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Current Zoology
61 (2): 265–273, 2015
No association between brain size and male sexual behavior
in the guppy
Alberto CORRAL-LÓPEZ*, Simon ECKERSTRÖM-LIEDHOLM, Wouter VAN DER BIJL,
Alexander KOTRSCHAL, Niclas KOLM
Department of Zoology/Ethology, Stockholm University, Svante Arrhenius väg 18B. SE-10691, Stockholm, Sweden
Abstract Animal behavior is remarkably variable at all taxonomic levels. Over the last decades, research on animal behavior
has focused on understanding ultimate processes. Yet, it has progressively become more evident that to fully understand behavioral variation, ultimate explanations need to be complemented with proximate ones. In particular, the mechanisms generating
variation in sexual behavior remain an open question. Variation in aspects of brain morphology has been suggested as a plausible
mechanism underlying this variation. However, our knowledge of this potential association is based almost exclusively on comparative analyses. Experimental studies are needed to establish causality and bridge the gap between micro- and macroevolutionary mechanisms concerning the link between brain and sexual behavior. We used male guppies that had been artificially selected
for large or small relative brain size to study this association. We paired males with females and scored the full known set of male
and female sexual behaviors described in guppies. We found several previously demonstrated associations between male traits,
male behavior and female behavior. Females responded more strongly towards males that courted more and males with more
orange coloration. Also, larger males and males with less conspicuous coloration attempted more coerced copulations. However,
courting, frequency of coerced copulation attempts, total intensity of sexual behavior, and female response did not differ between
large- and small-brained males. Our data suggest that relative brain size is an unlikely mechanism underlying variation in sexual
behavior of the male guppy. We discuss these findings in the context of the conditions under which relative brain size might affect
male sexual behavior [Current Zoology 61 (2): 265–273, 2015].
Keywords
Brain size, Brain morphology, Sexual behavior, Guppy, Artificial selection, Behavioral mechanisms
Behavioral variation is ubiquitous at all biological
levels and what underlies this variation is a long-standing question in biology (Darwin, 1859; Tinbergen; 1963,
Alcock; 2013). Behavioral ecology has been incredibly
successful in elucidating the ultimate processes that
generate this variation (Milinski, 2014). Yet, to fully
understand behavior, it has become evident that more
information is needed on the mechanistic background of
behavioral variation (Bateson and Laland, 2013).
The brain, as the central unit controlling behavior, is
a logical focus of interest when investigating the mechanistic basis of behavioral variation. Indeed, the interplay between variation in brain morphology and behavioral patterns has received considerable attention
(Dunbar, 1998; Allman, 2000; Northcutt, 2002; Striedter,
2005; Hofman and Falk, 2012). For instance, relative
brain size (i.e. brain size controlled for body size), a relatively coarse attribute of brain morphology, correlates
with a wide spectrum of behavioral and behavior-related
traits, including parental care (Gittleman, 1994; GonReceived Oct. 31, 2014; accepted Feb. 20, 2015.
 Corresponding author. E-mail: [email protected]
© 2015 Current Zoology
zalez-Voyer et al., 2009a), mating system (Pollen et al.,
2007), diet (Iwaniuk and Nelson, 2001; Gonzalez-Voyer
et al., 2009b), social group size (Dunbar, 1998; Lindenfors, 2005), and migratory behavior (Sol et al.,
2005). On a finer scale, variation in brain structure is
also linked to behavioral variation as exemplified by the
relatively larger hippocampus in food caching species
(Volman et al., 1997). These comparative studies provide insights into phylogenetic patterns and suggest
ultimate explanations for the link between brain morphology and behavior. To fully understand cause and
effect, such macroevolutionary analyses should ideally
also be complemented by experimental analyses at the
within-species level (Kotrschal et al., 2013a, Kolm,
2014).
