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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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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
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
¨, PO Box 35, 40014 Jyva
¨, Finland
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.
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
(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
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
=75.57, p\0.001; SVL*Sex: F
=4.84, p=0.029, Sex:
=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
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
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
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;
=0.21) and females (circles;r
=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
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.
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
=10.071, p=0.002;
Throat: Levene statistic
=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.
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
Table 2 Non-parametric correlation matrix for body size and colour pattern characteristics
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**
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
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
Fig. 3 Scatterplots showing the relationships among colour pattern characteristics. See Table 2for details
on statistics
746 Evol Ecol (2013) 27:739–753
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
=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
=1.865 115
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
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
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
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
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
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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... Aposematic coloration is common among other brightly coloured anurans (e.g., many species within Dendrobatidae and Mantellidae), and has been shown to vary among and within populations (Klonoski et al., 2019;Maan & Cummings, 2008;Rojas et al., 2014;Roland et al., 2017;Summers & Clough, 2001;Tarvin et al., 2017). Variation in the colour pattern of aposematic species is often attributed to the interplay between ecological and sexual selection (Maan & Cummings, 2008;Nokelainen et al., 2012;Rojas & Endler, 2013). Future studies of red-eyed treefrogs that test the role of colour pattern in predator avoidance would inform how ecological and sexual selective pressures interact to shape colourpattern distribution. ...
Investigating the spatial distribution of genetic and phenotypic variation can provide insights into the evolutionary processes that shape diversity in natural systems. We characterized patterns of genetic and phenotypic diversity to learn about drivers of color-pattern diversification in red-eyed treefrogs (Agalychnis callidryas) in Costa Rica. Along the Pacific coast, red-eyed treefrogs have conspicuous leg color patterning that transitions from orange in the north to purple in the south. We measured phenotypic variation of frogs, with increased sampling at sites where the orange-to-purple transition occurs. At the transition zone, we discovered the co-occurrence of multiple color-pattern morphs. To explore possible causes of this variation, we generated a SNP dataset to analyze population genetic structure, measure genetic diversity, and infer the processes that mediate genotype-phenotype dynamics. We investigated how patterns of genetic relatedness correspond with individual measures of color pattern along the coast, including testing for the role of hybridization in geographic regions where orange and purple phenotypic groups co-occur. We found no evidence that color-pattern polymorphism in the transition zone arose through recent hybridization. Instead, a strong pattern of genetic isolation by distance (IBD) indicates that color-pattern variation was either retained through other processes such as ancestral color polymorphisms or ancient secondary contact, or else it was generated by novel mutations. We found that phenotype changes along the Pacific coast more than would be expected based on genetic divergence and geographic distance alone. Combined, our results suggest the possibility of selective pressures acting on color pattern at a small geographic scale.
... Field evidence supports our results on the correlated evolution of aposematism and phytotelm-breeding, which might have enabled the further diversification of microhabitat use in the context of reproduction in aposematic dendrobatids. In species that transport tadpoles to arboreal phytotelmata, parents could be under high predation risk as they climb trees without concealing structures (e.g., leaf litter) and with reduced understory coverage, limiting the availability of places to hide if detected by a potential predator 25,88,89 . Parents may also prefer to go far from their territories to deposit their tadpoles as an offspring dispersal strategy to reduce competition and inbreeding 33,90 . ...
Full-text available
Many organisms have evolved adaptations to increase the odds of survival of their offspring. Parental care has evolved several times in animals including ectotherms. In amphibians, ~ 10% of species exhibit parental care. Among these, poison frogs (Dendrobatidae) are well-known for their extensive care, which includes egg guarding, larval transport, and specialized tadpole provisioning with trophic eggs. At least one third of dendrobatids displaying aposematism by exhibiting warning coloration that informs potential predators about the presence of defensive skin toxins. Aposematism has a central role in poison frog diversification, including diet specialization, and visual and acoustic communication; and it is thought to have impacted their reproductive biology as well. We tested the latter association using multivariate phylogenetic methods at the family level. Our results show complex relationships between aposematism and certain aspects of the reproductive biology in dendrobatids. In particular, aposematic species tend to use more specialized tadpole-deposition sites, such as phytotelmata, and ferry fewer tadpoles than non-aposematic species. We propose that aposematism may have facilitated the diversification of microhabitat use in dendrobatids in the context of reproduction. Furthermore, the use of resource-limited tadpole-deposition environments may have evolved in tandem with an optimal reproductive strategy characterized by few offspring, biparental care, and female provisioning of food in the form of unfertilized eggs. We also found that in phytotelm-breeders, the rate of transition from cryptic to aposematic phenotype is 17 to 19 times higher than vice versa. Therefore, we infer that the aposematism in dendrobatids might serve as an umbrella trait for the evolution and maintenance of their complex offspring-caring activities.
