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Sexual dimorphism and intra-populational colour pattern variation in the aposematic frog Dendrobates tinctorius

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Despite the predicted purifying role of stabilising selection against variation in warning signals, many aposematic species exhibit high variation in their colour patterns. The maintenance of such variation is not well understood, but it has been suggested to be the result of an interaction between sexual and natural selection. This interaction could also facilitate the evolution of sexual dichromatism. Here we analyse in detail the colour patterns of the poison frog Dendrobates tinctorius and evaluate the possible correlates of the variability in aposematic signals in a natural population. Against the theoretical pre- dictions of aposematism, we found that there is enormous intra-populational variation in colour patterns and that these also differ between the sexes: males have a yellower dorsum and bluer limbs than females. We discuss the possible roles of natural and sexual selection in the maintenance of this sexual dimorphism in coloration and argue that parental care could work synergistically with aposematism to select for yellower males.
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ORIGINAL PAPER
Sexual dimorphism and intra-populational colour
pattern variation in the aposematic frog
Dendrobates tinctorius
Bibiana Rojas John A. Endler
Received: 11 September 2012 / Accepted: 21 March 2013
ÓSpringer Science+Business Media Dordrecht 2013
Abstract Despite the predicted purifying role of stabilising selection against variation in
warning signals, many aposematic species exhibit high variation in their colour patterns.
The maintenance of such variation is not well understood, but it has been suggested to be
the result of an interaction between sexual and natural selection. This interaction could also
facilitate the evolution of sexual dichromatism. Here we analyse in detail the colour
patterns of the poison frog Dendrobates tinctorius and evaluate the possible correlates of
the variability in aposematic signals in a natural population. Against the theoretical pre-
dictions of aposematism, we found that there is enormous intra-populational variation in
colour patterns and that these also differ between the sexes: males have a yellower dorsum
and bluer limbs than females. We discuss the possible roles of natural and sexual selection
in the maintenance of this sexual dimorphism in coloration and argue that parental care
could work synergistically with aposematism to select for yellower males.
Keywords Aposematism Polymorphism Sexual dimorphism Parental care
Poison frog
Introduction
Aposematism is an anti-predator strategy by which some animals warn their predators
about their unprofitability with conspicuous colours or patterns (Poulton 1890; Ruxton
et al. 2004). Because variation in aposematic signals makes it difficult for predators to learn
and retain the association between colour patterns and distastefulness, warning signals are
expected to be simple and uniform (Endler 1988; Joron and Mallet 1998; Endler and
B. Rojas J. A. Endler
Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University at
Waurn Ponds, 75 Pigdons Road, Geelong, VIC 3217, Australia
B. Rojas (&)
Centre of Excellence in Biological Interactions, Department of Biological and Environmental Science,
University of Jyva
¨skyla
¨, PO Box 35, 40014 Jyva
¨skyla
¨, Finland
e-mail: bibiana.rojas@jyu.fi
123
Evol Ecol (2013) 27:739–753
DOI 10.1007/s10682-013-9640-4
Mappes 2004; Darst et al. 2006). However, variation in aposematic species occurs in many
different taxa such as moths (Nokelainen et al. 2012), ladybirds (O’Donald and Majerus
1984; Ueno et al. 1998), butterflies (Mallet and Joron 1999) and frogs (Myers and Daly
1983), suggesting that signal variation may serve other purposes or respond to additional
selective pressures.
Recent studies have suggested that an interaction between natural and sexual selection
might be responsible for colour pattern variation in some aposematic species. Different
components of sexual selection (intra-sexual competition, female choice, etc.) might select
for individuals with certain patterns to become more attractive to conspecifics (Ueno et al.
1998; Maan and Cummings 2009; Nokelainen et al. 2012), or to be better competitors
during intra-sexual encounters (Crothers et al. 2011), possibly leading to sexual dimor-
phism in the aposematic signals (Maan and Cummings 2009). Natural selection, on the
other hand, may give individuals with certain other patterns an advantage in avoiding
predation, leading to the maintenance of such variation (Nokelainen et al. 2012).
Here we evaluate some of the factors that may allow for intra-populational variability in
aposematic signals in the wild. We studied a natural population of the aposematic, highly
polymorphic poison frog Dendrobates tinctorius in order to (1) document in detail the main
characteristics of their variable colour patterns and (2) test for the occurrence of sexual
dimorphism in colouration. We predict that, if there were such dimorphism, males would be
more conspicuous given their prolonged exposure to predators due to parental duties.