Sexual behaviors have intrigued scientists and laymen alike, even before Darwin (1871) developed the
first theories of sexual selection. However, despite a longstanding tradition in sexual selection research (Andersson, 1994; Eberhard, 1996; Ryan, 1998; Ritchie, 2007),
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how variation in sexual traits is generated and maintained in the light of strong sexual selection remains a
major question in evolutionary biology (Arnqvist and
Rowe, 2005). Furthermore, variation in aspects of brain
morphology has been suggested as a factor underlying
variation in sexual behavior at the individual and species level (Jacobs, 1996; Balaban, 1997; Boogert et al.,
2011; Kotrschal et al., 2012). For instance, brain size
correlates positively with sexual traits across several
taxa, such as bower complexity in bowerbirds (Madden,
2001), intensity of sexual selection in birds (Garamszegi
et al., 2005), and mating success determined by social
ranking in primates (Pawlowski et al., 1998). Brain size
has further been found to correlate negatively with the
degree of polyandry in bats (Pitnick et al., 2006; but see
LeMaitre et al., 2009). In addition, a negative correlation has been found between brain structure, telencephalon size, and the degree of polygamy in cichlid
fishes (Pollen et al., 2007).
Previous studies demonstrate that the link between
brain morphology and cognitive ability is likely to mediate behavioral variation in contexts such as spatial
behavior (Jacobs et al., 1990), innovation (Lefebvre et
al., 1997; Reader and Laland, 2002), and tool use (Lefebvre et al., 2002; Tebbich and Bshary, 2004), although
such comparative studies need to be interpreted with
caution (Chittka and Niven, 2009). Recent theory concerning the mechanistic background of sexual behavior
suggests that it is the positive association between cognitive abilities and brain size that affects sexual behavior (Miller, 2000, see review by Boogert et al., 2011).
Variation in cognitive ability is thought to have a strong
impact on individual fitness during mate choice for both
the signaler and the receiver of sexual signals and displays (Andersson, 1994; Shettleworth, 2010; Kotrschal
et al., 2012). The most straight-forward association between cognitive ability and sexual behavior can be observed when courtship behavior is cognitively demanding itself (Boogert et al., 2011). Some traits that are under
sexual selection consist of complex displays which involve long learning periods and much practice before
they are fully developed, as is the case with song-learning ability in certain birds (Nowicki et al., 1998; Nowicki et al., 2002). Furthermore, complexity of sexual
behavior has been suggested to vary depending on brain
morphology, such as the coevolution of brain size and
bower complexity across bowerbird species (Miller,
2000; Keagy, 2009) and brain size and acrobatic courtship displays in manakins (Lindsay et al., 2015). In view
of these findings, to address the mechanistic basis of
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sexual behavior it is important to consider sexual behavior in the light of brain morphology variation, particularly in species with a known association between brain
morphology and cognitive ability.
One experimental approach to study the link between
brain morphology, cognitive ability and behavioral traits
is manipulation of brain morphology via artificial selection. Indeed, artificial selection has proven to be a powerful tool in brain evolution research (Mery and
Kawecki, 2005; Kotrschal et al., 2013a). Work on the
recently developed brain size selection lines of guppies
Poecilia reticulata, artificially selected for large or
small relative brain size (Kotrschal et al., 2013a), has
shown considerable differences in behavior between the
lines (Kotrschal et al., 2014a), including better performance in cognitive tasks by individuals with larger
brains (Kotrschal et al., 2013a, b; Kotrschal et al.,
2014b). These brain size selection lines now offer us the
opportunity to test experimentally how known differences in brain size and cognitive ability may relate to
differences in sexual behavior.
Here we experimentally test the hypothesis that brain
size and cognitive ability affect male courtship and copulatory behavior in replicated lines of male guppies
artificially selected for large and small relative brain
size. The guppy is a model organism for sexual selection research (Kodric-Brown, 1993; Houde, 1997; Brooks and Endler, 2001; Kodric-Brown and Nicoletto, 2001;
Godin et al., 2005) and the male sexual behaviors have
been described in great detail (see Houde, 1997). Briefly,
prior to copulation, males follow and circle around the
females to display their sexual ornaments, such as their
body coloration. In addition, males swing their gonopodium (the intromittent organ of this internally fertilizing
species) in front of the females. In order to complete
copulation, males display a characteristic s-shaped (sigmoid) display in front of the female thereby seeking her
collaboration. Frequently, male guppies also exhibit a
complementary ‘sneak’ copulation behavior where they
perform coerced copulations without female consent.
