (pri-
marily Typha sp.; 13.8 and 35.7 m, respectively). We
captured males and uniquely marked their abdomens
with four dots of acrylic paint (randomly chosen from
among five different colours; Anderson et al., 2011).
We kept males on ice in plastic bags before processing
to slow their movement and facilitate safe handling
(McCauley, 2010). To assess variation in wing
melanization, body size and wing size (two traits associ-
ated with odonate reproductive success; Koenig, 2008),
we took digital photographs (Canon G15; Canon, USA,
Inc., Lake Success, NY, USA) of each male’s wings and
body. We standardized the lighting conditions by taking
pictures of males against a standard white background
(DGK Color Tools
; Fig. 1) in a dark box that excluded
ambient light. We attempted to include only males with
little wing wear and fully developed abdomen coloura-
tion to minimize potential variation due to age differ-
ences (Grether, 1996a; Contreras-Gardu~
no et al., 2008;
McCauley, 2010). In two cases, we recaptured and
reprocessed males that had not developed their full
abdomen colouration. Following processing, we
released males from a common location approximately
10 m from the pond. While several ponds were within
the average dispersal distance of breeding males
(430 m, McCauley, 2010), no marked males were ever
observed at any of these other ponds.
We quantified all traits from digitized photographs in
ImageJ (Rasband, 2012). Body size was calculated as
the distance (mm) from the front of the head to the
tips of the cerci. Wing area was scored as the total area
) of all four wings. Wing area and body size are
highly correlated (r=0.834, P<0.001), and thus, we
calculated relative wing size by taking the standardized
residuals from the linear regression of body size on total
wing area. To quantify the extent of wing melanization,
we identified the highest mean grey value (0255,
0=most opaque; 255 =most transparent) in ImageJ of
the pigmented portion of each wing (i.e. least darkly
pigmented), converted the photograph to binary black
and white with this value as the threshold for black
and calculated the size (mm
) of the digitized
black area. Wing melanization was then estimated as
the proportion of the total wing area that was pig-
mented. To ensure the consistency of measurements,
we calculated repeatability by randomly resampling a
subset of 16 individuals and blindly rescoring each trait.
The repeatability was high for all traits (all R>0.99, all
>259.2, all P<0.001; Lessells & Boag, 1987).
We evaluated the phenotypic variation in the popula-
tion by considering how wing melanization varied with
body size and relative wing size using Pearson’s pro-
duct-moment correlation coefficients, with individuals
included as the unit of replication.
Do territory-holding success and longevity vary with
wing melanization?
We examined the fitness costs and benefits of our focal
traits using behavioural observations of marked individ-
uals. One observer (MPM) continuously circled the
pond during the peak activity hours (09001530 EST)
on all sunny days between 23 June and 24 July
(n=18), recording each marked male’s location, terri-
torial behaviour and the time. On most days, approxi-
mately 50% of the territorial males at the pond were
marked. Territorial males exhibit characteristic, unam-
biguous behaviours, such as perching in an obelisk
position or chasing other males (see Johnson, 1962;
Robey, 1975). We quantified a male’s within-day terri-
torial tenure as the amount of time (minutes) that it
was territorial during that day. Males that were sighted
only once were assigned a territorial tenure of zero
minutes. We could not directly evaluate mate choice as
we observed only four marked males copulating with
females. However, as females choose among territorial
males, a male’s territorial tenure is strongly correlated
with mating success (Sherman, 1983).
We assessed how daily territorial tenure varied with
wing melanization, body size and relative wing size
using a generalized linear mixed-effects model with a
negative binomial error distribution to account for
overdispersion. We did not test interactive effects
among traits because models including these terms did
not converge, and preliminary visual assessment of the
interactions suggested that there were no strong effects
between any combinations of the traits. To account for
multiple territorial tenures of the same male among
days, and the nonindependence among males within a
given day, we included random intercepts for individ-
ual identity and observation date, respectively. As terri-
torial tenures of zero minutes were potentially
misidentified males, we excluded these observations
from analyses. However, our results are qualitatively
robust to their inclusion. Using individuals’ daily terri-
torial tenures, as opposed to total time spent defending
a territory over the flight season, reduces bias resulting
from variation in longevity (Hamon, 2005).
We evaluated how wing melanization, body size and
relative wing size varied with minimum-estimated
longevity using a generalized linear model with a
Sexual selection on dragonfly ornamentation 3
quasipoisson error distribution to account for overdis-
persion. Each male’s minimum-estimated longevity
(hereafter: ‘longevity’) was calculated as the number of
days between marking and the last day it was observed.
As we conducted field observations regularly through
the end of the flight period, this sample of days reflects
a realistic period over which viability selection may act
through differences in longevity. This metric is com-
monly used in odonate studies (e.g. Grether, 1996a;
ordoba-Aguilar, 2002) and is relatively robust to low
resighting probabilities (Waller & Svensson, 2016). We
only included males marked prior to 5th July to control
for differences in the available number of days between
marking date and the end of the flight season. We only
considered males that were observed at least twice after
marking to ensure that we exclusively included resident
To estimate the strengths of intrasexual and viability
selection on our focal traits, we used standard regres-
sion techniques to calculate selection gradients (Lande
& Arnold, 1983), dividing each individual’s fitness com-
ponent (territorial tenure or longevity) by the popula-
tion mean (i.e. relative fitness) and converting
phenotypic values to mean of 0 and unit variance. To
compare overall fitness variation acting through intra-
sexual selection vs. viability selection, we also calcu-
lated the opportunities for sexual and viability selection
by dividing the variance in each fitness component by
its squared mean (Arnold & Wade, 1984).
Do males with greater wing melanization receive less
aggression from territorial rivals?
