Animal Behaviour 81 (2011) 1015e1021
Contents lists available at ScienceDirect
Animal Behaviour
journal homepage: www.elsevier.com/locate/anbehav
Female preference and the evolution of an exaggerated male ornament: the shape
of the preference function matters
Donelle M. Robinson a, *, M. Scarlett Tudor a, b,1, Molly R. Morris a
a
b
Department of Biological Sciences, Ohio University
Department of Biology, University of Florida
a r t i c l e i n f o
Article history:
Received 25 August 2010
Initial acceptance 8 October 2010
Final acceptance 2 February 2011
Available online 10 March 2011
MS. number: A10-00563R
Keywords:
exaggerated trait
Poeciliidae
preference function
swordtail fish
Xiphophorus birchmanni
Sexual selection theory often predicts that female preferences will produce directional selection for male
traits that either reinforces or opposes maleemale competition. However, without considering the
complexity of preference functions and the potential for adaptive variation in female mate preferences,
the direction of selection due to female preference can be misidentified. Previous studies have suggested
that female preference opposed maleemale competition in the evolution of the large, sexually dimorphic
dorsal fin in the swordtail fish, Xiphophorus birchmanni. We present two lines of evidence to suggest that
female preference selects for enlarged dorsal fins in male X. birchmanni, and therefore female preferences
are not directional for small dorsal fins, but instead are potentially disruptive. Xiphophorus birchmanni
females prefer dorsal fins that are larger than expected given the male’s size, and during maleefemale
interactions, males raise their dorsal fins as part of their courtship display directed towards females. We
argue that selection due to female preference is likely to be much more complex than is often considered.
Ó 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Historically, sexual selection theory predicted that female mate
choice and maleemale competition select for the same male traits
(Arnqvist & Rowe 2005). Female mate choice should reinforce
maleemale competition when male traits favoured by maleemale
competition are correlated with direct or indirect benefits that
females receive from those males. However, traits used in
maleemale competition may not benefit females (Qvarnström &
Forsgren 1998), and mating with males that have these traits may
be costly to females (e.g. coercion to mate), suggesting that these
two components of sexual selection may oppose one another in
some cases (Arnqvist & Rowe 2005). In addition, there is empirical
evidence for traits being favoured by maleemale competition but
not by female mate choice (e.g. cockroaches, Nauphoeta cinerea:
Moore & Moore 1999; meadow voles, Microtus pennsylvanicus:
Spritzer et al. 2005; killifish, Lucania goodei: McGhee et al. 2007;
reviewed in Arnqvist & Rowe 2005). Determining whether the two
components of sexual selection are congruent or antagonistic in the
evolution of a particular trait requires an accurate assessment of the
shape of the female mate preference function.
* Correspondence: D. M. Robinson, Department of Biological Sciences, 107 Irvine
Hall, Ohio University, Athens, OH 45701, U.S.A.
E-mail address: [email protected] (D. M. Robinson).
1
M. S. Tudor is at the Department of Biology, 220 Bartram Hall, University of
Florida, Gainesville, FL 32611, U.S.A.
Several studies have determined that female preference functions can be complex (reviewed in: Jennions & Petrie 1997;
Widemo & Sæther 1999; Candolin 2003). Distinguishing between
preference functions that produce directional selection as
compared to stabilizing or disruptive selection requires that preferences be tested in both directions (for traits that are both larger
and smaller than average) (Wagner 1998). For example, female red
bishops, Euplectes orix, prefer males with long tails over short tails.
However, additional tests determined that females also discriminate against longer tails that resemble tails of closely related
species (Pryke & Andersson 2008), suggesting stabilizing rather
than directional selection. In some populations of sailfin mollies,
Poecilia latipinna, males prefer females that are the average size in
the population (Gabor et al. 2010). The mode of selection can also
differ from trait to trait (e.g. treefrogs, Hyla versicolor: Gerhardt &
Brooks 2009). While more complete examinations of preference
functions suggest that some studies have correctly reported
directional selection due to female mate preference (e.g. birds,
Taeniopygia guttata: Clayton & Prove 1989; grasshoppers,
Chorthippus biguttulus: Klappert & Reinhold 2003; frogs, Oophaga
pumilio: Maan & Cummings 2009), the prevalence of research
reporting directional selection may be overestimated both by study
design and publication bias. Studies cannot conclude directional
selection on traits without eliminating alternative types of selection using multiple female preference tests.