Since successful courtship in the guppy requires carefully coordinated movements and awareness of behavioral cues from both male competitors and courted females (Jirotkul, 1999; Head and Brooks, 2006), we hypothesize that this places demands on multiple cognitive
traits such as perception, attention and/or decision-making. Moreover, when guppy males attempt coerced copulations, they often sneak up on females from behind
and this requires an ability to respond to and synchronize
with female movement patterns, which has been sug-
CORRAL-LÓPEZ A et al.: No association between brain size and male sexual behavior
gested to be cognitively challenging (Houde, 1997;
Fraser, 2014). In our study, we paired large- and smallbrained males with non-selected females and simultaneously examined male sexual behavior and female response behavior. If relative brain size affects sexual behavior, we predict differences between large- and smallbrained males in sexual behaviors such as courting and/
or attempting coerced copulations with the female.
1
Materials and Methods
1.1 Study system
We studied the association between brain morphology and reproductive behavior in male guppies from laboratory populations previously artificially selected for
small or large relative brain size (Kotrschal et al.,
2013a). Briefly, two relative brain size treatments (three
replicates for large- and three replicates for smallbrained, six populations in total) were performed on
animals of a large outbred laboratory population of Trinidadian guppies (Kotrschal et al., 2013a). To select for
relative brain size, brain weight data corrected for body
size were collected from 225 pairs (75 per replicate)
after they had produced two clutches each. Brains from
euthanized parents were removed under a stereomicroscope and weighed. Offspring from the top and bottom 20% were then used to set up the large- and
small-brain selection lines. To avoid inbreeding, fullsiblings were never mated. See Kotrschal et al. (2013a)
for full details on the selection experiment. These selections lines showed a 9% difference in relative brain size
in the second generation (Kotrschal et al., 2013a), and
an 11% difference in the third generation (Kotrschal et
al., 2015). Furthermore, measurements performed on a
subsample of individuals from the fourth generation
showed a 13.6% difference in relative brain size (Kotrschal et al., 2014a).
For the present experiment, we used a total of 60
males from the fourth generation, 10 individuals from
each of the three up- and down-selected lines. All fish
were removed from their parental tanks after birth and
males were isolated from females before they were
sexually mature. Once sexually mature, the fish were
transferred to single 3-L tanks containing 2 cm of gravel
with continuously aerated water. We allowed visual
contact between the tanks. The laboratory was maintained at 26°C with a 12:12 light:dark schedule, which
resulted in 25°C water temperature. Fish were fed a diet
of flake food six days per week.
1.2 Sexual behavior and physical traits
To study the association between brain size and male
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sexual behavior we measured a set of sexual behaviors
in males that were individually placed in a tank together
with a sexually mature female guppy from a non-selected laboratory population. The quantification of behavior took place in a 19 × 28 × 10 cm observation tank
with fine gravel. Water was changed every day and temperature was held constant at 25 °C. We placed the female and male guppy in the observation tank simultaneously. Both individuals were fed in their home tanks
one hour prior to the trial. Behavior of both animals was
recorded for 25 min from the top view using a Logitech
HD webcam and from the side view using a Sony HDRSR11 video camera. Six trials per day during 10 consecutive days were performed between 08:00 am and
12:00 pm. In total 30 males of each brain size selection
line (10 per replicate) were tested. We tested one individual of each replicate and brain size combination
per day, with the order randomized on each day. After
the behavioral trials, we collected measurements of physical attributes of all participating individuals. In females, we measured standard length (body length, from
the tip of the snout to the end of the caudal peduncle).
For males, we took photographs and performed image
analyses with ImageJ software v. 1.44 (Schneider et al.,
2012) to quantify their standard length, tail size and
orange coloration (all traits were corrected for body
size).
We quantified male sexual behaviors using Jwatcher
software v. 1.0. (Blumstein and Daniel, 2007). Quantification was performed blind to the treatment since only
running numbers identified individuals. We used videos
recorded from the side view to measure the characteristic male guppy courting behaviors (for detailed
description see Baerends et al., 1955; Liley, 1966): the
frequency of forward movements of the gonopodium
(‘gonopodial swings’); frequency of gonopodium thrusts
towards the female genital pore from a behind position
(‘coerced copulation attempts’); and frequency and
average duration of the characteristic s-shaped
quivering movement performed in front of the female
(‘frequency of sigmoid display’ and ‘average duration
of sigmoid display’). We also used videos from the top
view to measure the total and average time that males
actively chased the female to within the distance of an
average female body size (‘time following’ and ‘average
following bout’). In addition, we normalized every male
sexual behavior (not including latencies) between 0 and
1 using maximum and minimum values. We then obtained a score for the total intensity of male sexual behavior by summing up these values for every individual.