To assess whether wing melanization has direct effects
on the aggression received from rival males, we pre-
sented decoys (previously frozen males) to territorial
males, experimentally augmented the ornamentation of
the decoys, presented them to new males and com-
pared the aggression received before and after the
experimental manipulation (see also Anderson &
Grether, 2010; Guillermo-Ferreira et al., 2015). We
tethered decoys to a 2-m aluminium pole using clear
nylon line (diameter =0.18 mm), and presented them
to territorial males. Typical of natural encounters
between rivals (Suhonen et al., 2008; McCauley, 2010),
males engaged the decoys by aggressively making
direct, physical contact multiple times (mean number
of strikes SD =4.4 5.1) over short durations
(mean number of seconds SD =6.2 4.6). For each
presentation, we evaluated the following: whether the
territorial male engaged the decoy (‘engagement’, y/n);
the time between the territorial male engaging the
decoy and returning to a perch in its territory (‘engage-
ment duration’, seconds); how many times it struck the
decoy (‘strikes’, n); and the number of strikes per sec-
ond (‘aggression rate’, strikes per second). After pre-
senting the decoy to several different territorial males
(median: 4, range: 25), we augmented the
ornamentation by homogenously colouring the wings
distally from the nodus (Fig. S2) with a felt-tip marker
chosen to approximate the natural colour (Crayola
Cuppa’ Cappucino;sensu Anderson & Grether, 2010;
Guillermo-Ferreira et al., 2015). This degree of orna-
mentation is within the natural phenotypic range. We
then presented the decoys to a different set of territorial
males and again evaluated the interactions. While the
same territorial males were often presented multiple
decoys, many of these males were presented post-
manipulation decoys before premanipulation decoys,
and thus, any observed effects of the manipulation on
territorial male aggression are not confounded with ter-
ritorial males becoming acclimated to the decoys.
We compared interactions before and after the
manipulation using mixed-effects models with decoy
identity as a random effect to account for multiple pre-
sentations of the same decoy to the different males. For
error distributions, we specified the binomial for
engagement, negative binomial for number of strikes
and gaussian for engagement duration and aggression
rate. Engagement duration was natural log-transformed
to improve normality of the residuals. Significance was
assessed with likelihood ratio tests of models with and
without the fixed effect for generalized linear mixed-
effects models and F-tests with the KenwardRoger
degrees of freedom approximation for linear mixed-
effects models (Kenward & Roger, 1997).
Is wing melanization associated with fighting ability?
To assess the potential for wing melanization to signal
fighting ability to territorial rivals, we observed natu-
rally occurring, aggressive interactions (e.g. chasing,
striking) between males during the field observations
described above. We defined the winner of a territorial
contest as the male that succeeded in forcing the other
male out of the territory. Many contests included
marked males, and we attempted to capture all
unmarked males from contests. However, as contest
losers frequently fly to another location on the pond or
off the pond altogether, we rarely knew the phenotypic
values of both males in a contest.
We analysed the likelihood of winning a territorial
contest using a generalized linear mixed-effects model
with a binomial error distribution and contest outcome
(win =1, lose =0) fitted as the response variable. We
included wing melanization, body size and relative wing
size as fixed effects. To account for repeated measures of
some individuals across disputes, and the nonindepen-
dence of two individuals in the same contest when both
were known, we included random intercepts for both
individual and contest identity, respectively.
Does wing melanization correlate with melanin-based
immune responses?
To evaluate whether wing melanization proximately
signals an individual’s condition via investment in the
shared melanin synthesis pathway (sensu Siva-Jothy,
2000), we considered the relationship between a male’s
wing melanization and its ability to mount a melanin-
based immune response. We captured and assayed the
melanin-based immune responses of 33 territorial males
over 2 days (28 July and 3 August). To assay immuno-
competence, we inserted a piece of sterilized nylon
monofilament (mean length SD =2.70 0.38 mm,
diameter =0.18 mm) into the body cavity dorsally
between the fifth and sixth abdominal segments and
allowed the males’ immune systems to react to it for
24 h. A pilot study indicated that 24 h provided the
strongest and most variable immune responses in this
species (M. P. Moore, unpublished). During this period,
males were kept in plastic bags in a dark climate cham-
ber set to 8.2 °C. While this treatment may have slo-
wed the rate of melanin immune responses, it was
necessary to prevent adults from injuring themselves
during or after the surgical implantation, and we do
not expect that any temperature effect will have differ-
entially affected males with different phenotypes. We
then dissected out the implants and stored them in a
freezer set to 22.8 °C. In four cases, the implant fell
out or was accidentally inserted into the midgut, and
these males were not considered further.
We quantified the melanin-based immune responses
from digitized photographs of the implants. Using a dis-
secting microscope with a bright field background, we
took one photograph of the implant, rotated the
implant 90°and then took another photograph. In
every photograph, we also had a nylon monofilament
that was not inserted into any males as a negative con-
trol. We used ImageJ to assess the mean grey values
(0 =opaque, 255 =transparent) of each implant. To
calculate an immune response score for each male, we
subtracted the mean grey values of the implant from
the control nylon for each picture and averaged the
two pictures. Higher scores indicate a darker implant
and therefore a stronger melanin-based immune
response, and previous work indicates this standard
technique reflects resistance to naturally occurring
pathogens (Rantala & Roff, 2007). Using the procedure
described above (see also Lessells & Boag, 1987), the
repeatability of this metric was high (R=0.995,
=404.00, P<0.001).
We used a linear model to consider how immune
response scores varied with wing melanization, body
size and their interaction. To account for potential vari-
ation between the two dates when males were cap-
tured, we also initially included date and its
interactions in the model. As these interactions were
not significant (all F<1.75, P>0.201), we removed
them from the model and retested effects. The immune
score from one very large male was an outlier and was
not included in the analysis to improve the normality
of model residuals. However, our results are qualita-
tively robust to its inclusion.
Statistical analyses
All statistical analyses were conducted using R v. 3.1.2
(R Development Core Team, 2014). Mixed-effects mod-
els were fit using the ‘lme4’ package (Bates et al.,
2014). To account for large scaling differences among
three focal phenotypes, wing melanization, body size
and relative wing size were z-transformed for all analy-
ses (Schielzeth, 2010). All model parameter estimates
and selection gradients are reported as estimate SE.