Methods
Study species and study site
Dendrobates tinctorius is one of the largest species of the Neotropical family Dendro-
batidae (Silverstone 1975), with a body length (from snout to vent; hereon referred to as
SVL) that ranges between 37 and 53 mm in adult individuals at the study site (this study).
This species is distributed along the Eastern Guiana Shield and is associated with
canopy gaps in primary forests at elevations between 0 and 600 m (Noonan and Gaucher
2006; Born et al. 2010). This study was done at a lowland forest next to Camp Parare
´, Les
Nouragues Reserve, French Guiana (3°590N, 52°350W, at an elevation of approximately
120 m), over three field seasons between January and February 2009, January and March
2010, and January and June 2011. These months of the year correspond to part of the
breeding season of the species. The population density at the study site is about 4.3
individuals/100 m
2
(Devillechabrolle 2011).
Like most dendrobatid species, D. tinctorius is diurnal and exhibits an elaborated
paternal care that consists of clutch attendance and tadpole transport, both performed
exclusively by males (Lo
¨tters et al. 2007; Rojas, personal observation). In contrast to all
other dendrobatids, males of this species lack a regular advertisement call and seldom
vocalise during courtship. When they do produce calls, they are very soft (Lescure and
Marty 2000) and difficult for a human to hear (Rojas, personal observation); calls usually
occur when the courting female is out of their sight (Rojas, unpublished data). Calls are
also emitted during physical agonistic encounters, especially by the male being attacked
(Rojas, personal observation).
Dendrobates tinctorius has alkaloid-based chemical defenses (Summers and Clough
2001) and bright colour patterns that, according to field experiments with clay models,
seem to signal unprofitability to potential aerial predators (Noonan and Comeault 2009;
740 Evol Ecol (2013) 27:739–753
123
Comeault and Noonan 2011). These colour patterns vary significantly within (personal
observation; Fig. 1) and among populations (Wollenberg et al. 2008).
Sexual dimorphism in colour patterns
At the beginning of the study, sex was identified on the basis of behaviour during courtship (i.e.
individuals vocalising were males). Both courting individuals were caught when possible and
their snout-vent lengths and disc widths (third finger of left hand) were measured. These data
(from 36 males and 36 females) were used to construct a sex index from a discriminant function
analysis so that all subsequent individuals could be assigned to male or female on the basis of
their measurements. 100 % of individuals in the training setwere classified correctly, indicating
that this is a very reliable indicator of sex. Males are smaller than females (Table 1) and can be
reliably distinguished from the latter on the basis of a combination of body size and the size of
their finger discs (Fig. 2). Males have wider discs in proportion to their body size than females
(Ancova: SVL: F
(1,310)
=75.57, p\0.001; SVL*Sex: F
(1,310)
=4.84, p=0.029, Sex:
F
(1,310)
=0.014, NS; Fig. 2a). According to the discriminant analyses, based on SVL (dis-
criminant function coefficient =-0.884) and disc size (discriminant function coeffi-
cient =0.985), 100 % of the total number of individuals included in the study were classified
correctly for sex (Canonical correlation =0.932, Wilks’ Lambda =0.132, v
2
=621.28,
df =2, p\0.001; Fig. 2b), indicating that sex can be identified reliably from morphometrics.