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Furthermore, we used top-view videos to assess female
response to male courtship. For this, we measured the
number of times that females oriented their bodies towards the male (‘orientation’), the number of times a female slowly approached the male after sigmoid displays
(‘gliding response’), and the total time a female spent
escaping from males (‘time escaping’). Orientation and
gliding response have been shown to be correlated with
the probability of accepting a given male, while the time
escaping has been shown to correlate with rejection
(Liley, 1966; Houde, 1987; Nicoletto, 1993). In addition,
a score for the total female response was obtained combining normalized values of the frequency of orientations and gliding responses.
1.3 Statistical analyses
To evaluate how male and female physical traits relate to male sexual behaviors and female responses, we
studied their correlations based on the combined data of
small- and large-brained individuals. We had clear predictions concerning these correlations based on previous
literature (Farr, 1980; Houde, 1997; Kodric-Brown and
Nicoletto, 2001; Karino and Shinjo, 2004). Therefore,
we kept the critical value (α) at 0.05 and did not correct
for multiple testing (Nakagawa, 2004).
To test for potential differences in sexual behavior
between the relative brain size selected lines, we used a
Linear Mixed-Effects Model (LMM) for every male
sexual behavior scored as the dependent variable. Full
models included brain size as a fixed effect, a random
intercept and slope for brain size for each replicate and
time of the day, female size and male physical attributes
(standard length and orange coloration) as covariates. In
addition, full models included the full interaction
between brain size and male/female attributes (lme4
syntax: y ~ brain.size * female.size * male.standardlength * male.orangecoloration + time of day + (brain.
size | replicate)). We performed a stepwise backward
model selection based on Akaike Information Criteria
(AIC), only varying the fixed effects structure (Zuur et
al., 2009). Even though the interaction in the full model
was non-significant for all of the male sexual behaviors
scored, removing it from the model resulted in a distinct
increase of the AIC value. In addition, we observed no
changes in the outcome of simpler models. Also, using
female behavior data we tested whether females responded differently to individuals of large and small relative
brain size. We again used brain size as a fixed effect and
the random intercept and slope for brain size for each
replicate. In this case the model with the lowest AIC did
not include any covariates.
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We found multiple significant correlations between
the male sexual behaviors. Therefore, to maximize the
power of the analysis and reduce the number of inferential tests, we performed a principal component analysis on the correlation matrix of the male sexual behaviors (Quinn and Keough, 2002). We excluded latencies
in the PCA since, although they were correlated with the
frequencies, these observed latency correlations did not
differ from values obtained by simulating expected
latency based on frequency data (sigmoid displays: ρ =
-0.62, P = 0.43; coerced copulation attempt attempts:
ρ = -0.68, P = 0.64; gonopodial swings: ρ = -0.43, P =
0.55). Two components presented an eigenvalue > 1.
The first principal component, which explained 41% of
the variation, was characterized mainly by three aspects:
the time that males spent following females at a close
distance, the average duration of each following bout
and the frequency of coerced copulation attempts. The
second principal component, explaining 28% of the
variation, was characterized mainly by the frequency of
gonopodial swings and the frequency and average duration of sigmoid displays (Fig. 1A). We then performed a
LMM using these components. We used an analogous
model to the one described above to test for potential
differences in sexual behavior between males with different brain sizes.
Model diagnostics showed that residual distributions
were roughly normal with no signs of heteroscedasticity.
Note that ten individuals were removed from the
analyses because they did not perform sexual behavior
during trials (5 from large-, 5 from small-brained lines).
Nevertheless, we performed analogous analyses of the
data including non-performing individuals and the results remained qualitatively identical. The final sample
size used was 50 individuals, 25 from large-brained
lines and 25 from small-brained lines. We performed all
analyses in R v.3.1.1 (R Core Team, 2013) and used
lme4 package version 1.1-7 (Bates et al., 2014) for
LMM analyses.