Phenotypic variation
We first assessed the phenotypic variation of males in
our population. The mean body size SD of males was
38.06 2.18 mm, and the mean wing melaniza-
tion SD was 0.41 0.09 (proportion of melanized
win area; n=115). There was no relationship between
body size and wing melanization (r=0.090,
=0.96, P=0.339; Fig. S1a), or between relative
wing size and wing melanization (r=0.143,
=1.54, P=0.126; Fig. S1b).
Do territory-holding success and longevity vary with
wing melanization?
In total, we observed 126 territorial tenures across 45
males (mean SD per individual: 2.8 2.2 tenures),
with a mean tenure SD of 104.9 84.2 min. Males
with greater wing melanization had longer territorial
tenures (0.348 0.090; v
=13.99, d.f. =1, P=0.002;
Fig. 2). In contrast, territorial tenure did not vary with
body size (0.023 0.077; v
=0.09, d.f. =1,
P=0.767) or relative wing size (0.057 0.088;
=0.43, d.f. =1, P=0.515). Overall, the opportunity
for intrasexual selection was 0.707, and the estimated
strength of intrasexual selection on wing melanization
was relatively strong (b=0.326 0.104; c.f. King-
solver et al., 2012). We report nonsignificant intrasex-
ual selection gradients in Table S1.
Of the 24 males included in the longevity analyses,
the mean longevity SD was 17.4 5.4 days. Longev-
ity was not associated with wing melanization
(0.078 0.066, v
=1.43, d.f. =1, P=0.232), body
size (0.096 0.079, v
=1.49, d.f. =1, P=0.222) or
relative wing size (0.022 0.093, v
=0.05, d.f. =1,
P=0.817). Overall, the opportunity for viability selec-
tion was 0.097, and we report the nonsignificant viabil-
ity selection gradients in Table S1.
Do males with greater wing melanization receive
less aggression from territorial rivals?
Regardless of experimental treatment, decoys were
equally likely to be engaged by territorial males (before
Sexual selection on dragonfly ornamentation 5
vs. after: 0.719 0.479, v
=2.31, d.f. =1, P=0.129).
However, engagement durations were shorter following
the manipulation (0.429 0.201, F
P=0.040). Similarly, decoys received fewer strikes
(0.951 0.367, v
=6.12, d.f. =1, P=0.0134;
Fig. 3a) and lower aggression rates (0.441 0.121,
=12.98, P<0.001; Fig. 3b) after augmenting the
decoy’s ornamentation.
Is wing melanization associated with fighting
We observed 155 territorial contests (94 winners, 73
losers; mean contests SD per individual: 2.8 3.1).
Males with greater wing melanization (0.484 0.181;
=6.50, d.f. =1, P=0.011) and larger body sizes
(0.433 0.176; v
=5.39, d.f. =1, P=0.020) were
more likely to win contests (Fig. 4). Relative wing size
was not associated with the probability of winning con-
tests (0.213 0.166; v
=1.72, d.f. =1, P=0.189).
Does wing melanization correlate with melanin-
based immune responses?
Immune response scores increased with wing melaniza-
tion and marginally decreased with body size (Table 1).
Immune response scores were also marginally different
between the two capture dates (Table 1).
We investigated the adaptive function of melanin orna-
mentation in the sexually dimorphic dragonfly,
P. longipennis. Following patterns in damselflies with
red wing ornaments (Grether, 1996b), we hypothesized
that greater wing melanization would improve terri-
tory-holding success by decreasing aggression that
males receive from territorial rivals, but that benefit
may come at the cost of a shorter reproductive lifespan
(Grether, 1997). We also hypothesized that wing
melanization would signal fighting ability to territorial
rivals by proximately reflecting condition via invest-
ment in the costly melanin synthesis pathway (Hooper
et al., 1999; Rantala et al., 2000; Siva-Jothy, 2000).
Overall, our results provide broad support for the
hypothesized adaptive function of male wing melaniza-
tion as a sexual signal of fighting ability to territorial
Male fitness is determined by the combined effects of
intrasexual, intersexual and viability selection (Arnold
& Wade, 1984; Hamon, 2005). Intrasexual selection via
territorial occupancy is crucial to male reproductive
success in territorial odonates (Moore, 1990; Grether,
1996b) and especially in P. longipennis (Sherman,
1983). Among the traits considered, only wing
melanization improved territory-holding success
−2 −1 0 1
Wing melanization [z−transformed]
Territorial tenure (min)
Fig. 2 Territorial tenure increased with wing melanization. Each
point represents the duration of time within a day that an
individual held a territory, and points are jittered horizontally by
0.05 to improve visual clarity. The regression line is fitted from the
mixed-effects model reported in the Results, and wing
melanization was z-transformed to improve scaling among
explanatory variables.
Strikes (n)
Before After
Aggression rate (strikes * s–1)
Fig. 3 Territorial males exhibited reduced aggression (a: total
number of strikes; b: number of strikes per second) to decoy males
following experimental increase of wing melanization. Each circle
represents a presentation of a decoy to a territorial male, and
points in panel (a) are jittered vertically by 0.1 to improve visual
clarity. Squares represent the model-estimated means SE.
(Fig. 2), and our selection analysis indicated strong
intrasexual selection on this ornament (c.f. Kingsolver
et al., 2012). Although we are unable to assess the
strength of intersexual selection in this study, other
selection analyses in odonates have found positive (e.g.
ordoba-Aguilar, 2002) or no (e.g. Grether, 1996b)
intersexual selection on wing ornamentation. Contrary
to many studies of other odonates (reviewed in Koenig,
2008), and despite a positive relationship between body
size and the likelihood of winning territorial disputes
(Fig. 4b), we did not observe selection on body size. As
small males are likely to lose fights and never acquire a
territory, it is possible that, by including primarily
males that had already acquired territories, our esti-
mates of selection on body size (and all other traits)
may be conservative. While we also predicted that
increased melanization may come at the cost of repro-
ductive lifespan (e.g. Grether, 1997; Kuchta & Svens-
son, 2014), we found no evidence for viability selection
against wing melanization. However, the opportunity
for viability selection (0.097) was considerably lower
than the opportunity for intrasexual selection (0.707),
and therefore, intrasexual selection may be relatively
more important for generating variance in male fitness
in this population, further suggesting strong overall fit-
ness benefits of ornamentation.