... Due to its dependence on predators being able to easily recognize defended prey, aposematic signals are expected to be under stabilizing selection and to therefore exhibit reduced variation (Poulton, 1890;Borer et al., 2010). Species with colour-based aposematic signals nevertheless show considerable variation (Rojas & Endler, 2013). In a recent review, Briolat et al. (2019) highlighted the need to consider both the genetic underpinnings of signal production and the variety of potential selection pressures at play in order to understand how such variation can persist (Briolat et al., 2019). ...
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Despite the fact their coloration functions as an aposematic signal, and is thus expected to be under stabilizing selection, hibiscus harlequin bugs (Tectocoris diophthalmus) show an impressive level of variation in their iridescent coloration both within and between populations. To date the heritability of coloration in this species remains unknown. Here we focus on a single population in New South Wales (the southern part of this species’ Australian range), with the greatest colour variation. We reared full-sib families of known pedigree in the laboratory and analysed the extent of iridescent coloration at adulthood. We then looked for evidence of heritability, condition dependence and antagonistic sexual selection acting on colour in this species. We found significant heritability in the extent of iridescent coloration for both sexes, as well as in development time and body size, but no evidence that condition dependence played a role in the determination of adult coloration. There was, however, a sex by genotype interaction for iridescent cover, in the form of a negative intersexual genetic correlation: in families where sons had high iridescent cover the daughters had low, and vice versa. Our results suggest that different selective pressures may act on coloration in males and females of this species.
... for the chromatic part of the abdomen pattern ([red area/chromatic area] × [blue area/chromatic area], adapted from Rojas and Endler 2013). We used this pattern contrast value to describe the relative abundance between red and blue. ...
How animals assess information encoded in individual color patches have been extensively studied, yet the role of both individual color patches and gross color pattern (i.e., the combination of color patches) remains understudied. We tested the functioning of both individual color patches and gross color pattern in sexual selection using the jumping spider Siler semiglaucus as a study system. We first quantified sexual dimorphism in S. semiglaucus in both individual patches and gross color pattern using the newly developed quantitative color pattern analysis (QCPA) framework. After detecting sexual differences in color coverage and pattern contrast, we manipulated the abdomen color pattern of males and had them engage in both female mate choice and male contest trials. Females spent more time watching males with lower pattern contrast and greater red coverage during mate assessment, suggesting that they evaluate information from both individual patches and gross color pattern of males. However, male color pattern had no significant effect on the outcomes of male contests. Thus, we suggest that the observed sexual color pattern dimorphism evolved primarily through female mate choice in S. semiglaucus. This is the first study to use QCPA framework to quantify sexual dimorphism in within-pattern conspicuousness from an intraspecific perspective in invertebrates. Our study also highlights the importance of both individual color patches and gross color pattern in sexual selection.
... (3) Colour polymorphisms and colour change Colour polymorphisms (Table 1) can persist as a result of assortative mating, fitness trade-offs of correlated characters, or gene flow from neighbouring populations. They can also Ecology of protective coloration result from predation pressure: background matching against different microhabitats, as responses to spatio-temporal variation in ecological conditions, or frequency-dependent selection resulting from predator search-image formation (see Nokelainen et al., 2012;Rojas & Endler, 2013;McLean & Stuart-Fox, 2014;Price et al., 2019). Venerated examples of colour polymorphisms that involve background matching to different microhabitats are the normal and melanistic forms of the peppered moth Biston betularia (Grant, 2012) and the pelage colour of oldfield mice Peromyscus polionotus (Belk & Smith, 1996). ...
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The strategies underlying different forms of protective coloration are well understood but little attention has been paid to the ecological, life-history and behavioural circumstances under which they evolve. While some comparative studies have investigated the ecological correlates of aposematism, and background matching, the latter particularly in mammals, few have examined the ecological correlates of other types of protective coloration. Here, we first outline which types of defensive coloration strategies may be exhibited by the same individual; concluding that many protective coloration mechanisms can be employed simultaneously, particularly in conjunction with background matching. Second, we review the ecological predictions that have been made for each sort of protective coloration mechanism before systematically surveying phylogenetically controlled comparative studies linking ecological and social variables to antipredator defences that involve coloration. We find that some a priori predictions based on small-scale empirical studies and logical arguments are indeed supported by comparative data, especially in relation to how illumination affects both background matching and self-shadow concealment through countershading; how body size is associated with countershading, motion dazzle, flash coloration and aposematism, although only in selected taxa; how immobility may promote background matching in ambush predators; and how mobility may facilitate motion dazzle. Examination of nearly 120 comparative tests reveals that many focus on ecological variables that have little to do with predictions derived from antipredator defence theory, and that broad-scale ecological studies of defence strategies that incorporate phylogenetics are still very much in their infancy. We close by making recommendations for future evolutionary ecological research.