Frogs (including those used to obtain the sex index) were found during daily surveys
along the full length of a 1.5 km transect. Upon capture, every frog (N =321) was pho-
tographed against graph paper for scale. Snout-vent length and disc size were measured on
Fig. 1 Colour pattern variation in D. tinctorius at the study site
Evol Ecol (2013) 27:739–753 741
123
Table 1 Descriptive statistics
Variable Mean ±SD (range)
Population Males Females
Snout-vent length (mm) 43.32 ±1.97 (35.48–44.66) N =311 40.89 ±1.97 (35.48–44.66) N =170 46.19 ±2.55 (36.96–52.54) N =141
Disc size (mm) 2.49 ±0.41 (1.52–3.35) N =311 2.81 ±0.24 (2.02–3.35) N =170 2.11 ±0.20 (1.52–2.61) N =141
Proportion of arms covered with yellow 0.28 ±0.33 (0–1) N =320 0.24 ±0.34 (0–1) N =173 0.33 ±0.33 (0–1) N =147
Proportion of arms covered with blue 0.37 ±0.38 (0–1) N =320 0.37 ±0.38 (0–1) N =173 0.30 ±0.36 (0–1) N =147
Proportion of legs covered with yellow 0.02 ±0.08 (0–1) N =320 0.03 ±0.09 (0–1) N =173 0.02 ±0.07 (0–1) N =147
Proportion of legs covered with blue 0.49 ±0.25 (0–1) N =320 0.50 ±0.24 (0–1) N =173 0.47 ±0.25 (0–1) N =147
Number of yellow patches in the back 1.65 ±1.10 (1–7) N =321 1.62 ±0.98 (1–6) N =174 1.69 ±1.23 (1–7) N =147
Number of dark patches within yellow 0.97 ±0.64 (0–3) N =321 0.95 ±0.63 (0–2) N =174 0.99 ±0.66 (0–3) N =147
Number of interruptions of dorsal yellow 1.08–1.44 (0–7) N =321 1.12 ±1.31 (0–6) N =174 1.03 ±1.59 (0–7) N =147
Proportion of dorsal yellow 0.30 ±0.09 (0.07–0.60) N =321 0.32 ±0.08 (0.09–0.60) N =174 0.29 ±0.09 (0.07–0.57) N =147
Pattern elongation 2.46 ±0.37 (1.51–3.62) N =321 2.46 ±0.29 (1.51–3.59) N =174 2.45 ±0.36 (1.60–3.62) N =147
Pattern complexity 0.07 ±0.02 (0.03–0.25) N =321 0.07 ±0.02 (0.04–0.20) N =174 0.07 ±0.03 (0.03–0.25) N =147
Dorsal contrast 0.20 ±0.03 (0.06–0.25) N =321 0.21 ±0.03 (0.08–0.25) N =174 0.20 ±0.04 (0.06–0.25) N =147
Proportion of ventral side coloured 0.46 ±0.22 (0–1) N =115 0.49 ±0.20 (0.25–0.75) N =61 0.42 ±0.24 (0–1) N =55
Proportion of throat coloured 0.34 ±0.17 (0–0.81) N =116 0.36 ±0.14 (0.06–0.80) N =61 0.32 ±0.19 (0–0.81) N =55
Throat contrast 0.19 ±0.06 (0–0.25) N =116 0.21 ±0.05 (0–0.25) N =61 0.18 ±0.07 (0–0.25) N =55
742 Evol Ecol (2013) 27:739–753
123
the photos using the software ImageJ. The dorsal region of each frog was extracted from the
photographs for subsequent analyses of colour patterns with a method (Endler 2012) that
uses transects across colour patterns, and allows the estimation of parameters like pattern
complexity, pattern elongation, and proportion of a particular colour based on the number of
transitions between adjacent colours (in this case yellow and black). These analyses were
done with MATLAB software. In addition to the parameters mentioned above, we also
recorded the number of yellow patches and the number of interruptions of yellow in the back
(modified from Wollenberg et al. 2008). We calculated a value of dorsal contrast by mul-
tiplying the proportion of yellow x the proportion of black; a larger product means more
contrast since if either colour is rarer the pattern has less contrast than if both are equally
frequent. We estimated the rank proportion of blue and yellow covering both the arms and
the hind limbs by choosing by eye one of five values between 0 (no blue or yellow at all) to 1
(either completely blue or completely yellow) representing the approximate proportion
covered with each colour (0, 0.25, 0.5, 0.75, and 1). Ranks were used instead of direct
measurements because arms and legs are difficult to photograph in a standard position in
live frogs and therefore photographic measures of limb patterns would be unreliable.
Because ventral patterns were not as variable as dorsal ones, we took ventral photographs of
only a third (115) of the 321 individuals used for dorsal pattern analysis in order to estimate
the coloured proportion of the ventral side (blue in most cases) and, more specifically, of the
throat region. The presence of shadows and the variable position of the frogs in the ventral
photos made it impossible to use the automated method for measuring ventral colour
proportions. Therefore the rank proportion of ventral coloration was estimated in the same
way as that of the limbs’. The proportion of colour for the throat was estimated with the
software ImageJ, and the throat contrast was calculated in the same way as dorsal contrast.
