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doi:10.1111/j.1558-5646.2007.00174.x
ASSORTATIVE MATING IN POISON-DART
FROGS BASED ON AN ECOLOGICALLY
IMPORTANT TRAIT
R. Graham Reynolds1,2,3 and Benjamin M. Fitzpatrick4,5
1 Department
2 E-mail:
4 Department
5 E-mail:
of Biology, Duke University, Durham, North Carolina 27708
[email protected]
of Ecology and Evolutionary Biology, University of Tennessee Knoxville, Tennessee 37996
[email protected]
Received March 1, 2007
Accepted May 2, 2007
The origin of new species can be influenced by both deterministic and stochastic factors. Mate choice and natural selection may be
important deterministic causes of speciation (as opposed to the essentially stochastic factors of geographic isolation and genetic
drift). Theoretical models predict that speciation is more likely when mate choice depends on an ecologically important trait that
is subject to divergent natural selection, although many authors have considered such mating/ecology pleiotropy, or “magictraits” to be unlikely. However, phenotypic signals are important in both mate choice and ecological processes such as avoiding
predation. In chemically defended species, it may be that the phenotypic characteristics influencing mate choice are the same
signals being used to transmit a warning to potential predators, although few studies have demonstrated this in wild populations.
We tested for assortative mating between two color morphs of the Strawberry Poison-Dart Frog, Dendrobates pumilio, a group
with striking geographic variation in aposematic color patterns. We found that females significantly prefer individuals of their
own morph under two different light treatments, indicating strong assortative mating based on multiple coloration cues that are
also important ecological signals. This study provides a rare example of one phenotypic trait affecting both ecological viability and
nonrandom mating, indicating that mating/ecology pleiotropy is plausible in wild populations, particularly for organisms that are
aposematically colored and visually orienting.
KEY WORDS:
Aposematism, assortative mating, coloration, Dendrobates pumilio, dendrobatidae, female mate choice, magic trait,
speciation.
Speciation—the splitting of one species into two—can be driven
by a number of potential mechanisms including genetic drift, natural selection, and sexual selection (Coyne and Orr 2004). For
species to persist as separate clusters of phenotypes, reproductive
isolation must be strong enough to prevent fusion of those clusters due to interbreeding and production of intermediate offspring.
Such isolation could be mediated through positive assortative mat3 Present Address: Department of Ecology and Evolutionary Bio-
logy, University of Tennessee, 569 Dabney Hall, Knoxville, TN
37966.
C
2253
ing among phenotypically similar individuals. Despite growing
appreciation of the potential role of hybridization in evolution
(Arnold 1997; Rieseberg 1997; Mavarez et al. 2006, Gompert
et al. 2006), most individuals of most species mate assortatively
(Mayr 1963; Mallet 2005). Thus, the evolution of mate choice is
among the most important processes generating and maintaining
biological diversity (Boake 2002).
Models have shown that when mate choice is based on an
ecologically important trait, divergence in that trait can accelerate allopatric speciation and facilitate more controversial processes of divergence-with-gene-flow (e.g., sympatric speciation
C 2007 The Society for the Study of Evolution.
2007 The Author(s). Journal compilation Evolution 61-9: 2253–2259
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or reinforcement). However, the frequency with which assortative mating and adaptation are based on the same “magic trait”
(Gavrilets 2004) is unknown and few examples from nature have
been documented (Schluter 1996, 1998; McMillan et al. 1997;
Jiggins et al. 2001; Podos 2001; Vines and Schluter 2006). In
many phytophagous insects, host plant choice by parents simultaneously affects offspring viability and causes assortative mating
(Caillaud and Via 2000; Craig et al. 2001; Berlocher and Feder
2002). However, the traits directly affecting performance in such
systems (e.g., tolerance of plant secondary chemicals) are not necessarily the same traits as those directly affecting plant choice or
mate choice and most models of speciation by host shift assume
separate genetic control of preference and performance (Diehl and
Bush 1989; Berlocher and Feder 2002; Fry 2003). Gavrilets (2004,
p. 297) distinguished models of habitat preference from “magic
trait” models in which a single trait (or set of loci) simultaneously affects ecological components of fitness and nonrandom
mating. Here we examine positive assortative mating of poisondart frogs based on their most salient ecological feature: their
bright warning-color patterns. Further, we suggest that the evolution of this trait is driving allopatric speciation of Dendrobates in
Central America.