0003-3472/$38.00 Ó 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.anbehav.2011.02.005
1016
D. M. Robinson et al. / Animal Behaviour 81 (2011) 1015e1021
Swordtails (genus: Xiphophorus) are livebearing fish belonging
to the family Poeciliidae and have internal fertilization. Northern
swordtails are found in streams and rivers of the Rio Pánuco River
basin in Mexico (Rosen & Bailey 1963). Both males and females
mate multiply, and females are capable of storing sperm for several
months (Constantz 1989). Xiphophorus birchmanni is the only
species of northern swordtails that has large males that do not
develop swords. However, males develop large dorsal fins that are
strongly correlated with male body size: large males have larger
dorsal fins than small males (Fisher et al. 2009).
Males in several species of swordtails raise the dorsal fin during
maleemale competition (e.g. Zimmerer & Kallman 1989; Rosenthal
et al. 2003). Xiphophorus birchmanni males are more aggressive
towards models of males with smaller dorsal fins and less
aggressive towards models with larger dorsal fins (Fisher &
Rosenthal 2007). However, the relationship between a male’s
own dorsal fin size and his aggression level has not yet been
determined. It has been hypothesized that males with larger dorsal
fins are more aggressive, and that females avoid them for that
reason (Fisher & Rosenthal 2007). In support of this idea, Fisher &
Rosenthal (2007) found that females prefer males with smaller
dorsal fins to males with dorsal fins of average size. Females also
preferred live males with relatively smaller dorsal fins for their
body size (Fisher et al. 2009). One interpretation of these results is
that female preferences exert directional selection for small dorsal
fin size. To test this hypothesis fully, however, it is necessary to
explore the other half of the preference function: to test female
preferences for larger relative to average fin sizes. This is one of the
goals of the present study. If female preference is producing
directional selection against larger dorsal fins, then we would
predict a female preference for average dorsal fins when given
a choice between average and larger dorsal fins. In addition, we
examined the use of the dorsal fin by males during courtship and
the relationship between dorsal fin size and the use of aggressive
and coercive mating behaviours. Previous research compared
males raising their dorsal fins across different social conditions to
suggest that this signal is directed towards males but not females
(Fisher & Rosenthal 2007). In the present study, we explore the use
of the dorsal fin during courtship by adding another social condition to those previously studied. If raising the dorsal fin is a signal
directed towards females, we predicted that males would raise the
dorsal fin more when they were with a female than when alone. If
males use the dorsal fin during courtship, we also predicted that
males that raised the dorsal fin more would perform more courtship behaviours. Finally, if females prefer males with smaller dorsal
fins as a means to avoid more aggressive large-finned males, we
predicted that males with larger dorsal fins would be more
aggressive towards females or use more coercive mating
behaviours.
METHODS
We collected X. birchmanni males and females from the Rio
Garces (20 560 24”N, 98 160 53”W), and males from the Rio Santa
Maria (2130 30”N, 98 21012”W) in Mexico. Fish were isolated into
19-litre aquaria on a 12:12 h light:dark cycle and fed Tetramin
flakes (Tetra, Blacksburg, VA, U.S.A.). Behavioural tests
(maleefemale interactions and female preference) occurred
between 0800 and 1400 hours. All experiments complied with
current laws and with the Animal Care Guidelines of Ohio University (Animal Care and Use Protocol No. L01-01). All statistical tests
were parametric and two tailed. Analyses were performed using
JMP 8.0 (SAS Institute, Cary, NC, U.S.A.) and R (R Project for Statistical Computing, Vienna, Austria).
Female Preferences
While a previous study found a preference for males with dorsal
fins reduced by 55% area (33% decrease in length width; Fisher &
Rosenthal 2007), we further explored the preference function by
examining female preference for average as compared to larger
dorsal fins. Females (N ¼ 17) were tested in a 39-litre aquarium
divided into three equal compartments. Females were tested with
pairs of transparencies consisting of one unaltered image
(‘average’) and one image with dorsal fin area increased by 200%
(‘larger’, 73% increase in length width; see Supplementary
Material, Fig. S1). Increased dorsal fin sizes were larger than the
absolute dorsal fin size and the relative dorsal fin size (i.e. relative
to standard length; see Dorsal Fin Size below) of all males measured
(453e748 mm2), but the absolute size was not outside of the range
of X. birchmanni from other populations (M. R. Morris, unpublished
data). Pairs of transparencies (3 pairs created from 3 males) were
created using digital photographs of the same male with dorsal fin
area altered in Paint.NET v3.08 (copyright 2009 dotpdn LLC; see
Supplementary Material). Each photograph was horizontally flipped and both images were printed onto transparencies using
a Xerox Tektronix 7760 printer (Xerox Corporation, Wilsonville, OR,
U.S.A.). White paper in the shape of the fish’s body (excluding fins)
was placed between the mirror images. We cut the photographs
from the transparencies and fastened both photographs and the
white paper together using clear double-sided tape, creating a twodimensional model with an opaque body and transparent fins.