With the exception of pattern elongation (Endler 2012) none of the parameters of colour
patterns were normally distributed even after transformations, so we used non-parametric
analyses (Mann–Whitney) in order to test for differences in colour patterns characteristics
between the sexes. Pattern elongation was compared between males and females by means
Fig. 2 a Scatterplot showing the relationship between snout-vent length and disc size in males (triangles;
r
2
=0.21) and females (circles;r
2
=0.18) of D. tinctorius;bBox plots illustrating the distribution of
discriminant scores for the two sexes (see ‘‘Methods’ section for details on discriminant analysis)
Evol Ecol (2013) 27:739–753 743
123
of a one-way Anova, pvalues were corrected for multiple comparisons using sequential
Bonferroni tests. All statistical analyses were done with the software SPSS 19.0 for Mac.
Results
Intra-populational variation in colour patterns
There is much variation in the characteristics of colour patterns studied in this population
(Fig. 1; see Table 1for descriptive statistics).In general, the background dorsal colouris black,
with yellow dorsolateral lines that may fuse at the sacrum and extend to the vent. This often
results in the appearance of a large ovoid black spot on the dorsum. The width of dorsolateral
lines and completeness varies considerably covering between 7 and 60 % of total dorsum. The
lines can be interrupted between one and six times forming, in some cases, discontinuous
patches. As opposed to some other populations where individuals have a completely yellow
dorsum (Lo
¨tters et al. 2007; Noonan and Comeault 2009), in the study population even the
yellower individuals have a black patch within the yellowarea, and some individuals havetwo
or three. The limbs also have a black reticulated pattern with blue or a few scattered yellow
patches.The ventral side has most often a reticulated pattern of blackand blue, but can be almost
entirely black. Aside from patterncomplexity, none ofthe characteristics of the colour patterns
measured was correlated with body size (Table 2). Table 2provides a summary of the sig-
nificant correlations among the colour pattern characteristics measured. Individuals with yel-
lower arms have a larger proportion of dorsal yellow (Fig. 3a) distributed in fewer patches.
Individuals with bluer arms have less yellow in their dorsum (Fig. 3b), more elongated patterns
and a larger proportion of their ventral side coloured (Fig. 3c).
Pattern elongation is positively correlated with pattern complexity (Fig. 3d). Individuals
with dark patches within the yellow area have higher contrast (Fig. 3f) and a higher pattern
complexity (Fig. 3g), whereas those individuals with the largest number of interruptions of
yellow had the lowest dorsal contrast (Fig. 3h).
Sexual dimorphism in relation to colour patterns
There are no differences between the sexes in pattern complexity, pattern elongation,
number of interruptions of yellow patches, coloration of the hind limbs and the coloured
(blue or yellow) proportion of the ventral side (Table 3). Males have a significantly larger
proportion of dorsal yellow (Tables 1,3; Fig. 4a) and a higher dorsal and throat contrast
(Tables 1,3). Both dorsal (Fig. 4b) and throat contrast (Fig. 4c) were, however, more
variable in females than in males (Dorsal: Levene statistic
(1,320)
=10.071, p=0.002;
Throat: Levene statistic
(1,115)
=5.916, p=0.016). The coloration of the arms also differs
significantly between the sexes; females have yellower arms whereas males tend to have
bluer arms (Tables 1,3; Fig. 4d). The differences in throat contrast and proportion of arms
covered with yellow do not hold after a sequential Bonferroni correction.