Our results indicate that the functional benefit of wing
melanization in P. longipennis is through decreased
aggression received from rival males. Territorial disputes
in odonates are extremely energetically costly, and con-
sume most of an individual’s daily energy budget (Fried
& May, 1983; Koskim
aki et al., 2004). As males do not
feed while they are defending territories (Fried & May,
1983), any decrease in the energy expended on battling
intruders may increase the time over which a male holds
its territory, and therefore also increase the likelihood of
mating (Suhonen et al., 2008). Moreover, in contrast
with many other odonates, P. longipennis males make
physical contact during territorial disputes, greatly
increasing the chances of severe injury or death (Sher-
man, 1983; McCauley, 2010; Paulson, 2012). Our results
suggest that rivals challenge males with greater ornamen-
tation less frequently and with lower intensity (Fig. 3),
potentially improving a male’s ability to remain in a terri-
tory and/or avoid injury. Similar to damselflies express-
ing red wing ornaments (Grether, 1996b; Guillermo-
Ferreira et al., 2015), it seems likely that a primary func-
tional advantage of greater melanin ornamentation is
through decreased aggression from territorial rivals.
The information provided to rivals and potential
mates is crucial to the evolution of sexual signals, and
those involved in malemale competition are predicted
to evolve to ensure that disputes are resolved as
cheaply as possible for both parties (Maynard Smith &
Harper, 2003; Searcy & Nowicki, 2005). In particular,
territorial males should assess the fighting ability of
their rival and avoid engaging them if they are unlikely
to win the dispute or if the cost of winning the dispute
is too high (Maynard Smith & Harper, 2003; Arnott &
Elwood, 2009). As wing melanization is associated with
a male’s ability to win contests (Fig. 4), rivals would
–3 –2 1 0 1 2
Body size [ztransformed (mm)]
Probability of winning contest
–2 –1 0 1 2
Wing melanization [ztransformed]
Probability of winning contest
Fig. 4 The likelihood of winning a territorial contest increased
with wing melanization (a) and body size (b). Each point
represents the outcome of a contest for an individual (0 =contest
lost, 1 =contest won), and points were jittered vertically by 0.1 to
improve visual clarity. Regression lines are fitted from the mixed-
effects model reported in the Results, and both explanatory
variables were z-transformed.
Table 1 Variation in immune response scores of 28 territorial
males as a function of wing melanization, body size and date
(multiple R
=0.306, F
=3.53, P=0.030). Model estimates
(SE) were obtained after removing the nonsignificant wing
melanization 9size interaction. Wing melanization and body size
were z-transformed prior to analysis, and date represents the
difference between the 2 days over which males were captured.
All partial F-tests were on 1 and 24 degrees of freedom.
Effect Estimate FP
Wing melanization 7.381 3.110 5.69 0.026
Body size 5.418 2.808 3.76 0.065
Date 9.466 5.414 2.94 0.100
Wing melanization 9body size 1.26 0.274
Sexual selection on dragonfly ornamentation 7
benefit from avoiding costly and/or potentially injuri-
ous disputes with highly ornamented males (Junior &
Peixoto, 2013; Guillermo-Ferreira et al., 2015). Indeed,
males with experimentally increased ornamentation
received significantly lower aggression from rivals
(Fig. 3). As the fitness benefits of displaying a large
ornament are great, the signal must be reliable, on
average, to be evolutionarily maintained, otherwise
males would cease to respond (Maynard Smith & Har-
per, 2003). In many cases, melanin ornaments in
arthropods may signal condition reliably because of the
biochemical link between immune defence and
colouration (Table 1). While a male’s immunocompe-
tence may not be specifically informative to rivals, the
high costs of the melanin synthesis pathway (Gonz
Santoyo & C
ordoba-Aguilar, 2012) will ensure that
only males in the best condition have the capacity to
allocate sufficient resources (e.g. energy, precursors,
enzymes) to support robust immune function and large
wing ornaments (e.g. Hooper et al., 1999; Rantala et al.,
2000; Siva-Jothy, 2000). The maintenance of melanin
wing ornaments in insects also requires some degree of
constant pigment deposition (Hooper et al., 1999; True
et al., 1999), further enabling the ornament to reflect
the individual’s present physiological state. As there is a
strong relationship between condition and fighting abil-
ity in insects (reviewed in Vieira & Peixoto, 2013), and
investment in many other condition-related traits ends
at metamorphosis or maturity (e.g. body size), the mel-
anin synthesis pathway may be a common mechanism
by which arthropods reliably signal proximate informa-
tion about their condition and fighting ability to rivals.
While the shared biochemical pathway linking
immune defence and colouration promotes signal relia-
bility, intrasexual selection will also favour males that
maximize signal efficiency (Badyaev, 2004; Stoehr,
2006), which will have consequences across the mela-
nin synthesis pathway. Indeed, artificial selection
experiments (Armitage & Siva-Jothy, 2005) and studies
of natural populations experiencing divergent selection
pressures (Fedorka et al., 2013) have found that selec-
tion on melanin colouration often promotes the corre-
lated evolution of melanin immune defence. As with
most sexual signals (reviewed in Hill, 2011; Morehouse,
2014; but see Craig & Foote, 2001), the specific targets
of selection for improving the efficiency of melanogene-
sis are unknown. However, two evolutionary outcomes
for the melanin synthesis pathway seem most likely:
(1) energetic resources may be more efficiently allo-
cated to the production of melanin synthesis enzymes
(e.g. phenoloxidase), and (2) amino acid precursors
may be more readily available for conversion to mela-
nin. It remains to be seen which of these two outcomes
is more likely or whether either is general across spe-
cies, as some studies of the melanin synthesis pathway
indicate energetic limitations (e.g. Cotter et al., 2010),
while others report precursor limitations (e.g. Srygley
et al., 2009). Importantly, as both immune defence and
colouration depend on many of the same precursors
and enzymes, selection for increased signalling effi-
ciency may be unable to completely erode the associa-
tion between colouration and condition, and the signal
will remain reliable, on average. Nevertheless, if intra-
sexual selection favours greater efficiency of signal pro-
duction, then populations exhibiting stronger
intrasexual selection on wing melanization should
express more efficient melanogenesis.