Transparencies have been used successfully to test female preferences in poeciliids (e.g. MacLaren et al. 2004; Gumm et al. 2006;
MacLaren & Daniska 2008).
The transparency apparatus was reproduced from MacLaren
et al. (2004) to fit a 37.9-litre aquarium. The apparatus was modified to stand on metal legs without touching the aquarium, and
foam insulation was used to prevent vibrations from transferring
from the apparatus to the floor and testing aquarium. A motorized
pulley system was created using a Planetary Gear Box (Tamiya
America, Inc., Aliso Viejo, CA, U.S.A.) to move each transparency
parallel to its respective side of the aquarium. Fishing line attached
transparencies to a rectangular motorized belt with rounded
corners (33 cm long 2 cm wide) placed on both sides above the
testing aquarium. Transparencies moved clockwise 5 cm and 7 cm
from each end of the aquarium so they appeared to swim. The top
and back wall of the aquarium were covered with white plastic to
obscure the view of the apparatus.
For preference tests, the aquarium was divided by two lines into
three equal compartments. On each end of the aquarium, we placed
a transparency onto the motorized belt out of view of the focal
female. We randomly assigned the transparencies to the sides of the
aquarium. Females acclimated in a clear tube in the centre
compartment for 10 min. We then started the motor so the transparencies moved into view and ‘swam’ parallel to the aquarium.
Females observed transparencies for 2 min. After the 2 min observation, females were released from the clear tube and could interact
with the transparencies for 8 min. During the 8 min interaction, we
recorded the time females spent in the compartment adjacent to
each transparency. We re-acclimated and retested females after
switching transparencies between sides to control for side bias. A
female was scored as having a side bias when she spent less than
10 s on one of the two sides of the testing aquarium when added
across the two trials. Females with side biases were retested after
7e14 days. All females were tested again after 7 days with the same
stimulus pair. After the final trial, females were measured for
standard length. During each trial, we recorded the amount of time
the female spent in the compartment adjacent to each transparency
to measure her preference for each transparency. The difference
D. M. Robinson et al. / Animal Behaviour 81 (2011) 1015e1021
between the time females spent with each transparency across both
tests indicated strength of preference. In closely related X. nigrensis,
association time is the most consistent receptive behavioural
measure within females (measured as a low coefficient of variation
over consecutive tests; Cummings & Mollaghan 2006). Association
times have been found to be a good predictor of mate choices made
in nature. For example, association times reflected mate choice
decisions, as measured by paternity, in the field for closely related
X. multilineatus (Morris et al. 2010) and in captivity for X. helleri
(Walling et al. 2010). As strength of preference was not significantly
different between the first and second preference tests (paired
t test: t16 ¼ 0.74, P ¼ 0.472), the amount of time the female spent
with each transparency across both tests was summed to obtain
a better estimate of female preferences. We used a paired t test to
assess female preferences for larger versus average transparencies.
We used linear regression to determine whether female strength of
preference differed with female standard length. We used ANOVA to
assess whether different transparencies affected the female
strength of preference and total association time (measured as total
time spent with both the large and average transparencies).