Discussion
Dendrobates tinctorius exhibits a remarkable variation in colour patterns in the population
studied. Even though there seem to be discrete morphs given the little or no resemblance
among some individuals, colour pattern variation in this population is continuous. In spite
744 Evol Ecol (2013) 27:739–753
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Table 2 Non-parametric correlation matrix for body size and colour pattern characteristics
SUL pYA pBA nY nDP nIY pVC pDY PC PE DC pYL
SUL 1.000 (314)
pYA 0.081 (314) 1.000
pBA -0.083 (314) 20.854** (320) 1.000
nY 0.010 (314) 20.162** (320) -0.002 (320) 1.000
nDP 0.033 (314) 0.257** (320) 20.125* (320) 20.567** (320) 1.000
nIY -0.059 (314) 20.192** (320) 0.032 (320) 0.870** (320) 20.564** (320) 1.000
pVC -0.101 (115) -0.112 (115) 0.334** (115) 20.273** (115) 0.238* (115) 20.233* (115) 1.000
pDY -0.090 (314) 0.322** (320) 20.124* (320) 20.476** (320) 0.476** (320) 20.515** (320) 0.280** (320) 1.000
PC 20.118* (314) 0.031 (320) 0.007 (320) -0.052 (320) 0.216** (320) -0.019 (320) 0.127 (320) -0.080 (321) 1.000
PE -0.035 (314) -0.100 (320) 0.138* (320) 20.344** (320) -0.018 (320) 20.361** (320) 0.040 (320) 0.022 (321) 0.204** (321) 1.000
DC -0.089 (314) 0.322** (320) 20.125* (320) 20.477** (320) 0.477** (320) 20.515** (320) 0.276** (320) 1.000** (321) -0.081 (321) 0.024 (321) 1.000
pYL -0.044 (314) 0.457** (320) 20.286** (320) 20.175** (320) 0.162** (320) 20.172** (320) -0.041 (320) 0.390** (320) -0.021 (320) -0.095 (320) 0.388**
(320)
1.000
pBL -0.079 (314) 20.414** (320) 0.575** (320) 20.144** (320) 0.081 (320) 20.125* (320) 0.658** (320) 0.018 (320) 0.038 (320) 0.131* (320) 0.017
(320)
20.389**
(320)
SVL snout-vent length, pYA proportion of arms covered with yellow, pYB proportion of arms covered with blue, nY number of yellow patches in the back, nDP number of dark patches within yellow,
nIY number of interruptions of yellow, pVC coloured proportion of the ventral side, pDY proportion of dorsal yellow, PC pattern complexity, PE pattern elongation, DC dorsal contrast, pYL proportion
of legs covered with yellow and pBL proportion of legs covered with blue. Values given are Spearman rho and sample size (in brackets). Values in bold letters denote significant relationships at the
0.05 (*) or 0.01(**) significance level
Evol Ecol (2013) 27:739–753 745
123
Fig. 3 Scatterplots showing the relationships among colour pattern characteristics. See Table 2for details
on statistics
746 Evol Ecol (2013) 27:739–753
123
of this, there is sexual dimorphism in some characteristics of colour patterns: males have
overall significantly yellower backs with a higher contrast and bluer arms than females, and
show less variation in their coloration.
Understanding intra-populational variation in aposematic signals is challenging
As a result of stabilising selection, aposematic prey are expected to have uniform warning
signals (Endler 1988; Joron and Mallet 1998; Endler and Mappes 2004; Darst et al. 2006).
Signal variability should be selected against because it might reduce the ability of predators
to learn and retain the association between colour patterns and unprofitability (Greenwood
et al. 1981; Mallet and Joron 1999; Exnerova
´et al. 2006). In spite of this, aposematic
polymorphisms do occur in nature in a variety of taxa (Myers and Daly 1983; O’Donald
and Majerus 1984; Brakefield 1985; Ueno et al. 1998; Williams 2007; Nokelainen et al.
2012), making the selective pressures that lead to the origin and maintenance of variation
in aposematic signals difficult to understand.
In species with known (or potential) aerial predators, dorsal coloration might be subject
to natural selection. Ventral, throat, and limb coloration, on the other hand, could be the
result of sexual selection if those parts are particularly exposed during mating (Siddiqi
et al. 2004; Maan and Cummings 2008). A recent study on the geographic variation in
colour patterns of D. tinctorius using neutral molecular markers suggests that dorsal colour
patterns are under selection, whereas ventral colouration is not (Wollenberg et al. 2008). In
support of this, studies with clay models have shown that dorsal patterns can indeed
influence attacks by predators in D. tinctorius (Noonan and Comeault 2009; Comeault and
Noonan 2011) as well as other species of poison frogs (Saporito et al. 2007; Chouteau and
Angers 2011), and snakes (Brodie 1993; Valkonen et al. 2011), implying a possible role of
natural selection in their evolution. Similarly, recent evidence has demonstrated that dorsal
colour patterns might be related to differential attractiveness of some morphs over others in
Table 3 Differences between the sexes in colour pattern characteristics
Variable U or F N
Proportion of arms covered with yellow 10,623.0 320
Proportion of arms covered with blue 15,009.0** 320
Proportion of legs covered with yellow 13,097.0 320
Proportion of legs covered with blue 13,640.5 320
Number of yellow patches in the back 13,094.5 320
Number of dark patches within yellow 12,468.0 320
Number of interruptions of dorsal yellow 14,202.0 320
Proportion of dorsal yellow 15,723.5** 321
Pattern elongation F
(1,321)
=0.025 321
Pattern complexity 13,134.0 321
Dorsal contrast 15,717.5** 321
Proportion of ventral side coloured 10,623.0 115
Proportion of throat coloured F
(1,115)
=1.865 115
Throat contrast 2,166.0 115
Values given are Mann–Whitney Uunless specified otherwise. Values in bold letters denote significant
relationships at the 0.05 (*) or 0.01(**) significance level after the corresponding sequential Bonferroni
correction (Rice 1989)
Evol Ecol (2013) 27:739–753 747
123
the Ladybird Harmonia axyridis (Ueno et al. 1998) and the poison frog Oophaga pumilio
(Maan and Cummings 2009), indicating a possible influence of sexual selection.