... Coupled with the unique patterning of D. tincorius that emerges in late metamorphosis and settles in adulthood (Courtois et al., 2012;Rojas & Endler, 2013), tags can provide early life identification that could be followed by pattern recognition, enabling individual discrimination throughout an individual's entire lifespan. Bainbridge et al. (2015) report recently metamorphosed VIE tag retention to be high (88-95%); we also find that tags that lasted throughout larval development persisted across metamorphosis and into terrestrial life. ...
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Animals are often difficult to distinguish at an individual level, and being able to identify individuals can be crucial in ecological or behavioral studies. In response to this challenge, biologists have developed a range of marking (tattoos, brands, toe-clips) and tagging (banding, collars, PIT, VIA, VIE) methods to identify individuals and cohorts. Animals with complex life cycles are notoriously hard to mark because of the distortion or loss of the tag across metamorphosis. In amphibians, few studies have attempted larval tagging and none have been conducted on a tropical species. Here, we present the first successful account of VIE tagging in early larval stages (Gosner stage 25) of the dyeing poison frog (Dendrobates tinctorius) coupled with a novel anesthetic (2-PHE) application for tadpoles that does not require buffering. Mean weight of individuals at time of tagging was 0.12 g, which is the smallest and developmentally youngest anuran larvae tagged to date. We report 81% tag detection over the first month of development, as well as the persistence of tags across metamorphosis in this species. Cumulative tag retention vs tag observation differed by approximately 15% across larval development demonstrating that "lost" tags can be found later in development. Tagging had no effect on tadpole growth rate or survival. Successful application of VIE tags on D. tinctorius tadpoles introduces a new method that can be applied to better understand early life development and dispersal in various tropical species. Subjects Ecology, Zoology
Color and pattern are often dynamic traits that change throughout an individual's lifetime. Still, long‐term shifts in coloration have received limited attention. Dendrobatid poison frogs are a classical system in the study of color and pattern evolution in which both sexual selection and predation avoidance are thought to drive the evolution of color and pattern at the population and species level. Here, we highlight an overlooked axis of pattern diversity, within individual variation, using three species in the genus Dendrobates. We collected longitudinal photographs of individuals at the National Aquarium to test the hypothesis that patterns shift predictably throughout the lifetimes of individual frogs. In all three species, we found a consistent reduction in the relative area of aposematic color as individuals aged and that the rate of pattern shift did not differ between the sexes. Consequently, within individual variation in coloration may confound inferences from ecological studies that inherently assume individual pattern is static. Finally, we note that using simple and noninvasive photography protocols, animals in zoos and aquaria have the potential to deepen our understanding of how color and pattern change throughout the lifetimes of a wide range of species. Color and pattern often change throughout an individual’s lifetime. However, this intra‐individual variation has received limited attention. We demonstrate consistent shifts in the color patterns of three species of poison frogs through time characterized by increasing melanization.
Full-text available
Investigating the spatial distribution of genetic and phenotypic variation can provide insights into the evolutionary processes that shape diversity in natural systems. We characterized patterns of genetic and phenotypic diversity to learn about drivers of color-pattern diversification in red-eyed treefrogs ( Agalychnis callidryas ) in Costa Rica. Along the Pacific coast, red-eyed treefrogs have conspicuous leg color patterning that transitions from orange in the north to purple in the south. We measured phenotypic variation of frogs across Pacific sites, with increased sampling at sites where the orange-to-purple transition occurs. At the transition zone, we discovered the co-occurrence of multiple color-pattern morphs. To explore possible causes of this variation, we generated a SNP dataset with RAD sequencing to analyze population genetic structure, measure genetic diversity, and infer the processes that mediate genotype-phenotype dynamics. We investigated how patterns of genetic relatedness correspond with individual measures of color pattern along the coast, including testing for the role of hybridization in geographic regions where orange and purple phenotypic groups co-occur. We found no evidence that color-pattern polymorphism in the transition zone arose through recent hybridization or introgression. Instead, a strong pattern of genetic isolation by distance (IBD) indicates that color-pattern variation was retained through other processes such as ancestral color polymorphisms, ancient secondary contact or generated by novel mutations. We found that color phenotype changes along the Pacific coast more than would be expected from geographic distance alone. Combined, our results suggest the possibility of selective pressures acting on color pattern at a small geographic scale.