Dorsal Fin Size
We assessed dorsal fin size in X. birchmanni to (1) relate female
preference tests to natural variation in male dorsal fin size and (2)
evaluate any correlation between male courtship behaviour and
dorsal fin size (see MaleeFemale Interactions below). The dorsal fin
sizes of both males (N ¼ 14) and females (N ¼ 10) were measured
and compared to body size and mating behaviours. Live fish were
digitally photographed with their dorsal fins raised and then were
measured for standard length with callipers. We measured standard length again with the straight line selections tool in ImageJ
(1997e2009, National Institutes of Health, Bethesda, MD, U.S.A.) to
convert from pixels to millimetres for digital photographs. Dorsal
fin area was measured with the polygon selections tool and converted from pixels to mm2. Each picture was measured three times
and the average measurements used for the analyses. We assessed
whether there is an isometric relationship between dorsal fin area
and standard length. An isometric relationship indicates that dorsal
fin area changes proportionally with standard length across the
range of measurements. Since dorsal fin area (a two-dimensional
measure) was compared to standard length (a one-dimensional
measure), the slope of the logelog regression should be 2.0 for
isometry (Warton & Weber 2002; Warton et al. 2006). From the
equation of the logelog regression between male standard length
and dorsal fin size, we also calculated the residuals for dorsal fin
size for each male (residuals ¼ observed expected dorsal fin size),
which provided us with a measure of dorsal fin size relative to male
size (hereafter ‘relative’ dorsal fin size). Males with positive residuals had dorsal fins larger than expected for their body size, while
males with negative residuals had dorsal fins smaller than expected
for their body size. We used both of these measurements (absolute
dorsal fin size and relative dorsal fin size) to examine the
relationship between dorsal fin size and male behaviours in the
maleefemale interactions.
MaleeFemale Interactions
We examined the interactions between males and females to
determine whether either the absolute or relative dorsal fin size was
correlated with male aggression and coercive mating behaviours or
courtship behaviours. Maleefemale pairs (N ¼ 16) were tested in
a 78-litre aquarium. Pairs acclimated for 10 min with the female in an
opaque chamber. The chamber was removed and the time the male
raised his dorsal fin was recorded for 10 min. Copulation attempts
1017
and male courtship behaviours (displays, headstands, gonopore
nibbling) were also recorded. Whereas we detected no aggression
(e.g. chases, bites), copulation attempts are considered a coercive
mating behaviour in livebearing fishes (e.g. Houde 1997; Pilastro
et al. 1997; Plath et al. 2007; Morris et al. 2008) and can cause
physical injury to females (R. Deaton, personal communication).
We compared the time a male raised his dorsal fin when he was
with a female to the time he raised it when alone to determine
whether raising the dorsal fin is a signal directed towards females.
Fourteen of the 16 males were also tested without females (sample
sizes varied because of the death of two males). To obtain a baseline
estimate for each male, the time a male raised his dorsal fin when
alone was recorded using the same procedure (10 min acclimation,
10 min observation). The order of the two tests (with and without
a female) was randomized. We compared male use of the dorsal fin
with and without a female using a paired t test. The difference
between the amounts of time a male raised his dorsal fin in each test
(with and without a female) was used as an indicator of his strength of
response to females, with positive values indicating that a male spent
more time with his dorsal fin raised when females were present.
Finally, we examined the relationships between the behaviours
males used when interacting with a female and the size of his
dorsal fin to determine whether female preference for smaller
dorsal fins could be explained by females avoiding more aggressive
or coercive males. We used Akaike’s (1974) Information Criterion
(AIC) to determine the most parsimonious model for explaining the
strength of response, total number of courtship behaviours (coaxing) and number of attempted copulations (coercive). AIC selects
models by weighting the residual error of each model against the
number of parameters in the model. This is especially powerful for
parameter reduction given that more parameters often explain
more variation. While its use in behavioural ecology has so far been
limited (but see Garamszegi et al. 2009), the use of AIC in biological
studies is widespread (Anderson 2008). For strength of response,
we assessed male standard length (covariate), female standard
length (covariate), male absolute dorsal fin size (covariate), relative
male dorsal fin size (covariate) and population (Santa Maria or
Garces, factor). For number of copulations, we assessed number of
courtship behaviours (covariate), male standard length (covariate),
female standard length (covariate), absolute male dorsal fin size
(covariate), relative male dorsal fin size (covariate), population
(Santa Maria or Garces, factor) and strength of response (covariate).