The evolution of sex-specific ornamentation depends
in part on the functional mechanisms by which the
ornament affects reproductive success (Andersson,
1994; Lailvaux & Irschick, 2006). We found strong
support for a sexual signalling function shaping the
evolution of sex-specific wing melanization in a terri-
torial dragonfly. Melanin colouration exhibits a diverse
suite of adaptive functions in arthropods (e.g. Punza-
lan et al., 2008c; Fedorka et al., 2013; Debecker et al.,
2015), but given its frequently observed condition
dependence (e.g. Talloen et al., 2004; Punzalan et al.,
2008a), the ability to act as a sexual signal of condi-
tion may commonly shape its evolution. Although any
direct or indirect positive covariance between orna-
mentation and aspects of condition may ultimately
facilitate condition-related sexual signalling of an orna-
ment, linkages underlain by shared condition-depen-
dent developmental pathways are predicted to readily
evolve via sexual signalling functions (Hill, 2011; Rou-
lin, 2016). As the melanin synthesis pathway links
ornamentation and immunocompetence in arthropods,
sexual signalling, like that observed here, may indeed
prove to be a common adaptive function shaping the
evolution of sex-specific melanin colouration.
We thank M. Dugas for his invaluable assistance and
insight during all stages of the study. J. Larsen, H. Roll-
ins and A. Gilmore greatly assisted with the collection
of the data. A. Locci and the Squire Valleevue Farm
staff generously provided access to the field site. We
further appreciate comments from S. Diamond, P.
Lorch, M. Benard, K. Krynak, L. Chick, I. Ghergel, A.
Perez, T. Schwander, D. Punzalan, members of the Case
Western Reserve University Ecology and Evolution
group, and two anonymous referees that improved the
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Supporting information
Additional Supporting Information may be found
online in the supporting information tab for this article:
Figure S1 There was no relationship between a male’s
wing melanization and its body size (a) or its relative
wing size (b). Each point represents an individual.
Figure S2 Rear wings of territorial Pachydiplax longipen-
nis showing examples of weak natural melanization
(top), experimentally manipulated melanization (mid-
dle) and strong natural melanization (bottom).
Table S1 All variance-standardized selection gradients
for intrasexual and viability selection (Lande & Arnold,
Data deposited at Dryad: doi: 10.5061/dryad.rc1k8
Received 6 May 2016; revised 3 July 2016; accepted 19 July 2016
... /10.5061/dryad.44j0zpccf; Moore and Martin 2021). For each analysis, we first used corrected Akaike information criterion to determine the best method of accounting for shared evolutionary history: a Pagel's l branch-length transformation, a Brownian motion model, or a star phylogeny (table S3). ...
... Rationale. Selection has driven the diversification of melanin wing coloration across odonates (e.g., Svensson et al. 2007; Moore and Martin 2016;Santos and Machado 2016). However, arthropods use only a few highly conserved genes to synthesize melanin for many traits (Stoehr 2006)-including the melanin that encapsulates parasites and pathogens during immune responses (González-Santoyo and Córdoba-Aguilar 2012). ...
... each species' entire range. To do this, we digitized plates from every eastern North American odonate field guide that had dorsal views of the species (see table S4) and then quantified the proportion of melanized wing area using ImageJ (Moore and Martin 2016). Coloration values estimated in this way are approximate but reflect both the rank order of coloration and the magnitude of interspecific differences in many organisms, including odonates (e.g., Zeuss et al. 2014;Dale et al. 2015). ...
Although natural selection often fluctuates across ontogeny, it remains unclear what conditions enable selection in one life-cycle stage to shape evolution in others. Organisms that undergo metamorphosis are useful for addressing this topic because their highly specialized life-cycle stages cannot always evolve independently despite their dramatic life-history transition. Using a comparative study of dragonflies, we examined three conditions that are hypothesized to allow selection in one stage to affect evolution in others. First, we tested whether lineages with less dramatic metamorphosis (e.g., hemimetabolous insects) lack the capacity for stage-specific evolution. Rejecting this hypothesis, we found that larval body shape evolves independently from selection on adult shape. Next, we evaluated whether stage-specific evolution is limited for homologous and/or coadapted structures. Indeed, we found that selection for larger wings is associated with the evolution of coadapted larval sheaths that store developing wing tissue. Finally, we assessed whether stage-specific evolution is restricted for traits linked to a single biochemical pathway. Supporting this hypothesis, we found that species with more wing melanization in the adult stage have evolved weaker melanin immune defenses in the larval stage. Thus, our results collectively show that natural selection in one stage imposes trait-dependent constraints on evolution in others.
... Briefly, in the cooler portions of the species' range (i.e. northern and eastern), male P. longipennis produce dark intrasexually selected wing melanisation (Paulson, 2012;Moore & Martin, 2016;Moore et al., 2018a). In addition to signalling a male's condition and fighting ability to rivals (Moore & Martin, 2016), recent work in a wild population showed that having more of this wing colouration improves a male's heating ability and, subsequently, its territorial success under cooler conditions . ...
... northern and eastern), male P. longipennis produce dark intrasexually selected wing melanisation (Paulson, 2012;Moore & Martin, 2016;Moore et al., 2018a). In addition to signalling a male's condition and fighting ability to rivals (Moore & Martin, 2016), recent work in a wild population showed that having more of this wing colouration improves a male's heating ability and, subsequently, its territorial success under cooler conditions . Because of these thermal properties, males that facultatively develop more colouration under cooler conditions should gain a fitness advantage, all else being equal. ...
... Because of these thermal properties, males that facultatively develop more colouration under cooler conditions should gain a fitness advantage, all else being equal. Conversely, because colouration is energetically costly to produce and maintain (Moore & Martin, 2016, 2018Moore et al., 2018a), developing more colouration under warmer conditions should provide smaller net benefits or may even impose costs associated with overheating . Indeed, males have substantially reduced pigmentation in the warmest regions (Paulson, 2009;. ...
