An Indirect Cue of Predation Risk Counteracts Female
Preference for Conspecifics in a Naturally Hybridizing
Fish Xiphophorus birchmanni
Pamela M. Willis1*, Gil G. Rosenthal2,3, Michael J. Ryan1
1 Section of Integrative Biology, University of Texas at Austin, Austin, Texas, United States of America, 2Department of Biology, Texas A & M University, College Station,
Texas, United States of America, 3 Centro de Investigacio?n Cient??fica de las Huastecas ??Aguazarca??, Calnali, Hidalgo, Mexico
Abstract
Mate choice is context dependent, but the importance of current context to interspecific mating and hybridization is largely
unexplored. An important influence on mate choice is predation risk. We investigated how variation in an indirect cue of
predation risk, distance to shelter, influences mate choice in the swordtail Xiphophorus birchmanni, a species which
sometimes hybridizes with X. malinche in the wild. We conducted mate choice experiments to determine whether females
attend to the distance to shelter and whether this cue of predation risk can counteract female preference for conspecifics.
Females were sensitive to shelter distance independent of male presence. When conspecific and heterospecific X. malinche
males were in equally risky habitats (i.e., equally distant from shelter), females associated primarily with conspecifics,
suggesting an innate preference for conspecifics. However, when heterospecific males were in less risky habitat (i.e., closer
to shelter) than conspecific males, females no longer exhibited a preference, suggesting that females calibrate their mate
choices in response to predation risk. Our findings illustrate the potential for hybridization to arise, not necessarily through
reproductive ??mistakes??, but as one of many potential outcomes of a context-dependent mate choice strategy.
Citation: Willis PM, Rosenthal GG, Ryan MJ (2012) An Indirect Cue of Predation Risk Counteracts Female Preference for Conspecifics in a Naturally Hybridizing Fish
Xiphophorus birchmanni. PLoS ONE 7(4): e34802. doi:10.1371/journal.pone.0034802
Editor: Vincent Laudet, Ecole Normale Supe?rieure de Lyon, France
Received August 15, 2011; Accepted March 8, 2012; Published April 18, 2012
Copyright: 
 2012 Willis et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was funded by grants to PMW from the Society for Integrative and Comparative Biology, the Southwestern Association of Naturalists, the
American Livebearer Association, and the PADI Foundation grants. PMW was supported by a Zoology Scholarship Endowment for Excellence Fellowship from the
University of Texas. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: pamwillis@utexas.edu
Introduction
Mate choice is influenced by multiple factors, including mate
preference and the current context in which mate choice decisions
are made [1,2]. Internal and environmental conditions influence
the costs and benefits individuals accrue from their choice of mate.
As a result, mate choice often varies according to environmental
factors such as the level of predation risk [3,4] or the density of
potential mates [5,6], and attributes of the choosers themselves
such as age, condition, or reproductive state [7?9]. For example,
female tu?ngara frogs become less choosy about potential mates as
the time remaining for successful reproduction declines [10].
Factors that alter mate choice can in turn affect the strength of
sexual selection acting on, or the targets of sexual selection in, the
opposite sex. Context-dependent variation in mate choice is
therefore important because it may influence evolution by sexual
selection; for example, the evolution of novel male traits or the
ease of speciation [1,11?12].
While the context-dependence of mate choice within species is
well-recognized, less consideration has been given to the possibility
that mate choice between species is similarly influenced by current
internal and environmental conditions and can result in
hybridization. There is evidence, however, that changing condi-
tions can, by altering or constraining mate choice, make
hybridization more likely [13?17] For example, in hybridizing
populations of grebes (Aechmophorus occidentalis and A. clarkii), males
increasingly pursue heterospecific females as conspecific partners
become scarce over the breeding season [14]. Understanding the
extent to which context-dependent mate choice can promote or
inhibit hybridization is important because of its potential to affect
the origin, loss, and fate of evolutionary lineages through
interspecific gene flow (see [18?20]).
A prominent influence on mate choice is predation risk [1]. For
many species, mate sampling increases the risk of being detected
by predators (e.g., [21]) and individuals often become less choosy
when predation risk is high (e.g., [4,22]). For example, female sand
gobies (Pomatoschistus minutus) prefer large colorful males, but
become indiscriminate around predators [3]. Predation risk might
similarly decrease choosiness in potentially hybridizing individuals
and thereby increase the chance of hybridization, although this
hypothesis has not been tested experimentally.