For total number of courtship behaviours, we assessed number of
copulations (covariate), male standard length (covariate), female
standard length (covariate), absolute male dorsal fin size (covariate), relative male dorsal fin size (covariate), population (Santa
Maria or Garces, factor) and strength of response (covariate). All
morphometrics were log transformed for the analyses. We included
all possible models with up to seven parameters (five assessed
parameters plus the intercept and error terms), as well as the null
model (includes only the intercept and error term). We did not
include the parameter male dorsal fin size in the same model as
relative male dorsal fin size. Since some models included many
parameters (K), relative to sample size (N), we used AIC corrected
for small sample sizes (Anderson et al. 2000): AICc ¼ 2k 2 ln
(likelihood) þ (2k (k þ 1))/(N k 1). The model with the
minimum AIC was considered to have the highest probability given
the data (Anderson et al. 2000). Models were ranked using AICc,
ΔAICc, and AIC weights (wi) (Anderson et al. 2000). Models with
ΔAICc less than 2 are presented since models with a lower ΔAICc are
more likely to be biologically significant and therefore are considered competing models. In addition, models with a higher wi are
more likely to be biologically significant relative to other models
considered (Anderson et al. 2000). Competing models are models
that include parameters that should be considered for explaining
1018
D. M. Robinson et al. / Animal Behaviour 81 (2011) 1015e1021
the variation in preference (Anderson et al. 2000). For the model
with ΔAICc equal to 0, we also present the ANOVA table when the
null model was rejected.
Female Preferences
Females spent significantly more time near males with the
larger
dorsal
fin
(mean SE:
larger ¼ 724.82 50.65 s,
average ¼ 547.77 39.38 s; paired t test: t16 ¼ 2.47, P ¼ 0.03;
Fig. 1). Female size (standard length) was not correlated with
strength of preference (linear regression: F1,15 ¼ 0.29, P ¼ 0.60).
Female strength of preference did not differ significantly across
male transparencies (F2,14 ¼ 1.03, P ¼ 0.383), nor did total association time differ (F2,14 ¼ 1.28, P ¼ 0.309).
Log (dorsal fin area (mm2)
RESULTS
2.6
2.4
2.2
2
1.8
1.6
1.4
1.4
1.5
1.6
1.7
1.8
Log (standard length (mm))
Dorsal Fin Size
Dorsal fin area scaled to standard length did not differ significantly from isometry for males (slope test: r ¼ 0.02, N ¼ 14,
P ¼ 0.95; logelog regression: dorsal fin area (mm2) ¼ 1.10 þ
(2.06 standard length (mm)); R2 ¼ 0.68, F1,12 ¼ 25.75, P < 0.01) or
females (slope test: r ¼ 0.39, N ¼ 10, P ¼ 0.26; logelog regression:
dorsal fin area (mm2) ¼ 1.91 þ (2.29 standard length (mm));
R2 ¼ 0.92, F1,8 ¼ 91.00, P < 0.01) (Fig. 2). Therefore, although larger
individuals have larger dorsal fins, the geometric relationship
between dorsal fin size and body size is maintained within each sex
of this species. Males always had larger dorsal fins than females
(mean SE: males: 247.7 14.0 mm2, range 163.9e347.6 mm2,
N ¼ 14; females: 64.9 6.2 mm2, 32.2e90.2 mm2, N ¼ 10).
MaleeFemale Interactions
Males raised their dorsal fin significantly more when a female
was present than when no other fish was present (paired t test:
t14 ¼ 4.00, P ¼ 0.001; Fig. 3), suggesting that raising the dorsal fin is
a signal directed at females. The model that best explained variation in male strength of response to females (strength of response ¼ time dorsal fin raised with female e time dorsal fin raised
without female) was the null model (intercept), indicating that
none of the assessed parameters, including either of the measures
Figure 2. Isometry of the dorsal fin size (mm2) and body size (standard length) in
Xiphophorus birchmanni. Open circles: females; closed circles: males.
of dorsal fin size, explained variation in strength of response. The
null model also best explained variation in the number of copulations (coercive behaviour). The model that best explained variation
in the total number of male courtship behaviours (coaxing behaviours) included strength of response and absolute dorsal fin size
(Table 1). This was the only candidate model (ΔAICc < 2) for male
courtship behaviours. This model significantly explained variation
in the total number of courtship behaviours (ANCOVA: R2 ¼ 0.53,
F2,11 ¼ 6.30, P ¼ 0.015). Males with a greater strength of response
courted more (ANCOVA: b ¼ 0.023, F1,11 ¼ 6.90, P ¼ 0.024; Fig. 4a)
as did males with smaller dorsal fins (b ¼ 45.2, F1,11 ¼ 6.05,
P ¼ 0.032; Fig. 4b). These results suggest that males that court more
raise their dorsal fin more, and that smaller males with smaller
absolute dorsal fins court more. Because of the tight correlation
between male size and dorsal fin size, it was not possible to
determine whether body size or dorsal fin size was more important
in this case. Therefore, we performed an additional ANCOVA to
investigate these effects separately by separating absolute dorsal
fin size into the variables male standard length and relative dorsal
fin size (based on residuals). This model explained a similar amount
of variation in the total number of courtship behaviours as the prior
800
600
300
Time raised (s)
Association time (s)
400
400
200
0
200
100
Average
Large
Transparency
Figure 1. Mean SE time that female Xiphophorus birchmanni spent associating with
each transparency.