1. When the breeding environment fluctuates across generations, reproductive traits may evolve plasticity that optimises the balance between survival and mating success for the prevailing environment. 2. For sexually selected colouration, this balance can depend on environmental temperatures. Accordingly, breeding colouration often co-varies with temperature through space and time. However, whether such traits exhibit plasticity in response to environmental temperatures is poorly understood. 3. In the present study, a dragonfly (Pachydiplax longipennis) was reared under ambient or experimentally warmed conditions and tested for plasticity in its intrasexually selected wing colouration. Although wing colouration improves male territorial success, these advantages are smaller under warmer conditions than cooler conditions. It was therefore predicted that males reared under the ambient thermal conditions of the study site (Cleveland, Ohio) would develop more wing colouration than those reared under experimentally warmed conditions. 4. Contrary to this prediction, males reared in warm larval temperatures produced more wing colouration. Thus, although the secondary sexual colouration of this species displays some thermal plasticity, it does not appear to be adaptive relative to the known thermal variation of intrasexual selection in this population. 5. Given that the environment often determines the strength and direction of sexual selection, future studies should consider the potential for non-adaptive, and even maladaptive, developmental plasticity in the sexually selected traits of insects.
... In this study, we explored temperature's potential to influence the costs, benefits and geographic diversification of sexual coloration in a North American dragonfly (Pachydiplax longipennis Burmeister). Males of this medium-sized species produce dark, condition-dependent coloration on their wings , which intimidates rivals and improves territorial success (Moore & Martin 2016). As territorial success determines a substantial amount of mating success in this (Sherman 1983) and similar species (reviewed in Suhonen et al. 2008), such advantages strongly increase male fitness. ...
... Males exhibit continuous variation in wing coloration within populations across the northern and eastern portions of the species' range (e.g. Moore & Martin 2016). However, males possess drastically reduced coloration in western regions (e.g. ...
... Females sometimes, though not always, produce a small amount of basal wing pigmentation. Unless otherwise noted, we report wing coloration as the per cent of the total wing area with pigmentation, as this metric is a known target of intrasexual selection (Moore & Martin 2016). The Supporting Information Methods and Results provides detailed methods for measuring this trait from digitised photographs in ImageJ (Rasband 2012). ...
Full-text available
The environment shapes the evolution of secondary sexual traits by determining how their costs and benefits vary across the landscape. Given the thermal properties of dark coloration generally, temperature should crucially influence the costs, benefits and geographic diversification of many secondary sexual colour patterns. We tested this hypothesis using sexually selected wing coloration in a dragonfly. We find that greater wing coloration heats males-the magnitude of which improves flight performance under cool conditions but dramatically reduces it under warm conditions. In a colder region of the species' range, behavioural observations of a wild population show that these thermal effects translate into greater territorial acquisition on thermally variable days. Finally, geo-referenced photographs taken by citizen scientists reveal that this sexually selected wing coloration is dramatically reduced in the hottest portions of the species' range. Collectively, our results underscore temperature's capacity to promote and constrain the evolution of sexual coloration.
... wing spots). These are often considered 'honest' sexual signals that indicate the quality of a territorial male [15][16][17][18], but whether the size of these wing spots correlates with the success of holding a territory is so far inconclusive [19,20]. Furthermore, the possibility to implement modern phylogenetic analysis on an already existing dataset of odonate territory size [11] provided the stimulus for the current study. ...
... In several insect species that display territorial behaviour, males have melanin-based sexual characters that are highly visible and considered 'honest' indicators of male quality. The size of these characters has been found to correlate with, for example, the strength of immune defence [15,16,18,34,35] and the males' ability to hold territories against rival males [17,36,37]. Therefore, it is somewhat surprising that this trait that may strongly affect the outcomes of territorial fights has no effect on the territory size of an odonate species. ...
The territory is a distinct mating place that a male defends against intruding conspecific males. The size of a territory varies between species and most of the variation between species has been found to scale allometrically with body mass. The variation that could not be explained by body mass has been explained with several variables such as habitat productivity, trophic level, locomotion strategy and thermoregulation. All previous interspecific comparative studies have been done on vertebrate species such as birds, mammals, reptiles and fishes, meaning that studies using invertebrate species are missing. Here, we studied the relationship of a species's territory size with its fresh body mass (FBM) in addition to other ecologically relevant traits using 86 damselfly and dragonfly (Odonata) species. We found that territory size is strongly affected by species FBM, following an allometric relationship similar to vertebrates. We also found that the territory size of a species was affected by its territorial defence strategy, constantly flying species having larger territories than species that mostly perch. Breeding habitat or the presence of sexual characters did not affect territory sizes, but lotic species and species without wing spots had steeper allometric slopes. It seems that an increase in a species's body mass increases its territory size and may force the species to shift its territory defence strategy from a percher to a flier.
... large size, frequent patrolling), can be assumed to communicate its higher competitive ability condition to other males, thus discouraging poor-quality males from invading the territory. In addition, this can also be used as display to attract the attention of females (Contreras-Garduno et al. 2008;Schultz & Fincke 2009;Moore & Martin 2016). ...
In male odonates, both size and fat content are related to territory defence and mating success. Males that are larger and have higher energy reserves win relatively more disputes for territory and attract more females. Wing colour has also been regarded as a mechanism that influences agonistic behaviour between males, as wing pigmentation might be regarded as a sign of male quality. In this study, we analysed whether a set of male physical (body size and wing colour), physiological (body fat content) and behavioural (disputes between males) characteristics were involved in the territory defence and mating behaviour of the neotropical dragonfly Zenithoptera lanei Santos, 1941 (Anisoptera: Libellulidae). Males were characterised as territorial whenever they warded‐off other males and remained in the same place within the pond for two consecutive days. In general, these territorial males were larger and had more abdominal and thoracic fat, engaged in pursuits more frequently, spent more time on sexual behaviour and female guarding, and mated more in comparison to subordinate males. By evaluating whether the percentage of wing area covered by black ink influenced male behaviour, we found that territorial males tended to act aggressively towards other males whose wings were partially painted, and sexually towards females irrespective of wing area painted. In Z. lanei, both body size and fat content play a role in defining territoriality. By subduing competitors and dominating preferred locations within high‐quality sites, these males are likely to be visited by females and engage in mating.