The Strawberry Poison-Dart Frog, Dendrobates pumilio, is
a tropical dart-poison frog inhabiting the Atlantic lowland regions of Nicaragua, Costa Rica, and Panama (Leenders 2001).
This species is sexually monomorphic and exhibits bright aposematic coloration that has been shown to serve as an advertisement
of sequestered toxic alkaloids in the skin (Duellman and Trueb
1986; Zug et al. 2001). Warning color should be subject to strong
purifying selection due to the positive frequency-dependent nature of the benefit to individuals with a particular warning signal (Mallet and Joron 1999; Macedonia et al. 2002; Darst and
Cummings 2006). The effectiveness of aposematic coloration depends on a consistent signal-response system between unpalatable
prey and potential predators (Endler and Mappes 2004). New or
rare variants are more likely to be attacked if predators do not recognize them as unpalatable (Müller 1879; Guilford and Dawkins
1993). Selection against rarity leads to very uniform populations
of warning-colored species. On the other hand, warning color
variation in toxic butterflies is often dramatic, with sharp distinctions between geographic variants of the same species, divergence
between species, and even multiple “mimicry rings” within local
communities (Mallet and Joron 1999). Thus, although aposematic
coloration is subject to strong purifying selection, it shows levels
of divergence between populations that are rarely seen in other
traits. Similarly, color variation among populations of D. pumilio
in the Bocas del Toro region of Panama is one of the more dramatic examples of intraspecific morphological diversity yet discovered among vertebrates (Myers and Daly 1983; Summers et al.
2003, 2004). Isolated populations of D. pumilio in this region
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show distinct color patterns that can vary in dorsal coloration
(red, orange, blue, green, black, white, and yellow) and spotting/
speckling pattern (Myers and Daly 1983; Summers et al. 1999,
2003). Despite this diversity, D. pumilio has been considered a
single species on the basis of male advertisement call similarity
(Myers and Daly 1976) and DNA sequence similarity (Summers
et al. 1997). Mitochondrial DNA data indicate that the origin
of allopatric color morphs in the Bocas del Toro Archipelago
has occurred within the last 6000 years, a relatively recent estimate suggesting a role for strong natural or sexual selection in
the diversification of D. pumilio color pattern (Summers et al.
1997).
Research on mate choice in frogs has focused almost entirely on the use of acoustic advertisement signals (Ryan 1980;
Duellman and Trueb 1986; Schwartz 1987; Ryan and Rand 1990;
Tárano 2002; Pröhl 2003). However, many tropical poison frogs
are brightly colored and diurnal or crepuscular (Duellmann and
Trueb 1986), providing the opportunity to use visual cues in social behavior (Summers et al. 1999). Dendrobates pumilio has
color vision (Hailman and Jaeger 1974; Siddiqi et al. 2004) and
females do use visual cues in mate choice (Summers et al. 1999).
Siddiqi et al. (2004) also demonstrated that different color morphs
of D. pumilio present distinct conspicuous signals detectable by
both anuran and avian (model predator) visual systems against a
variety of spectral backgrounds. These studies raised the intriguing possibility that the same visual signals used to warn predators
of the frogs’ toxicity could also be used as intraspecific sexual
signals. If mate choice is influenced by color pattern, divergence
in warning color pattern could be driving speciation in the poison
frogs of the Bocas del Toro Archipelago.
Mating between individuals of D. pumilio from different populations has occurred in captivity; F1 offspring between D. pumilio
color morphs are viable and appear intermediate in both color
and spotting pattern (Summers et al. 2004). The F1s depicted in
figure 1 of Summers et al. (2004) seem less conspicuous than the
parentals due to their mixture of parental colors (although this
judgment may not predict predator perception). They also exhibit
distinct patterns of spectral reflectance (Summers et al. 2004) that
are probably discriminable by both avian and anuran visual systems (Siddiqi et al. 2004). This may lead to greater vulnerability
to predators (due to ineffective warning coloration) and lower attractiveness to potential mates. If so, color and spotting pattern
could be causing reproductive isolation between color morphs
by a combination of ecologically based selection and assortative
mating.