Many animals rely heavily on indirect cues, such as the distance
to cover or level of illumination, to assess the risk of predation
[23,24], and perceived predation risk increases with distance to
cover in many species, including fish (e.g., [25,26]). Here we
investigate whether variation in the distance to shelter influences
female mate choice in the swordtail fish Xiphophorus birchmanni.
Hybridization and introgression occur between this species and its
congener, X. malinche, in several tributaries of the R??o Pa?nuco basin
in Hidalgo, Mexico [27,28]. First generation hybrids occur at very
low frequencies, with a greater preponderance of backcross
PLoS ONE | www.plosone.org 1 April 2012 | Volume 7 | Issue 4 | e34802
individuals and later generation hybrids [28]. The two species
inhabit shallow rocky streams subject to seasonal flooding and
drought [29], and likely experience considerable variation in
predation pressure, to which swordtails attend [30,31]. Males of
each species differ morphologically in several ways [27,29].
Previous studies have shown that female X. birchmanni typically
prefer the cues of conspecific males over those of X. malinche
[32,33], but that their choice of mate can vary with environmental
conditions [32,34]. Xiphophorus birchmanni is therefore an excellent
model for investigating the effects of predation risk on female
choice. We experimentally tested female sensitivity to predation
risk, and whether it influences their choice of conspecifics over
heterospecifics.
Methods
Ethics Statement
All research was conducted in compliance with the Guide for
the Care and Use of Laboratory Animals. This study was
approved by the Institutional Animal Care and Use Committee
at The University of Texas, protocol number 07012201. All efforts
were made to maximize animal welfare.
Fish Collection and Experimental Design
We collected X. birchmanni from Garces (20u569240N,
98u169540W), and X. malinche from Chicayotla (20u559260N,
98u349350W) [28], in 2008 and 2009. Subjects and stimuli, all
sexually-mature, were either wild-caught or first-generation
descendents. Females were isolated from males for at least two
weeks before testing.
Water was conditioned with Prime (Seachem Laboratories Inc,
Georgia, USA) and carbon-filtered for $24 hrs before use. Two
filtered 500 W halogen lamps provided downwelling irradiance
(UV and visible) comparable to that of natural Xiphophorus habitat,
following [35]. The sides of the test aquarium (76630630 cm)
were lined with Teflon and overlain with filter gels, providing
diffused horizontal irradiance [35].
Fifteen females were individually offered the choice between
conspecific and heterospecific (X. malinche) males, presented at
opposite ends of the test tank behind clear, UV-transmittant,
porous barriers (Fig. 1). The barriers prevent physical interactions
between the sexes, while allowing female access to male visual and
olfactory cues, both important in X. birchmanni mate choice
[32,33]. Males were presented in randomly-assigned groups of
three per side to allow females access to within-species phenotypic
variation and to reduce male stress (as can occur when males are
presented individually, PMW pers. obs.); this design also
approaches the setting in the wild, where swordtails occur in
large social groups and males court in the presence of other males
[36]. Each pair of male groups served as stimuli for three to five
females. One X. malinche male died during the experiment, and was
replaced by a similarly-sized male.
In many species, perceived predation risk increases with
distance to cover (e.g., [25,26]). Swordtails are reluctant to
venture far from cover in both the wild [29] and in the lab, and
seek shelter immediately when startled (PMW, pers. obs.). We used
distance to shelter as an indirect cue of predation risk. Females
spontaneously took cover underneath a central shelter (a 7.5 cm
diameter sponge filter) upon introduction to the tank. Emergence
from beneath the shelter, followed by visits to both sides of the
tank, marked the onset of a 3 min acclimation period. We then
conducted two consecutive, 5 min trials: one with the shelter
equidistant from either male compartment, and one with it closer
to the heterospecific side (Fig. 1). Trial order was alternated
between females. To minimize disturbance to the fish between
trials, the shelter was moved remotely by overhead pulley very
slowly over a ,30 sec period, without removing the fish from the
tank. If the first trial was the one with the shelter equidistant from
either side, we moved the shelter halfway to the offset position, and
then returned it to the center, so as to introduce a comparable
amount of shelter movement over the two trials, regardless of trial
order. Trials in which the female either hid or was inactive for
over half the trial were declared void. As a measure of mate choice
we recorded association time with each male stimulus, which
predicts mate choice and reproductive success in Xiphophorus (e.g.,
[37?39]). We collected data using the automated EthoVision XT
video tracking system (version 5.0, Noldus Information Technol-
ogy, Wageningen, Netherlands). Tanks were emptied, rinsed, and
dried between females.