2
Results
Several sexual behaviors measured in large- and
small-brained male guppies correlated with their physical traits. Males with a lower proportion of orange
coloration spent significantly more time chasing the
female (r = -0.319, df = 48, P = 0.023), and showed a
tendency to perform a higher number of coerced copulation attempts, although not significantly so (r = -0.236,
df = 48, P = 0.098). In addition, larger males made a
significantly higher number of coerced copulation at
CORRAL-LÓPEZ A et al.: No association between brain size and male sexual behavior
269
Fig. 1
Principal component analysis of sexual behaviors of male guppies Poecilia reticulata, selected for large or small
relative brain size, when presented to a female
Negative values of PC1 describe higher values of coerced copulation-related sexual behaviors while positive values of PC2 describe higher values
of display-related sexual behaviors, as indicated by the direction of the arrows for specific behavioral measures. Larger symbols represent centroid
values for small- and large-brained males. No difference is observed in the set of sexual behaviors between small- (circles) and large-brained
(squares) males (A), or in the estimated marginal means and confidence intervals of a Linear Mixed Model (LMM) for values retrieved from the
first component (B) and the second component (C) with brain size as a fixed effect, replicate as a random effect and time of day, female size and
male physical traits as covariates.
tempts (r = 0.33, df = 48, P = 0.018), but we found no
correlation between male size and total time spent
following the female (r = 0.093, df = 48, P = 0.523).
We also found that female behavior was correlated with
variation in male physical traits. Female total response
was higher towards males with more orange coloration
(r = 0.346, df = 48, P = 0.014), and females spent more
time escaping from males with less orange coloration (r
= -0.318, df = 48, P = 0.024). In addition, total female
response was higher towards males that displayed more
frequently (r = 0.376, df = 48, P = 0.007), and for
longer average time (r = 0.438, df = 48, P = 0.001).
However, we did not find an effect of male brain size on
female response (LMMfemaleresponse: brain size: χ2 (1) =
0.099, P = 0.753).
Independent LMM analyses from each measured
behavioral trait revealed no differences in any of the
quantified sexual behavioral aspects between large- and
small-brained males (Table 1). In addition, we found no
effect of brain size on the score for the total intensity of
sexual behavior of males (Table 1). However, many of
the male sexual behaviors were inter-correlated. For
instance, the frequency of gonopodial swings correlated
positively with the number of sigmoid displays (r =
0.302, df = 48, P = 0.033), and with the average duration of sigmoid displays (r = 0.344, df = 48, P = 0.014).
The principal component analysis performed on the collapsed data corroborated these patterns of correlations
between male sexual behaviors (see methods). Furthermore, in support of the analyses on separate behaviors,
we did not observe any effect of brain size on either
PC1 (Fig. 1B), or PC2 (Fig. 1C).
3
Discussion
We detected several of the expected patterns concerning the association between male physical traits and
sexual behavior. However, we found no association
between brain size and male sexual behavior. Artificial
selection for relative brain size did not generate any
discernable effects in any of the independent sexual
behaviors studied, nor in the total intensity of sexual
behavior. We also used a principal component analysis
to group the courting- and coerced copulation-related
behaviors, but we failed to detect differences in
behavior between large- and small-brained males also
with this method.
Is the lack of evidence for differences between largeand small-brained individuals an indication of no
association between brain size and sexual behavior in
the male guppy, or were the methods used inadequate to
uncover such differences? Our design was powerful
enough to pick up previously demonstrated associations
between male traits and male and female behavior. For
instance, we found that female response was correlated
with the average duration of sigmoid displays (Farr,
1980), and the amount of orange coloration in males
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(Kodric-Brown, 1985; Kodric-Brown, 1989; Brooks
and Caithness, 1995; Pitcher et al., 2003). Furthermore,
less conspicuous males tended to attempt coerced copulations to a higher extent (Houde, 1997), and larger males
performed more coerced copulation attempts (Magellan
et al., 2005). Hence, we argue that had there been a
strong association between brain size and male sexual
behavior, we should have been able to detect it. Our
data therefore do not support the hypothesis that brain
size affects male sexual behavior for the suite of behaviors studied in this set-up where males were not
affected by competitive interactions with other males.
