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Female choice can often drive the elaboration of male traits, leading to the evolution of secondary sexual traits. In the Mexican molly, Poecilia sphenops (Poeciliidae), some males exhibit a mustache-like structure on the upper maxilla, the function of which has not been previously recognized. The mustache consists of epidermal outgrowths at the edge of the scales that appear to have no sensory function. Trait expression varies within as well as among populations of P. sphenops, but is not linked to male body size polymorphism. In mate choice experiments, female P. sphenops exhibited a visual mating preference for males with mustaches, suggesting that the trait may be sexually selected. Since the mating behavior of P. sphenops involves contact of the male’s snout and the female genital region prior to copulation, we hypothesize that the mustache may also convey tactile signals to the female.
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ORIGINAL PAPER
Anovel,sexuallyselectedtraitinpoeciliidfishes:
female preference for mustache-like, rostral filaments
in male Poecilia sphenops
Ingo Schlupp &Rüdiger Riesch &Michael Tobler &
Martin Plath &Jakob Parzefall &Manfred Schartl
Received: 27 March 2010 / Revised: 22 May 2010 / Accepted: 24 May 2010 / Published online: 9 June 2010
#Springer-Verlag 2010
Abstract Female choice can often drive the elaboration of
male traits, leading to the evolution of secondary sexual
traits. In the Mexican molly, Poecilia sphenops (Poecilii-
dae), some males exhibit a mustache-like structure on the
upper maxilla, the function of which has not been
previously recognized. The mustache consists of epidermal
outgrowths at the edge of the scales that appear to have no
sensory function. Trait expression varies within as well as
among populations of P. sphenops, but is not linked to male
body size polymorphism. In mate choice experiments,
female P. sphenops exhibited a visual mating preference
for males with mustaches, suggesting that the trait may be
sexually selected. Since the mating behavior of P. sphenops
involves contact of the males snout and the female genital
region prior to copulation, we hypothesize that the mus-
tache may also convey tactile signals to the female.
Keywords Mate choice .Mating preference .
Sexual selection .Structural ornaments
Introduction
Sexual selection is a powerful evolutionary force often
leading to the elaboration of male traits and the evolution of
sexual dimorphism (Andersson 1994; Andersson and Iwasa
1996). Numerous male traits, like conspicuous color pat-
terns or structural ornaments, have evolved as a conse-
quence of females preferring to mate with males bearing
them. Live-bearing fishes of the family Poeciliidae have
been particularly useful as model systems for studying
sexual selection (Houde 1997; Magurran 2005) because of
the diversity of male ornaments and the diversity of
underlying female preferences found in this group (Endler
1983,1992; Basolo 1998; Lindholm and Breden 2002).
In poeciliid fishes, there is a good understanding of how
females respond to male traits ranging from distinct colors
and color patterns (Schlüter et al. 1998; Kodric-Brown and
Johnson 2002; Cummings et al. 2003) to structural orna-
ments (Ptacek 1998; Rosenthal and Evans 1998; MacLaren
et al. 2004; Wong and Rosenthal 2006) and courtship
patterns (Kodric-Brown 1993; Rosenthal and Evans 1998;
Kodric-Brown and Nicoletto 2001). Even chemical com-
munication and its role in mate choice has been studied to
some extent (Shohet and Watt 2004; Fisher and Rosenthal
2006). In many of these cases, studies of the mechanisms
Communicated by M. Jennions
I. Schlupp (*):R. Riesch
Department of Zoology, University of Oklahoma,
730 Van Vleet Oval,
Norman, OK 73019, USA
e-mail: schlupp@ou.edu
I. Schlupp :J. Parzefall
Biozentrum Grindel, University of Hamburg,
20146 Hamburg, Germany
M. Tobler
Departments of Biology and Wildlife and Fisheries Sciences,
Texas A&M University,
2258 TAMU,
College Station, TX 77840, USA
M. Plath
Department of Ecology and Evolution,
J.W. Goethe University of Frankfurt,
Siesmayerstr. 70a,
60054 Frankfurt a.M., Germany
M. Schartl
Physiological Chemistry I, University of Würzburg,
Am Hubland,
97074 Würzburg, Germany
Behav Ecol Sociobiol (2010) 64:18491855
DOI 10.1007/s00265-010-0996-y
underlying mate choice were combined with studies on the
ultimate consequences of female choice.
In the present study, we investigated the form and func-
tion of an as yet unstudied structure found in some males of
the Mexican molly, Poecilia sphenops Valenciennes, 1846.