The interaction between natural and sexual selection has the potential to generate
variation in phenotypes (Endler 2000). Thus, one possible explanation for the existence in
intra-populational variation in aposematic signals could come from interplay between these
two forces. Recent approaches to the understanding of the origin and maintenance of
aposematic polymorphisms seem to support this idea, for example white males of the wood
tiger moth Parasemia plantaginis seem to have a selective mating advantage whereas
yellow males are better protected from predators (Nokelainen et al. 2012).
Intra-populational variation in aposematic colour patterns could also be possible
because of ecological, physiological, or behavioural differences between/among the
morphs. One possible explanation for the existence of these differences is correlational
Fig. 4 Differences in colour pattern characteristics between males and females
748 Evol Ecol (2013) 27:739–753
123
selection, a type of selection that favours combinations of traits by generating linkage
disequilibrium between them (Endler 1986; Brodie 1992; Sinervo and Svensson 2002).
Correlational selection results mostly from frequency-dependent interactions like those
between predators and prey or pathogens and hosts (Sinervo and Svensson 2002), and has
been suggested to be the mechanism by which the color patterns and escape behavior of
some non-aposematic snakes are associated (Brodie 1992).
Because variation in aposematic signals might imply differences in conspicuousness
among the morphs, individuals could be subject to morph-specific attack rates (Endler
1988; Endler 1991). Therefore, aposematism as an anti-predator strategy might be less
effective for individuals with some colour patterns than for others. These differences could
also lead, for example, to differential microhabitat use. In such case, regardless of the
availability of diverse niches for all types of colour patterns, only individuals with certain
colour patterns would be favoured in one specific microhabitat (Gray and McKinnon 2007)
either by increased conspicuousness or because it offers the best hiding or escaping
opportunities. If an aposematic species is variable, then it could be expected that each
colour form should select the microhabitat or visual background that maximizes its con-
spicuousness, especially if a specific colour pattern can evoke different responses from
predators depending on the surrounding background (Hegna et al. 2011). Males of the most
conspicuous populations of Oophaga pumilio, for example, tend to choose more exposed
perches for vocalisation than their less conspicuous counterparts (Pro
¨hl and Ostrowski
2011; Rudh et al. 2011). The combination of colours exhibited by D. tinctorius at the
studied population is especially suited for increased conspicuousness under the light
conditions of gaps (Endler 1993), which are the most representative habitat of the species
(Noonan and Gaucher 2006; Born et al. 2010). However, the specific hypothesis of
microhabitat segregation in relation to colour patterns remains to be tested in the future.
Sexual dimorphism in colour patterns
Colour polymorphisms have been proposed to be a transitional state in the evolution of
sexual dimorphism in colouration (Forsman and Appelqvist 1999). Sexual dichromatism
may result from different selective pressures and is often associated with sex-bias in
predation. Natural selection has favoured sexual dichromatism in viperid snakes, for
example, because males’ contrasting patterns seem to confuse visual predators when
moving rapidly in search of mates (Shine and Madsen 1994). This was corroborated during
a long-term field study on survival, which furthermore suggests that the higher survival of
zig-zagged males is not caused only by their colour patterns but by an interaction between
colour pattern and behaviour (Lindell and Forsman 1996). Sexual dimorphism in the bright
coloration of Papilio butterflies, on the other hand, seems most likely to be the result of
natural selection for the warning coloration of females (Kunte 2008) which, according to
Wallace (1889; cited in Kunte 2008), are more vulnerable to predation because of the
weight of their eggs and their less effective escape flight.