0
None
Female
Fish present
Figure 3. Mean SE time that male Xiphophorus birchmanni spent raising the dorsal
fin when a female was present or absent.
D. M. Robinson et al. / Animal Behaviour 81 (2011) 1015e1021
Table 1
Models of courtship behaviour for male Xiphophorus birchmanni
Model
K
AICc
ΔAICc
wi
Log (dorsal fin area), strength of response
Strength of response
Log (dorsal fin area)
Log (standard length), strength of response
Log (standard length)
Intercept (null model)
4
3
3
4
3
2
98.52
100.60
101.29
101.56
101.77
101.84
0
2.09
2.77
3.04
3.26
3.33
0.251
0.088
0.063
0.055
0.049
0.047
Models are ranked in order of support by Akaike’s Information Criterion (AIC).
K ¼ number of parameters included in model; AICc ¼ Akaike’s Information Criterion
corrected for small sample size; ΔAICc ¼ model AICc AICmin; wi ¼ AIC weights.
Only the first model was a candidate model with ΔAICc < 2. Additional models and
the null model are shown for comparison.
model (ANCOVA: R2 ¼ 0.54, F3,10 ¼ 3.89, P ¼ 0.044), although with
the additional parameter, the df decreased and P increased for the
overall model. Males with a greater strength of response still
significantly courted more (ANCOVA: b ¼ 0.024, F1,10 ¼ 6.16,
P ¼ 0.032). However, with the separation of absolute dorsal fin size
into its two components, we found no significant relationship
between male standard length and the number of courtship
behaviours (ANCOVA: b ¼ 81.49, F1,10 ¼ 3.26, P ¼ 0.101) or
between relative dorsal fin size and the number of courtship
behaviours (b ¼ 54.12, F1,10 ¼ 2.55, P ¼ 0.141).
DISCUSSION
Total courtship behaviours
The evolution of the sexually dimorphic dorsal fin of X. birchmanni has been described as an example of selection due to female
preference opposing selection due to maleemale competition
(Fisher & Rosenthal 2007; Fisher et al. 2009). However, we present
evidence to suggest that female preference was involved in the
evolution of the enlarged dorsal fins in males of this species. Given
a choice between average and larger dorsal fin sizes, females
preferred the model male with the larger dorsal fin. A preference for
larger dorsal fins suggests that at one end of the preference function
female preferences would reinforce male competition, which selects
for larger dorsal fins, while at the other end of the preference function females prefer smaller dorsal fins (Fisher & Rosenthal 2007).
Together, these studies suggest that females may prefer dorsal fin
sizes that deviate in either direction from average (disruptive
selection). We also demonstrated that males raise the dorsal fin as
part of courtship behaviour even when other males are not present,
and that the propensity to raise the dorsal fin in the presence of
females is correlated with the use of other coaxing behaviours
during courtship. Therefore, the results of the maleefemale interaction study suggest that raising the dorsal fin is a signal directed
towards females, and that the dorsal fin plays a key role in courtship.
30
Several hypotheses could explain female preference for larger
dorsal fins. However, the empirical data we currently have is
insufficient to distinguish between these possibilities. First, an
advantage of mating with males with larger dorsal fins could have
driven the female preference beyond its natural selection optimum
(Fisher 1930). Second, as dorsal fins are assessed in maleemale
competition, dorsal fin size may have indicated male genetic or
phenotypic quality and females may use the dorsal fin as a means of
detecting superior fathers for their offspring. Third, female preferences for larger male traits can evolve as mechanisms to reinforce
species barriers (Gerhardt 1991; Servedio & Noor 2003). The preference for larger dorsal fins we detected could have evolved as
a species-specific cue in X. birchmanni, as this species has larger
dorsal fins relative to body size than any of the other species of
northern swordtails (Rauchenberger et al. 1990; D. M. Robinson,
unpublished data). The populations of X. birchmanni we examined
are currently sympatric with only one other species of Xiphophorus
(X. variatus), in which males have much smaller dorsal fins than
X. birchmanni males. Fourth, a pre-existing preference for large
males could have led to the large dorsal fins in X. birchmanni, as
they make the males appear larger. A pre-existing preference for
large males has been suggested as a mechanism for the origin of the
swordtail in Xiphophorus (Basolo 1990; Rosenthal & Evans 1998).