Summers et al. (1999) demonstrated assortative mating based
on color between two D. pumilio color morphs (the red Cayo
Nancy and the green Pope Island forms). Although they did not
emphasize the importance of their results for speciation study, this
represents an important example of prezygotic isolation between
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Figure 1. Mean association times for female subject frogs from (A) Isla Colon and (B) Cayo Nancy. Darkened symbols represent blue-light
trials and gray symbols represent white light trials. Vertical bars illustrate standard errors.
allopatric populations with a causal link to divergence in an ecologically important trait, warning coloration. The importance of
color was supported by eliminating male behavior (see Methods)
and performing a second set of choice tests under blue light in
which colors were indistinguishable. Assortative mate choice did
not occur under the latter conditions. The morphs studied by Summers et al. (1999) differed in color alone (red vs. green). Here, we
extend these results by testing assortative mating between morphs
that differ in both overall coloration and the presence or absence
of a melanistic spotting pattern. The Isla Colon morph is yellow/green with large black spots (Fig. 1A) and the Cayo Nancy
morph is bright red/orange with few or no spots (Fig. 1B). If both
background color and spotting pattern are used as cues for assortative mating, some level of prezygotic isolation may exist between
all pairs of the 15 distinct D. pumilio forms of the Bocas Del Toro
Archipelago in Panama.
Materials and Methods
We tested for assortative mating using a simple mate choice experiment following the protocol established by Summers et al.
(1999). Female “subject” frogs were placed into a 19-liter terrarium with half of the tank occupied by plants for cover whereas the
remainder was left clear. All frogs were left overnight in the terraria to allow for acclimatization before experimental trials were
performed. Frogs were not fed during their captive period and
were released one to two days after experimentation.
Two female “object” frogs, one Cayo Nancy morph and one
Isla Colon morph, were placed inside identical overturned clear
glass cups 8 cm from each other at the clear end of the terrarium. Because D. pumilio are sexually monomorphic, females can
be effective object “males” with regard to visual cues (Summers
et al. 1999). Females were used as object frogs instead of males
because of the males’ tendency to call during captivity, which
could possibly influence subject female choice. As in Summers
et al. (1999), object females were matched for snout-vent length
to within 1 mm to control for possible size preferences. A previously recorded call of a male from Cayo Nancy of the same
snout-vent length as the subject females was played at a consistent volume from a single speaker behind and equidistant to
the cups. Calls of D. pumilio do not vary among islands, in
fact acoustic signal variation within islands is greater than differences between islands (Myers and Daly 1976; Summers et al.
1999).
The preference of subject females was estimated as the
amount of time spent facing the object frog while within 4 cm
of the cup. An experimental trial was defined as the experimental period (16 min. and 16 sec.) during which a single female was
presented with the opportunity to select a potential mate (this time
interval was determined by the length of the recorded advertisement call).
The influence of dorsal background color versus presence or
absence of large black spots was evaluated by comparing results
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of trials performed under two different light treatments: full white
light and filtered blue light. Blue lighting regimes have been previously used to effectively homogenize the coloration of D. pumilio
of different morphs, thereby removing any color signal differences between individuals from different populations (Summers
et al. 1999). Under full white light, visual information on both
color and spotting of the object frog was available to the subject
female. Under filtered blue light, the colors of the object frogs
were indistinguishable, as they both appeared blue, although any
melanistic patterning remained in contrast to the rest of the dorsal
coloration, leaving the presence or absence of spotting pattern as
the primary visual cue available for the subject females. Filtered
blue light was created by fitting blue-green spectrum filters (one
BG-12 and one BG-23, Schott filters from BES Optics, Warwick,
RT) to two 40-watt incandescent lights placed 50 cm above the
terrarium.
Totals of 19 Cayo Nancy and 19 Isla Colon females were
tested under white light, and 10 of each morph under blue light
(small and uneven sample sizes were due to time constraints and
practical challenges in collection, housing, and manipulation). The
time a subject frog spent associating with each object frog was
recorded and the difference between the time spent with the object
of the subject’s own color morph and the alternative morph was
evaluated with a paired t-test. Variation in the degree of preference
between the two morphs and between the two light environments
was tested with a two-way ANOVA. Here, the difference in individual association time between like and unlike object frogs was
the dependent variable and the subject’s morph and the light environment were fixed effects. The difference between association
times was adequately approximated by a normal distribution for
the purposes of parametric t-tests and ANOVAs (Shapiro–Wilk
test W = 0.92, P = 0.09). Nevertheless, nonparametric statistical
tests are also reported below.