Sexual selection may also affect the sexes of aposematic species differently. In the
butterfly Papilio polyxenes sexual dimorphism on dorsal colour patterns seems to be the
consequence of sexual selection favouring males that look as suitable mates or better
competitors against other males (Lederhouse and Scriber 1987; Codella and Lederhouse
1989). In Oophaga pumilio sexual dimorphism in brightness could be a consequence of
sexual selection either via female choice, given that females prefer brighter males (Maan
and Cummings 2009), or via male–male competition because of its role in conflict reso-
lution (Crothers et al. 2011). There is no evidence that yellower D. tinctorius males have a
Evol Ecol (2013) 27:739–753 749
123
mating advantage over duller ones, which makes female choice unlikely to be the mech-
anism explaining male-biased yellowness. In fact, there seems to be a mating advantage for
yellower females (Rojas and Endler, in preparation). Intra-sexual selection is also unlikely
to play a role in the D. tinctorius sexual dichromatism. Field data showed that both males
and females engaged in agonistic interactions; we recorded 47 male–female, 6 male–male
and 11 female–female interactions. On the basis of the sex ratio of 320 individuals and a
null hypothesis of random encounters and interactions, there was a highly significant
excess of male–female interactions, a significant deficiency of male–male interactions, and
female–female interactions similar to expected from chance encounters (v
2
=16.374,
df =2, p\0.001). Altogether this suggests not only that intra-sexual selection is not
responsible for the male-biased sexual dichromatism in D. tinctorius, but also that the
colouration of males and females could indeed be subject to different selective pressures.
Males are likely to experience more predation in several taxa (Christe et al. 2006;
Boukal et al. 2008). Animals with parental care often exhibit differences in behaviour
between males and females, being the sex that performs the parental duties and remains in
the nest less vulnerable to predation than the sex that, for example, travels looking for food
(Stokes et al. 2011). In the case of D. tinctorius, parental duties involve moving for
prolonged periods of time and long distances during tadpole transport, which could make
males more detectable by predators. There is evidence that an increase in aposematic
brightness enhances predator learning (Prudic et al. 2007), and that changes in colour (hue)
may cause concomitant changes in brightness (Maan and Cummings 2009), so males could
benefit from being yellower in order to quickly educate their predators and protect not only
themselves, but also their offspring. We have weak evidence for this given that males are
less variable than females, and stronger selection reduces variation more than weaker
selection. Thus, males may have yellower backs and higher dorsal contrast than females as
a result of a synergy between sexual selection in the form of parental care and natural
selection in the form of enhanced aposematism. To our knowledge, this is the first study to
consider the role of parental care as a selective force affecting the way in which apose-
matism works in a polymorphic species.
Additional evidence in support of this idea comes from the propensity of individuals
with simpler colour patterns to invade fresh tree-fall gaps (which implies increased pre-
dation risk) earlier than individuals with complex patterns (Rojas and Endler, in prepa-
ration). This differential arrival in relation to colour patterns is more pronounced in
females than in males, who are responsible for the transport of tadpoles to suitable rearing
sites. The availability of new tadpole deposition sites is a key factor in tree-fall gap
invasion by males (Rojas, in preparation). Since ensuring good rearing site increases the
probability of offspring survival, especially given the high rates of larval cannibalism
(Rojas, unpublished data), males that arrive early to a tree-fall gap increase the likelihood
of their offspring being predators rather than prey. Hence, males might face a trade-off
between the future survival of their offspring and their own, which odds could be improved
by being yellower.
We must not assume that aposematism functions the same way for individuals with
different colour patterns in both sexes. This study suggests that future attempts to under-
stand the maintenance of aposematic signal variability must consider selective forces other
than predation and mate choice as the only active component of sexual selection. Parental
care, as a component of sexual selection, could work in synergy with aposematism to select
for differences in colour patterns between the sexes. Additionally, colour-pattern mediated
differences in aspects of the behaviour and ecology of polymorphic aposematic species are
750 Evol Ecol (2013) 27:739–753
123
worth exploring as forces that might work jointly to allow for the existence and mainte-
nance of intra-populational variation in aposematic colour patterns.
Acknowledgments This study was funded by two Les Nouragues grants from the CNRS (France), and
student research allowances from the School of Psychology at the University of Exeter (UK) and the CIE at
Deakin University (Australia), all to BR. P. Gaucher and M. Fernandez provided logistic support. We are
thankful to Diana Pizano and J. Devillechabrolle for assistance in the field, and to J. Mappes, J. Valkonen, J.
Brown and two anonymous reviewers for thoughtful comments and suggestions that improved the manu-
script. This work was done in compliance with the local environmental regulations (research permit issued
by CNRS-Guyane) and following ASAB’s guidelines for the treatment of animals in research.
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