A sensory bias for large male body size also has been proposed as
the mechanism involved in the origin of the preference for enlarged
dorsal fins in the sailfin males of Poecilia latipinna (MacLaren et al.
2004) and for preferences for large male traits in general (Endler
1992; Ryan & Keddy-Hector 1992; Arnqvist 2006). To determine
whether the preference we detected for enlarged dorsal fins originated from sensory bias, historical inferences would be useful to
demonstrate the preference for larger dorsal fins evolved before the
enlarged dorsal fins in males. Finally, a preference for a large male
trait could be the outcome of antagonistic coevolution. When there
are costs to mating with males with particular traits, the amount of
stimulation required for females to respond to male traits may
increase (Rosenthal & Servedio 1999; Gavrilets et al. 2001). In this
situation, a coevolutionary arms race between female preferences
and male traits may occur, and female preferences may become so
extreme that no existing male traits are exaggerated enough to be
preferred. Considering the lack of aggression and the positive
relationship between courtship behaviours and raising the dorsal
fin, we have no evidence that sexual conflict by overt aggression is
currently influencing female preference for dorsal fin size.
Fisher and colleagues (Fisher & Rosenthal 2007; Fisher et al.
2009) explained the evolution of a preference for smaller dorsal
fins in X. birchmanni as evidence of antagonistic coevolution
(Arnqvist & Rowe 2005). While the preference we detected for large
dorsal fins does not necessarily rule out this hypothesis, there are
several other lines of evidence suggesting that it is unlikely.
30
(a)
20
20
10
10
0
−300
−100
100
300
500
Strength of response (s)
1019
0
2.2
(b)
2.3
2.4
2.5
Log (dorsal fin area (mm2))
Figure 4. Total number of courtship behaviours by male Xiphophorus birchmanni relative to (a) strength of response to females and (b) dorsal fin size.
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D. M. Robinson et al. / Animal Behaviour 81 (2011) 1015e1021
A relationship between dorsal fin size and aggression in
maleefemale interactions has not been demonstrated. We detected
no evidence of a relationship between either the absolute or relative dorsal fin size and male aggressive behaviours towards females
(no aggressive behaviours observed) or the use of coercive mating
behaviours such as attempted copulations (e.g. Houde 1997;
Pilastro et al. 1997; Plath et al. 2007; Morris et al. 2008). The only
behaviour correlated with dorsal fin size was courtship behaviours:
males with absolutely smaller dorsal fins courted more. Males with
smaller dorsal fins are smaller males that could be compensating
for being less attractive to females. Finally, female X. birchmanni
preferred larger males (Fisher et al. 2009), even though large body
size is commonly associated with more aggression during
maleemale competition (poeciliids: Hughes 1985; Riesch et al.
2006; reviewed in Arnott & Elwood 2009). Therefore, if females
are avoiding aggressive males (whether or not the aggression is
directed at females or other males), a preference for smaller males,
not larger males, would be predicted for the same females that
preferred smaller dorsal fins. More evidence that females incur
a cost to mating with males with larger dorsal fins is needed to
conclude that antagonistic coevolution can explain a preference for
males with smaller dorsal fins.
The study that detected a preference for smaller dorsal fins as
compared to average dorsal fins (Fisher & Rosenthal 2007) used
video animations as stimuli, while the current study, which detected a preference for larger dorsal fins as compared to average dorsal
fins, used transparencies. While courtship behaviour was controlled
for in both studies, the potentially more active male in the video
animations may have produced a stronger preference than the
males in our experiments (Rosenthal et al. 1996). The differences in
methodologies would not explain, however, why we detected
a preference for a larger dorsal fin over the average size fin, while
Fisher & Rosenthal (2007) detected a preference for a smaller dorsal
fin as compared to an average size fin. Therefore, given preferences
for both smaller and larger dorsal fins, hypotheses for why the
preference function may be bimodal need to be examined. One
possible explanation for this pattern within females would be
preferences for novel traits (Kokko et al. 2007). Alternatively, preference for dorsal fin size could be plastic, varying either across or
within females such that females sometimes prefer larger dorsal
fins and sometimes prefer smaller dorsal fins. Female preferences
are known to vary in both strength and direction due to several
variables, including age, condition and temporal variables
(reviewed in: Jennions & Petrie 1997; Widemo & Sæther 1999;
Cotton et al. 2006). As the same females were not tested in both
preference tests, it is not possible to know whether the disruptive
selection is driven by preferences within or across different females.