The structure consists of relatively long filaments found
exclusively on the snout of males, resembling a mustache
(Fig. 1a). The trait itself had been mentioned in a previous
taxonomic study (Schultz and Miller 1971) andalready
alluding to a potential functionwas characterized as a
contact organ.Contact organs typically are tiny hard
bumps of keratin (sometimes with a core of bone) that grow
on the fins, head, and body scales and have been described
in at least 25 families of fishes (Wiley and Collette 1970;
Collette 1977). They are predominantly found in males and
usually expressed during the breeding season when they
help males maintain contact with females during spawning.
Best known are probably the breeding tubercles of cyprinid
fishes in which high numbers of tubercles have been shown
to increase male reproductive success (Jacob et al. 2009).
Contact organs have also been described in some genera
of the family Poeciliidae, specifically in the genera
Poecilia,Poeciliopsis, and Phallichthys (Wiley and Collette
1970). In these groups, contact organs are slender ossified
extensions at the edge of the scales on the head posterior of
the upper lip and are thought to play a role during mating as
males of these genera touch females at the gonopore with
their snout prior to copulation (Rosen and Tucker 1961).
Compared to the structures found in P. sphenops, however,
the contact organs previously described in poeciliids are
small, barely visible by eye, and unbranched. In the present
study, we characterized male mustaches of P. sphenops
using electron microscopy, surveyed the distribution of
mustaches within and among populations, and studied their
potential role in sexual selection by investigating female
mate choice.
Materials and methods
Study system and material examined
P. sphenops is common along the Atlantic coast of Mexico
from the Río de la Palma Sola on southward into Guate-
mala on the Pacific side (Miller 2005). They are also dis-
tributed inland along the Isthmus of Tehuantepec. Contact
organs have previously been mentioned from several
populations of P. sphenops and some other Poecilia species
(Schultz and Miller 1971), but neither a thorough descrip-
tion of the structure nor systematic classification of popu-
lations with and without mustaches has been conducted so
far. We surveyed the occurrence of mustaches in males of
several populations of P. sphenops and museum holdings of
the species (see Table 1for material examined). Based on
Fig. 1 a Photograph of a male
P. sphenops. The mustache-like
structure is clearly visible on the
males rostrum. bDorsal EM
scan of the snout region of a P.
sphenops male depicting the
epidermal outgrowths that form
the mustache. cEM scan of a
single scale of the rostrum. The
epidermis was removed in the
posterior part of the scale. Epi-
dermal outgrowths are present
on the anterior edge of the scale
1850 Behav Ecol Sociobiol (2010) 64:18491855
topology of a molecular phylogeny (using cytochrome b
and control region sequences of mitochondrial DNA), the
presence or absence of this trait appears to represent within-
species variation (data not shown).
Distribution patterns of mustached males
within populations
To assess the occurrence of mustaches within a population,
P. sphenops were caught in a small coastal stream north of
Veracruz (El Limon, IS IV/6; Table 1) in April 2007. Males
and females were examined for the presence of mustaches,
and their standard length was measured to the closest
millimeter. Since sexual ornaments in poeciliids are often
expressed in larger males only (Farr 1989), we compared
the standard lengths of males with and without mustaches
using an independent-samples ttest.
Electron microscopy
In-depth examinations of mustaches and their significance
in female mate choice were all performed on P. sphenops
collected at the IS VI/6 site (Table 1). For the examination
of the mustache structure, male P. sphenops were collected
and fixed on site in 10% formalin. Samples were then
studied using routine electron microscopy (EM) processing
(Hansen and Finger 2000).
Mate choice experiments
In species like P. sphenops, males do not exhibit any
courtship displays prior to gonopodial thrusting. Given that
molly males constantly attempt to mate with females (e.g.,
even directly upon capture; Riesch et al. 2008), it is likely
that time spent by a female associating with a given male
(leading to physical proximity) facilitates male copulation
attempts by that particular male. In fact, a recent study by
Walling et al. (2010) experimentally demonstrated that
association preferences actually do translate into male
reproductive success in green swordtails, Xiphophorus
hellerii (Poeciliidae). Hence, association preferences should
translate into more copulations with the preferred male also
in P. sphenops.
Female mate choice experiments with live stimulus fish
were conducted in the field in Mexico in 1998 and 2006.
We used a portable test tank (42.6×30 ×16.5 cm) built from
UV-transparent Plexiglas. The tank was visually divided
into three equal zones by black marks on the outside. The
central zone was designated the neutral zone, the two lateral
zones as preference zones. Two stimulus males were
presented in two smaller tanks (19.5 ×30 ×14.5 cm) on
either side of the test tank. Females were only tested once.