This is somewhat surprising since previous comparative
studies have flagged up a potential link between brain
morphology and sexual behavior in different taxa, such
as birds (Garamszegi et al., 2005; Madden, 2001;
Lindsay et al., 2015), primates (Pawlowski et al., 1998),
and bats (Pitnick et al., 2006). These examples differ
from the present study in that they analyzed patterns
across rather than within species. Our study offers the
first experimental test on the relation between relative
brain size and direct quantification of sexual behavior
and, perhaps surprisingly, no association can be derived
from our data. Variation in sexual behaviors in male
guppies is generally very large (Rodd and Sokolowski,
1995, Magurran, 2005), and our results match these
previous results (Table 1). However, our data suggest
that this variation is not associated with brain size
despite a difference of over 10% in relative brain size of
the selection lines.
The set of sexual behaviors studied here might not
require high cognitive abilities in male guppies. For
example, male guppies appear to utilize the sexual behaviors we investigated without the need for learning,
although at varying rates depending on several environmental factors (Houde, 1997). In contrast, performance
of specific sexual behaviors in other species may require higher skills in cognitive traits such as greater
memory and/or learning, as is the case with male sedge
warbler Acrocephalus schoenobaenus songs (Airey et
al., 2000) or bower-building to attract females in bowerbird species (Madden, 2001). When considered alongside our results, these examples suggest that brain morphology might affect sexual behaviors only when higher
cognitive skills are necessary for the development of a
more complex display. Our setup did not allow us to
account for the role that past feedback and learning may
have played in the sexual behavior of male guppies
selected for relative brain size. Another explanation is
that if brain morphology affects male sexual behavior in
CORRAL-LÓPEZ A et al.: No association between brain size and male sexual behavior
the guppy, variation may instead be driven by fine-scale
differences in the relative size of brain subregions as has
been suggested to occur in other species. For instance,
Day et al. (2005) showed that not whole brain size, but
cerebellum size, was associated with the differences in
bower complexity across bowerbird species. In addition,
a recent study at the microevolutionary level showed
that individuals from a natural population of brown
trout Salmo trutta presented differences in various
aspects of brain structure depending on their mating
tactic (Kolm et al., 2009). Therefore, it would be of great
interest to study the association between brain substructures and sexual behaviors via artificial selection on
morphological characteristics of separate brain regions.
As mentioned above, previous work on the artificially selected relative brain size lines in guppies found
an association between brain size and cognitive ability
(Kotrschal et al., 2013a, b; Kotrschal et al., 2014a).
These studies showed that large-brained females and
males performed better in cognitive tests designed to
capture the specific ecology of the different sexes.
Combining these results with the ones obtained in our
present study, we suggest that relative brain size in this
species mainly constrains aspects of cognition that are
unrelated to male sexual display. There are some similarities between our findings and a recent study on
bowerbirds that failed to find any association between
cognitive ability and mating success (Isden et al., 2013).
Interestingly though, Shohet and Watt (2009) found that
female guppies preferred males that performed better in
a learning task where males went through a maze to find
a food item. Thus, male cognitive ability may be important in mate choice in the guppy, but mostly for behavior relating to ecological contexts other than courtship.
To conclude, we did not find support for a predicted
association between relative brain size and male sexual
behavior. Instead, we found high variability in the set of
sexual behaviors that male guppies perform. However,
further investigation is required before we can completely dismiss any link between brain size and male
sexual behavior in this species. For instance, we investigated the behavior of pairs in a single interaction in the
present study. The effect of relative brain size on sexual
behaviors might be more evident in situations permitting social interactions between multiple individuals,
allowing for male-male competition (Price and Rodd,
2006), or after multiple encounters with females in which
learning may be involved (Jordan and Brooks, 2012).
Hence, future studies should also take into account
complex social interactions, such as dominance and ag-
271
gression and/or the role of past experiences and repeated displays. Moreover, future studies should also investigate female behavior in these brain size selected lines
in more detail before we can fully understand the effect
of brain size on sexual behavior in both sexes.
Acknowledgments We thank Tim Fawcett and three anonymous reviewers for valuable comments on an earlier version
of the manuscript. N. K. was funded by the Swedish Research
Council. A.K. was funded by the Austrian Science Fund (J
3304-B24). The experiment was performed in accordance
with the ethical regulations of Stockholm University and
Swedish law.
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