... To understand the adaptive purposes of colorful traits, researchers have designed experiments that involve manipulating colors in various ways. Some researchers have used colored decoy stimuli such as models 4,5,6,7,8 , photographs 9 , or videos 10,11,12 that are presented to receivers in behavioral experiments. Others, especially when using invertebrates, have manipulated the lighting environment to affect the appearance of colors of live individuals 13,14,15,16,17 . ...
... Animals widely use coloration in communication, since it may convey information on fighting ability (Moore and Martin 2016), social dominance (Dey et al. 2015), and overall individual quality (Pérez i de Lanuza et al. 2013). Also, animal coloration may inform about physiological conditions (Arai et al. 2017), such as oxidative and immune status 1 3 (McGraw 2005;Simons et al. 2012), as well as parasite load (Molnár et al. 2013). ...
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Coloration is often key in animal communication, and is frequently subjected to strong natural and sexual selection, often with opposed directions: natural selection typically favors cryptic colorations whereas sexual selection may favor conspicuous colorations. Also, different coloration traits may convey different pieces of information. Plus, coloration may vary among habitats, mirroring local selective pressures. In this work, we test if color parameters (luminosity, chroma, and hue) of back and throat are related to different life-history and morphological traits in Epidalea calamita toads. Furthermore, we check possible variability of color parameters between agrosystem and natural habitat toads. Toad coloration was sexually dimorphic, which suggests a role of coloration in sexual communication. Moreover, coloration correlated with age, body size, hindlimb length, and sprint speed. These findings suggest communication based on coloration beyond sex recognition: coloration could act as a signal of overall quality of bearers, with a potential role in mate choice. Moreover, coloration differed between habitats. Greener backs in agrosystem toads could indicate greater intensity of predator pressure, while their higher saturation could indicate greater investment in mate attraction. This result is aligned with previous findings that agrosystem toads respond to reduced lifespan with greater reproductive investment.
For ectothermic insects, their colour and size are important determinants of body temperature: larger bodies require more heat to reach a certain temperature, and dark colours absorb heat more efficiently. These dark colours are expressed using melanin, which has been intimately linked with the thermoregulatory capabilities of insects. Melanin is also linked with immune defence and is often used as a secondary sexual character in insects. There is a potential trade-off situation between thermoregulatory capabilities, immune defence and secondary sexual characters, all of which use melanin. Some Calopteryx damselflies, such as Calopteryx splendens, have melanin-based wing pigmentation that is sexually selected and drives intra- and interspecific territorial aggression. Our goal was to study experimentally how the wing pigmentation and body size of C. splendens males affect their thermoregulation and, especially, their ability to become active (hereafter, ‘activate’) after being cooled down. Our results were in line with our hypotheses, showing that individuals with larger wing spots had significantly faster activation times than those with smaller wing spots, and that individuals with larger body size had significantly slower activation times than those with smaller body size. Both variables showed an interaction and are therefore important in damselfly warm-up and activation. We discuss the role of wing pigmentation and thermoregulation in the behavioural patterns observed in Calopteryx species.
Temperature shapes the processes and outcomes of behaviors that occur throughout the progression of insect and arachnid mating interactions and reproduction. Here, we highlight how temperature impacts precopulatory activity levels, competition among rivals, communication with potential mates, and the relative costs and benefits of mating. We review how both the prevailing temperature conditions during reproductive activity and the temperatures experienced early in life influence mating-related behavior. To effectively predict the consequences of global warming for insect and arachnid mating behavior, we advocate for future work that universally integrates a function-valued approach to measuring thermal sensitivity. A function-valued approach will be especially useful for understanding how fine-scale temperature variation shapes current and future selection on mating interactions.
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Although dragonflies are excellent environmental indicators for monitoring terrestrial water ecosystems, automatic monitoring techniques using digital tools are limited. We designed a novel camera trapping system with an original dragonfly detector based on the hypothesis that perching dragonflies can be automatically detected using inexpensive and energy-saving photosensors built in a perch-like structure. A trial version of the camera trap was developed and evaluated in a case study targeting red dragonflies ( Sympetrum spp.) in Japan. During an approximately 2-month period, the detector successfully detected Sympetrum dragonflies while using extremely low power consumption (less than 5 mW). Furthermore, a short-term field experiment using time-lapse cameras for validation at three locations indicated that the detection accuracy was sufficient for practical applications. The frequency of false positive detection ranged from 17 to 51 over an approximately 2-day period. The detection sensitivities were 0.67 and 1.0 at two locations, where a time-lapse camera confirmed that Sympetrum dragonflies perched on the trap more than once. However, the correspondence between the detection frequency by the camera trap and the abundance of Sympetrum dragonflies determined by field observations conducted in parallel was low when the dragonfly density was relatively high. Despite the potential for improvements in our camera trap and its application to the quantitative monitoring of dragonflies, the low cost and low power consumption of the detector make it a promising tool.
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The life spans of animals can be measured in natural populations by uniquely marking individuals and then releasing them into the field. Selection on survival (a component of fitness) can subsequently be quantified by regressing the life spans of these marked individuals on their trait values. However, marked individuals are not always seen on every subsequent catching occasion, and for this reason, imperfect detection is considered a problem when estimating survival selection in natural populations. Capture-mark-recapture methods have been advocated as a powerful means to correct for imperfect detection. Here, we use simulated and field data sets to evaluate the effect of assuming perfect detection ('naïve methods'), when detection is really imperfect. We compared the performance of the naïve methods with methods correcting for imperfect detection (mark-recapture methods, or MR). Although the effects of trait-dependent recapture probability are mitigated when recapture probability is high, mark-recapture methods still provide the safest choice when recapture probability might be trait-dependent. In our simulations, mark-recapture methods had a power advantage over naïve methods, but all methods lost statistical power at low recapture probabilities. The main advantage of mark-recapture methods over naïve methods is the ability to control for hidden trait-dependent recapture probability, as it is often hard to tell a priori if trait dependence is an issue in a particular study. However, when trait-dependent recapture probability is weak, naïve methods and mark-recapture methods perform similarly as long as recapture rates do not become too low, and the main problem of survival selection studies is still low statistical power. We provide a R package (EasyMARK) alongside with this paper to facilitate future integration between MR methods and classical selection studies. EasyMARK provides the opportunity to convert the regression coefficients from MR-approaches in to classical standardized selection gradients.