Regardless of how female preference selects for dorsal fin size, it is
clear that the behaviour of raising the dorsal fin is part of the
X. birchmanni courtship display. Recently it has been suggested that
ornaments most often arise secondarily as a way to enhance behavioural displays (Byers et al. 2010). Given the widespread use of raising
the dorsal fin during courtship in Poeciliidae (e.g. Ptacek 1998;
Rosenthal et al. 2003), the enlarged dorsal fin in male X. birchmanni
may have evolved to visually enhance the motor display of raising the
dorsal fin during courtship. The difference between our conclusion and
the conclusion of previous studies, which suggested that raising the
dorsal fin functions to deter male competitors, but not to attract
females, arises from examining this behaviour in different contexts.
Fisher & Rosenthal (2007) always tested males with an observer female
present (i.e. male with female, male with female and stimulus female,
male with female and competitor male), and found that the males
displayed more in the last social condition, with a male competitor and
female observer. We examined the time the dorsal fin was raised when
X. birchmanni males were alone as compared to being with a female.
Several studies have reported that males display more to females when
rival males are present (e.g. Bosch & Marquez 1996; Wilson et al. 2009;
Davie et al. 2010), which is the same pattern found in X. birchmanni
(Fisher & Rosenthal 2007). However, our study found that X. birchmanni
males display to females in the absence of rival males, suggesting that
these displays are not directed exclusively towards males.
It will be important to untangle the interactions between male
mating behaviours and dorsal fin morphologies, as well as the
potential for multiple, interacting female preference in X. birchmanni,
before the evolution of the preference for dorsal fin size can be fully
understood. For example, no study of X. birchmanni has investigated
how the preferences for body size and dorsal fin size interact. Given
that dorsal fin size is isometric, experimentally manipulating dorsal
fin size will result in a geometric relationship between dorsal fin size
and body size different from what females encounter in natural
males. Using live males, Fisher et al. (2009) found a preference for
males with negative residuals from the correlation between dorsal
fin and body size, suggesting that relative dorsal fin size may be the
key trait females assessed (i.e. a male with a negative residual could
have an absolutely larger dorsal fin than a male with a positive
residual). An inappropriate definition of a male trait can lead to
inappropriate conclusions about its evolution in relation to female
preference (Wiens & Morris 1996). It would also be worth assessing
whether females have additional preferences for dorsal fin shape
(e.g. morphometrics of height to width) in addition to size, as males
may vary in these aspects of the dorsal fin as well. Just as we need to
have a better description of the preference function, we need to have
a clear understanding of the aspects of the traits females are
assessing, so that it is clear when we may be measuring multiple,
independently evolving preferences as compared to one preference
based on multiple facets of the male trait.
In conclusion, detecting female preferences for both smaller
dorsal fins (Fisher & Rosenthal 2007) and larger dorsal fins (current
study) suggests that the evolution of female preference functions
are likely to be much more complex than previously appreciated,
requiring more complex models to understand their evolution
(Rowe et al. 2005). In addition, it is clear that the validity of our
conclusions about the relative roles of female preference and
maleemale competition in selecting for an exaggerated male trait
rely on a more complete evaluation of the range of female preferences
given a range of male trait values. Determining whether female
preferences vary across time or environments, as well as examining
how multiple preferences interact, is essential in describing the type
of selection female mate preference is producing.
Acknowledgments
We thank Julie Bauerschmidt, Theresa Beham, Shawn Conaster
and Sarah Klim for assistance with trials, Geoff Baker, Kevin de
Queiroz and Oscar Rios-Cardenas for assistance in the field, and the
Mexican government for collection permits. Funding was provided
by grants from the National Science Foundation (IBN 9983561) and
Ohio University (Research Incentive) to M.R.M., and by an Ohio
Center for Ecology and Evolutionary Studies fellowship to D.M.R.
Supplementary Material
Supplementary material associated with this article is available,
in the online version, at doi:10.1016/j.anbehav.2011.02.005.
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