Results
The response of subject females to the object frogs was low (34%),
with many trials resulting in no choice. As a consequence, final
sample sizes were five Isla Colon females in each light treatment,
four Cayo Nancy females in the white light treatment, and six Cayo
Nancy females in the blue light treatment. This low response rate
and small sample size is consistent with other studies of mating
behavior in poison frogs (Summers et al. 1999), yet still allows
the detection of strong assortative mating. Many of the 20 (of
58 attempted) females that did respond showed a clear courtship
behavior such as stroking or nudging the glass containing the
object frog (Limerick 1980; Summers et al. 1999).
Overall, female D. pumilio spent over ten times more time
associating with their own color morph than the alternative (Fig. 1;
means and standard errors: 24.8 ± 5.85 sec vs. 1.7 ± 0.9 sec). The
difference was significantly greater than zero according to both
parametric and nonparametric tests (Table 1). Females from Cayo
Nancy appeared somewhat less responsive than the Isla Colon
females, especially under the full light conditions (Fig. 1B), but we
could not reject the null hypotheses that preference was equivalent
between light treatments and that each color morph was equally
choosy (Two-way ANOVA: r2 = 0.06, F 3,16 = 1.40, P = 0.279).
Shirley’s (1987) nonparametric two-way ANOVA also found no
support for variation in the strength of preference between color
morphs and light environments (overall Kruskal–Wallis 23df =
4.69, P = 0.196).
In contrast to results of Summers et al. (1999) for the Cayo
Nancy and Pope Island morphs (green with few or no spots),
we found that the Cayo Nancy and Isla Colon morphs show
strong assortative mating under the monochromatic blue light
treatment in addition to the full-spectrum treatment (Fig. 1). Considering only the blue light treatment, subject females spent significantly more time associating with their own morph (mean
Differences in association times of subject females with like versus unlike object “males” in Dendrobates pumilio, including all
females tested and broken down by morph (Cayo Nancy and Isla Colon, see Fig. 1) and by light treatment within morph. Statistical tests
are one-tailed.
Table 1.
Group
All
Cayo Nancy
Blue
Light
Isla Colon
Blue
Light
2256
Mean
Difference (s)
Paired t-test
t
df
P
W
P
23.1
11.4
15.5
5.25
34.8
37.2
32.4
3.72
2.74
2.54
1.32
3.24
2.99
1.71
19
9
5
3
9
4
4
0.0007
0.0115
0.0261
0.1387
0.0051
0.0202
0.0814
191.5
50
20
8
52
14
14
0.0013
0.0098
0.0313
0.1875
0.0072
0.0625
0.0520
EVOLUTION SEPTEMBER 2007
Wilcoxon signed-rank test
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difference = 25.4 sec, paired t = 3.58, 10 df, P = 0.0025;
Wilcoxon signed rank test W = 63, P = 0.0024). These results
hold even when each morph is analyzed separately (Table 1).
Discussion
Direct links between mate choice and ecologically important traits
are expected to contribute to speciation because they bring about
divergence in mating behavior as a by-product of ecological divergence. This is an attractive idea, linking sex, ecology, and evolution
in a process that could rapidly produce new species as a consequence of natural selection and without the requirement of geographic isolation. However, the probability that the same trait will
be involved in both assortative mating and ecological adaptation
has been in doubt. Recent studies in Heliconius butterflies (Jiggins
et al. 2001) and Darwin’s finches (Podos 2001) have linked mate
choice to ecologically important traits in comparisons between
recently derived species. Together with the results of Summers
et al. (1999), our study provides evidence of a direct link between
assortative mating and ecologically important warning coloration
within a single species. This result suggests that warning pattern
evolution could be driving speciation in D. pumilio in the Bocas
del Toro archipelago.