Anti-predator strategies can influence trade-offs governing other activities important to fitness. Crypsis, for example, might make conspicuous sexual display especially costly, whereas aposematism might reduce or remove such costs. We tested for correlates of anti-predator strategy in Oophaga pumilio, a polytypic poison frog with morphs spanning the crypsis–aposematism continuum. In the wild, males of visually conspicuous morphs display from conspicuous perches and behave as if they perceive predation risk to be low. We thus predicted that, given a choice of ambient light microhabitats, these males would use high ambient light conditions the most and be most likely to perch in high-light conditions. We found no evidence that differently colored male O. pumilio preferentially used bright microhabitats or that ambient light influenced perching in a morph-specific manner. Independent of light conditions, males from the most conspicuous population perched the least, but the most conspicuous individuals from a polymorphic population perched the most. These patterns suggest that preferences do not necessarily underlie among-morph differences observed in the wild. This could be explained, and remain consistent with theory, if risk aversion is shaped, in part, by experience.
Full-text available
Seasonal rainfall affects tropical forest dynamics and behavior of species that are part of these ecosystems. The positive correlation between amphibian activity patterns and rainfall has been demonstrated repeatedly. Members of Dendrobatidae, a clade of Neotropical dartpoison frogs, are well known for their habitat use and behavior during the rainy season, but their behavior during the dry season has received little attention. We studied habitat use and diet of the dendrobatid frog Dendrobates tinctorius in French Guiana during the rainy and dry seasons. Unlike many other dendrobatid frogs, D. tinctorius does not maintain territories for the entire rainy season. Both sexes colonize recently formed canopygaps and stay in these forest patches for only a few weeks. The frogs in these patches consume a great diversity of prey, consisting of ants, beetles, wasps, insect larvae, and mites. During the dry season, frogs move to retreat sites in mature forest, such as palm bracts and tree holes. The frogs are less active and consume fewer prey items in the dry season, and they consume fewer wasps and insect larvae, but more termites. Ants are the most common prey items during both the wet and dry seasons. We discuss the effects of shifts in seasonal habitat use on the territorial behavior of dendrobatid frogs.
Empirical studies of mimicry have rarely been conducted under natural conditions. Field investigations of some lepidopteran systems have provided a bridge between experiments examining artificial situations and the mimicry process in nature, but these systems do not include all types of mimicry. The presence of dangerous or deadly models is thought to alter the usual rules for mimicry complexes. In particular, a deadly model is expected to protect a wide variety of mimics. Avoidance of different types of mimics should vary according to how closely they resemble the model. Coral snake mimicry complexes in the neotropics may provide natural systems in which these ideas can be examined, but there is no direct evidence that the patterns of venomous coral snakes or potential mimics are avoided in the wild. Plasticine replicas of snakes were used to assess the frequency of avian predation attempts as a function of color pattern. Avian predators left identifiable marks on the replicas, the position of which indicated that replicas were perceived as potentially dangerous prey items by birds. The number of attacks on unmarked brown replicas was greater than that on tricolor coral snake banded replicas. This result was true whether replicas were placed on natural or plain white backgrounds, suggesting that coral snake banded patterns function aposematically. In a separate experiment, replicas representing all six patterns of proposed coral mimics at the study site were attacked less often than unmarked brown replicas. Within these six banded patterns, some were attacked significantly more often than others. This study provides direct field evidence that coral snake banded patterns are avoided by free-ranging avian predators and supports theoretical predictions about mimicry systems involving deadly models.
Correlational selection favors combinations of traits and is a key element of many models of phenotypic and genetic evolution. Multiple regression techniques for measuring selection allow for the direct estimation of correlational selection gradients, yet few studies in natural populations have investigated this process. Color patterns and antipredator behaviors of snakes are thought to function interactively in predator escape and therefore may be subject to correlational selection. To investigate this hypothesis, I studied the survivorship of juvenile garter snakes, Thamnophis ordinoides, as a function of a suite of escape behaviors and color pattern. The only natural selection detected favored opposite combinations of stripedness of the color pattern and the tendency to perform during escape evasive behaviors called reversals. This selection presumably results from optical illusions created by moving patterns and their effects on visually foraging predators. Analysis of the bivariate selection surface shows that pure correlational selection can be thought of as a series of linear selection functions on one trait whose slopes depend on the value of the second trait. Alternatively, viewing the selection surface along its major axes reveals stabilizing and disruptive components of correlational selection. It is further shown that correlational selection alone can promote genetic variance and covariance within a generation. This phenomenon may be partially responsible for the extreme variation in color pattern and the genetic covariance between color pattern and behavior observed in natural populations of T. ordinoides.
During the early 1960s the frequency of mimetic dark morph Papilio glaucus females increased from less than 10% to over 20% at a Highlands Co., Florida, site. This increase in the mimetic morph is probably not due to an increase in distasteful models but may be related to a severe reduction in larval and adult host plants resulting in reduced P glaucus abundance and genetic drift. Adaptive superiority of the dark morph could also contribute to its apparent increase in frequency.