The shelter was visible to males as well as females, allowing for
the possibility that males might (also) respond to changes in shelter
position. If so, any treatment effect could reflect female responses
to changes in male behavior, rather than the distance to shelter.
We controlled for potential male-shelter interactions in two ways.
First, we recorded two uncorrelated (Pearson r = 0.04) measures of
male behavior: the number of aggressive events among males
within the group (bite attempts and lateral displays, [40]) and
overall group activity (total time during which at least one male is
actively moving). This allowed us to account for any variation in
female behavior arising due to changes in these (or other
correlated) male behaviors (see ?Statistical analyses?). Second, we
repeated the experiment without males. This allowed us to observe
the influence of shelter position alone on female behavior.
Statistical Analyses
We used linear mixed models to examine the influence of shelter
distance, male species (or side, for trials with no male stimuli), and
their interaction on female association time. In the presence of
a significant interaction, we performed nested contrasts to evaluate
the difference in association time between male species (or side)
Figure 1. Experimental tank design. Shaded regions represent
shelter (circles) and zones (rectangles) in which association time was
recorded. Upper panel = shelter equidistant from either male compart-
ment. Lower panel = shelter closer to the heterospecific compartment.
c = conspecific male compartment, h = heterospecific male compart-
ment. Drawn to scale. Representative paths of a subject female over
two consecutive trials are shown.
doi:10.1371/journal.pone.0034802.g001
Predation Risk Counteracts Conspecific Preference
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within each treatment. We used a maximum likelihood protocol
implemented by the lme4 package of R. Female ID and male pair
group were treated as random effects to account for the non-
independence of within-subject and within-male-group measures.
Treatment order was included as a covariate. For trials including
male stimuli, male aggression and overall activity were also
included as covariates. We used the second-order Akaike In-
formation Criterion (AICc) for model selection [41], using the
MuMIn package in R. As no competing models ranked highly (i.e.
delta AICc,2), model averaging was unnecessary [41]. Model
residuals were examined to ascertain assumptions of normality and
homogeneity of variances were met.
Conventional significance testing of fixed effects in mixed
models is a contentious issue, primarily because it is not clear how
to calculate the appropriate degrees of freedom [42]. As null
hypothesis testing is a familiar paradigm for many biologists, we
used Markov chain Monte Carlo sampling (10000 samples) of the
posterior distribution of the parameters to generate 95% posterior
density credibility intervals and p-values [42] using the pvals.fnc
function in the languageR library of R.
Results
Females preferentially associated with conspecific males when
the shelter was equidistant from either species (nested contrast,
PMCMC = 0.018; Figure 2A). When the shelter was closer to the
heterospecific side, females no longer exhibited a preference
(nested contrast, PMCMC = 0.123; linear mixed model, significant
male-species-by-shelter-position interaction; Table 1, Figure 2A).
A significant effect of male species was also detected, with females
associating more with conspecifics overall (Table 1). The two
measures of male behavior, aggression and activity, decreased
model fit considerably (DAIC = 7.249), and were not retained in
the final model. No other significant effects were detected (Table 1).
In the absence of males, and with the shelter equidistant from
either side, females spent their time equally on either side (nested
contrast, PMCMC = 0.225; Figure 2B). With the shelter offset,
however, females spent more time on the side nearest the shelter
(nested contrast, PMCMC = 0.005; Figure 2B), resulting in a signif-
icant side-by-shelter-position interaction (Table 1). No other
significant effects were detected (Table 1).
Discussion
In many species, searching for and choosing among potential
mates can conflict with predator avoidance (e.g., [21]), causing
individuals to adjust their mate choices to the level of risk [3?4,22].
We have shown that, when conspecific and heterospecific males
are equally distant from shelter, female X. birchmanni prefer
conspecifics. Such conspecific preferences are widespread in many
taxa, and are important in limiting gene flow between many
closely-related species in sympatry [43?45]. However, we have
also shown that female X. birchmanni are sensitive to the perceived
risk of predation, and adjust their mate choices accordingly. These
findings provide the first experimental evidence that predation risk
can override preferences for conspecifics among (actually or
potentially) hybridizing species. Our results are significant because
animal hybridization can be an important source of evolutionary
change [18?20]. Predation risk may therefore be important, not
only in shaping the form and strength of sexual selection within
populations (e.g., [46]), but for introducing genetic novelty
between them.