There are over 15 distinct color morphs of D. pumilio in the
Bocas del Toro region (Summers et al. 2003). Morphs are distinguished by color and/or degree of black spotting or striping that
stands in contrast to the background color (e.g., see photographs
in Siddiqi et al. 2004). Summers et al. (1999) showed assortative
mating based on color alone between the Cayo Nancy morph (orange/red with few or no spots) and the Pope Island morph (green
with few or no spots). Under the blue-light treatment, both of these
unspotted morphs appeared uniformly blue, and females failed to
choose their own color morph under these conditions of reduced
spectral information (in fact there was a slight tendency to choose
the opposite morph). Our results indicate that the contrasting pattern of black spots on a light background was adequate to maintain strong assortative mating between Cayo Nancy and Isla Colon
morphs under the monochromatic blue light conditions. Our work
and that of Summers et al. (1999) show that background color and
melanistic spotting pattern each contribute to assortative mating
in D. pumilio.
Interestingly, clinal variation in coloration also seems to be a
component of D. pumilio population structure on the mainland of
the Bocas del Toro region (Summers et al. 2003). We have similarly observed spatial variation in color pattern within a single
island, both on Isla Colon and Isla Bastimentos (R. G. Reynolds,
pers. obs.). Although assortative mating has not been tested between variants from the same island, reproductive isolation between parapatric color morphs is an intriguing possibility.
The reasons for color divergence among D. pumilio populations have yet to be completely understood. Color differences may
be ecologically neutral if all color patterns are aposematic, as long
as they are conspicuous (Siddiqi et al. 2004). The color differences
among islands may represent alternative outcomes of independent
processes of runaway (Fisherian) sexual selection whereby female
preference drives the evolution of male coloration characteristics
within constraints dictated by natural selection on aposematism
(Lande 1981; Summers et al. 1997, 1999). The problem is that
both mate choice and predator warning should often result in
strong purifying selection against rare forms (Mallet and Joron
1999; Gavrilets 2004). If frogs with abnormal color characteristics are discriminated against by potential mates and more likely
to be attacked by predators, how can novel color forms become
established?
Divergent color patterns and preferences may have become
established by a drift in small island populations (Gavrilets and
Boake 1998). Drift may result in a population passing through
an adaptive valley and subsequently climbing a new adaptive
peak. Although this is unlikely for very rugged adaptive landscapes (Barton and Charlesworth 1984), it could be facilitated by
fluctuations in the intensity of selection (e.g., if predators are occasionally extirpated from small islands), or by the existence of
complex high-fitness ridges across adaptive landscapes (“holey
adaptive landscapes” Gavrilets 1997). Alternatively, divergent coloration may result from divergent natural selection. Different color
patterns may be adapted to different light environments (Endler
1993; Boughman 2001) although this seems unlikely in the Bocas del Toro Archipelago due to the similarity of habitats among
islands (Summers et at. 2003). Different color patterns may also
be adapted to different predator communities or may be involved
in alternative Müllerian mimicry rings (Mallet and Joron 1999).
Mimicry is unknown in D. pumilio, and we have no empirical basis for speculating that different color patterns signal to different
predators. Ironically, the chemical defenses and warning signals
of poison frogs are so effective that little is known about specific
predators in nature.
In short, the causes of warning color diversity in D. pumilio
are unknown. However, the consequences for reproductive isolation are clear. Divergent color morphs mate assortatively (Table 1;
Fig. 1; Summers et al. 1999), and hybrids tend to be intermediate and distinguishable from both parents (Siddiqi et al. 2004;
Summers et al. 2004). Thus, divergence in warning color and pattern result in prezygotic isolation and likely postzygotic isolation
due to the same trait. We propose that the strawberry poison frogs
of the Bocas del Toro comprise a recent or incipient radiation
where the evolution of reproductive isolation is being driven by
warning color evolution.
ACKNOWLEDGMENTS
We wish to thank S. Alberts, Duke University, whose advice, support, contribution, and encouragement were what allowed this project to develop
EVOLUTION SEPTEMBER 2007
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and succeed. Thanks to the Smithsonian Tropical Research Institute and
staff; particularly L. Mou and M. Leone. Thanks as well to J. Fordyce,
C. Boake, M. Niemiller, S. Gavrilets, and two anonymous reviewers who
provided constructive criticism of the manuscript. We are indebted to the
Bocas del Toro Smithsonian Tropical Research Institute (STRI) research
station for assistance and support, and to the Republic of Panama and
the Autoridad Nacional del Ambiente (ANAM) for collection permits.
This project was funded by the Duke University Mellon Foundation and
Center for Latin American Studies Travel Award Committee, the Duke
University Dean’s Summer Fellowship, and the Duke University Howard
Hughes Fellowship in the Biological Sciences.
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