Technical Report
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Description Fit linear and generalized linear mixed-effects models. The models and their components are represented using S4 classes and methods. The core computational algorithms are implemented using the 'Eigen' C++ library for numerical linear algebra and 'RcppEigen' ``glue''.
I studied the sex-limited red spots on the wings of male rubyspot damselflies (Hetaerina americana) in relation to territoriality and fitness in the wild. Both observational and experimental (wing spot manipulation) studies indicated that wing spots were selected through competition among males for mating territories, not through female choice or direct competition for females. Males with naturally or artificially large wing spots were more successful at holding territories and consequently mated at higher rates than males with relatively small wing spots. In contrast, sexual selection on male body size appeared to operate among nonterritorial males at the clasping stage of the mating sequence, perhaps because larger males were better at clasping females forcibly. Of four models proposed to explain the evolution of ornaments through territory competition, only the agonistic handicap model makes predictions consistent with the results of this study.
Genetically distinct anadromous (sockeye) and nonanadromous (kokanee) morphs of the Pacific salmon, Oncorhynchus nerka, develop identical, brilliant red color at maturity during sympatric breeding in freshwater streams. The marine and lacustrine environments they occupy prior to maturity, however, appear to differ in the availability of dietary carotenoid pigments necessary to produce red coloration. We tested the hypothesis that kokanee, which occupy carotenoid-poor lakes, are more efficient at using the dietary pigments than are sockeye, which occupy the more productive North Pacific Ocean. In a 2-year controlled breeding study, flesh and skin color of mature and immature crosses fed a low-carotenoid diet were quantified with both a chromameter and by chemical extraction of carotenoid pigments. Results revealed striking countergradient variation in carotenoid use, with kokanee approximately three times more efficient at sequestering the pigments to the flesh musculature than similar age sockeye. This difference translated into virtually nonoverlapping differences between pure crosses in secondary sexual color at maturity, when the pigments are mobilized and transported to the skin. Kokanee crosses turned pinkish red over most of their body, whereas sockeye turned olive green. The olive green was similar to the breeding color of residuals in the wild, the progeny of anadromous sockeye that remain in fresh water and are believed to have given rise to kokanee on numerous independent occasions. Reciprocal hybrids were similar to each other and intermediate to the pure crosses, indicating additive genetic inheritance. Mate choice trials with sockeye males in the wild showed the ancestral morph strongly preferred red over green models. These results suggest a preference for red mates maintained in nonanadromous breeding populations drove the reevolution of the red phenotype in kokanee via more efficient use of dietary carotenoid pigments. This is a novel, yet hidden, mechanism by which sexual selection promotes the genetic differentiation of these sympatric populations.
This chapter summarizes studies of lifetime reproductive success (LRS) conducted on odonates. Such studies have focused on many characters, but have typically concluded that survivorship - the main component of natural selection, is more important than mating efficiency - a primary component of sexual selection, in determining LRS. They have also frequently found that environmental factors are important and that selection and the opportunity for selection vary considerably depending on density, sex ratio, and community composition. LRS studies have been most successful when focused on specific traits and when complemented by experimental manipulations. Progress in understanding the current actions of natural and sexual selection is thus most likely to involve long-term LRS work combined with experimental or comparative approaches. Particularly desirable are studies that incorporate the larval stage in fitness calculations, perform parentage analyses to determine realized fitness, and consider the role of non-breeding behaviours such as foraging efficiency.
Sexual ornaments are favoured to be both less integrated with other organismal traits for greater expression, and yet more integrated with organismal development and functions to better indicate the physiological quality of an organism. Two conceptual approaches in morphological evolution - the consideration of internal and external processes and the evolution of integration and modularity - are useful in resolving this apparent paradox, yet these approaches are mostly overlooked in studies of the development of sexual displays. Moreover, whereas recent studies have recognized the evolutionary continuum of the mechanisms by which sexual selection operates, the consequences for the evolution of development of sexual displays are not well understood. Here I suggest that the concept of morphological integration may provide a useful framework for understanding the development and evolution of sexual ornamentation.
This chapter discusses causes and consequences of territorial behaviour in odonates. In territorial species, males may use two mating tactics or strategies that may be environmentally or genetically determined: territoriality and non-territoriality. The tactic a male exhibits in each particular case is determined by the cost-benefit ratio of territorial and nonterritorial behaviours. The main benefit of territoriality is increased access to females, and the costs may accumulate due to e.g., predation, injuries, and/ or energy loss due to territorial contests. Moreover, density of both males and females as well as sex-ratio at breeding sites both contribute to the costs and benefits of each tactic. Interspecific aggression by heterospecific males may also influence the profitability of these tactics.
It is generally believed that resource holding potential reliably reflects male quality, but empirical evidence showing this is scarce. Here we show that the outcome of male-male competition may predict male immunocompetence in the territorial damselfly, Calopteryx virgo (Odonata: Calopterygidae). We staged contests between 27 pairs of males and found that winners of the contests showed higher immunocompetence, measured as encapsulation response, compared with that of losers. Furthermore, the winners had larger fat reserves. We also collected 29 males that had not been used in staged contests, and found that in these males encapsulation response correlated positively with an individual's fat reserves. Both immunocompetence and resource holding potential seem to depend on energy reserves, suggesting a trade-off between parasite resistance and energetically costly territorial behavior. The results suggest that the outcome of male-male contest can be used to predict male quality in terms of immune defense. Copyright 2004.