Mate sampling under threat of predation likely occurs In wild
Xiphophorus [30,47]. Cichlid fishes co-occur with all northerm
swordtail species and are likely important predators [30,48], as are
birds (GGR, unpub. dat.). Other potential predators of X.
birchmanni include the Mexican tetra (Astyanax mexicanus), eleotrid
fishes and snakes [47,49]. Seasonal flooding and drought likely
expose individuals to variation in predation risk. For example,
drought conditions frequently isolate Xiphophorus fishes in small
pools (e.g., [50?51]), potentially exposing individuals to increased
risk of predation, particularly by birds. Conditions of elevated
predation risk may constrain female mate choice and increase the
likelihood of hybridization.
Although many other species of Xiphophorus live in sympatry
with others and can hybridize in the lab, hybridization has ony
been reported for a few species pairs, and in all cases appears rare
(reviewed in [52]). In X. birchmanni, both organic pollution [32] and
encounter rates with conspecific males [34] reduce female
discrimination against X. malinche males, in addition to predation
risk as reported here. Predation risk may therefore facilitate
hybridization in the wild; however, it may be that a variety of
conditions are necessary to overcome the strong prezygotic
isolation observed in other sympatric species pairs.
Figure 2. Female time in association zones as a function of
male species and shelter position. Female time spent in either zone
in the A) presence or B) absence of male stimuli, with the shelter either
centered or offset within the tank. In A), white bars = conspecific male
side, gray bars = heterospecific male side. In B), bar color designates
opposite sides of the tank.
doi:10.1371/journal.pone.0034802.g002
Predation Risk Counteracts Conspecific Preference
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Female preference for the sword is common in many Xiphophorus
species, and this preference is considered ancestral [53]. However,
this male ornament is also attractive to predators [47], and
predation on sworded males can eliminate female preference for
the sword [31]. Swords are both absent in X. birchmanni males and
unattractive to female conspecifics [29,33], and the trait has failed
to spread across hybrid zones [27]. In the present study, predation
risk reduced female discrimination against (sworded) heterospe-
cifics, suggesting that the relationships among female preference,
sword presence and predation risk in this species may be complex.
Futures studies of the role of the sword in the patterns reported
here can help illuminate its complex role in the evolution of
Xiphophorus.
Given that predation risk influences mate choice in a wide range
of species [1], it seems likely that it can alter mate choice in other
hybridizing taxa. For example, Enos Lake stickleback species
underwent extensive hybridization and subsequent species collapse
following the introduction of an omnivorous crayfish [54?55], the
presence of which inhibits reproductive behavior in one of the
parental species [56]; however, the exact mechanisms of this
collapse are unknown. Identifying the consequences of hybridiza-
tion is important for understanding the selective forces affecting
reproductive isolation and speciation, and a well-developed
literature addresses this topic (e.g., [43,57?59]); however, less
often addressed are the behavioral causes of hybridization, which
are important for the same reason. Our findings suggest that, in
some cases, hybridization may arise as just one of the many
potential outcomes of a context-dependent mate choice strategy.
Studying the behavioral causes from this perspective may broaden
our understanding of the processes reducing or increasing
diversity.
Acknowledgments
Thanks to G. Calabrese, J. Cheng, F. Masood, S. Monsivais, J. Moran, and
S. Stapleton for assistance with data collection. Felix Breden and several
anonymous reviewers provided valuable feedback on earlier versions of the
manuscript. We thank the Mexican federal government for permission to
collect fish.
Author Contributions
Conceived and designed the experiments: PMW. Performed the experi-
ments: PMW. Analyzed the data: PMW. Contributed reagents/materials/
analysis tools: GGR MJR. Wrote the paper: PMW. Data interpretation:
PMW GGR MJR. Article revision for intellectual content: GGR MJR.
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Experiment Parameter Coefficient estimate HPDlower HPDupper PMCMC
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Shelter position 239.67 285.26 2.79 0.073
Treatment order 14.97 217.86 47.75 0.372
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Males absent Side 210.21 248.76 28.83 0.599
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Predation Risk Counteracts Conspecific Preference
PLoS ONE | www.plosone.org 5 April 2012 | Volume 7 | Issue 4 | e34802