The fish were collected using a seine and were acclimated
in a 10-l bucket with creek water.
Video playback experiments were conducted in spring of
2009 at the University of Oklahoma in Norman. P.
sphenops for this experiment originated from field collec-
tions in 2006 and were maintained as randomly outbred
stocks in tanks (2501,000 l) in a greenhouse. The tanks
contained naturally growing algae and other submerged
plants as well as a variety of naturally occurring inverte-
brates like chironomid larvae, copepods, and amphipods on
which the fish could feed. In addition, the fish were fed ad
libitum amounts of flake food every 2 days. All fish used in
this study were sexually mature and had interacted with the
opposite sex; thus, all females were most likely pregnant.
Table 1 Material examined in this study including field site/accession
numbers, latitude and longitude, the presence of bearded males, and
the number of individuals examined
Latitude Longitude Mustached
males
N
Collections by the authors
IS 98/3 18.66 95.75 No n.a.
a
IS 98/4b 18.79 95.80 Yes n.a.
IS 98/7 19.50 96.93 Yes n.a.
IS VI/1 19.42 96.61 Yes n.a.
IS VI/2 19.46 96.57 Yes n.a.
IS VI/3 19.50 96.58 Yes n.a.
IS VI/4 19.51 96.46 Yes n.a.
IS VI/6 19.68 96.51 Yes 101
IS VI/8 19.25 96.37 No n.a.
Museum collections examined
CU64287 18.88 95.97 No 40
TNHC13876 16.27 94.15 No 34
TNHC13896 16.13 93.80 No 89
UMMZ157628 19.17 96.17 Yes 704
UMMZ164743 19.03 96.03 Yes 13
UMMZ181298 17.80 95.17 Yes 46
UMMZ184513 19.75 96.47 No 433
UMMZ184516 19.63 96.47 Yes 11
UMMZ184564 17.80 95.17 Yes 59
UMMZ187252 19.03 96.03 Yes 2
UMMZ187731 17.80 94.75 Yes 14
UMMZ187750 17.80 94.75 No 17
UMMZ187773 17.75 94.80 No 113
UMMZ187808 17.83 94.75 Yes 71
UMMZ192842 19.08 96.13 Yes 6
UMMZ194688 19.03 96.17 Yes 11
UMMZ194767 18.03 94.53 Yes 11
CU Cornell University Ichthyology Collection, Ithaca, NY, USA,
TNHC Texas Natural History Collection, Austin, TX, USA, UMMZ
University of Michigan Museum of Zoology, Ann Arbor, MI, USA
a
This information is not available for this collection
Behav Ecol Sociobiol (2010) 64:18491855 1851
Generation of stimulus videos
To produce the video animations for our video playback
experiment, digital images of two males were taken while a
male was swimming in a small tank using a Nikon D70
digital camera. From each resulting picture, the image of
the male was extracted from the background using the
magic extractorfunction in Adobe® Photoshop Elements
6.0. In a first step, actual rostral filaments were virtually
removed. Then, using the coloration of the snout region of
each individual male, mustache-like rostral filaments were
pasted onto the body of one male in each pair of images
using the brush tool.Several pictures of mustached P.
sphenops served as models to ensure visual accuracy (e.g.,
Fig. 1). Consequently, the pairs of animation showed two
identical males differing only in the presence or absence of
a mustache. Differences in the response to the animation by
the tested females can therefore be attributed to the trait
under study, rostral filaments.
The resulting images were then animated and converted
to an AVI file (resolution, 800×600) using Pencil
v.0.4.4bfor Apple. A straight movement of the pictures
from left to right and right to left was generated in front of a
uniform white background. The animations were 14 s long:
twice 6 s for the distance of 28.5 cm on the screen forth and
back, each followed by an invisible turn of 1 s. Simulta-
neous playback was performed using two identical com-
puter monitors (Belinea 10 30 40) with a Matrox Millenium
G400 dual-head graphic card. The monitor refresh rate was
85 Hz, and the AVI films were run in infinite loops during
the experiment using the Monitor Plug-Inthat is part of
the Viewer software package (BIOBSERVE GmbH).
To ensure that male size was appropriate for the
individual trials (i.e., resembled the approximate size of
the original males photographed), sample videos were run
and male sizes measured on the screen. If needed, male size
was then digitally adjusted and new videos were created
until male size was appropriate for each stimulusvideo
pair.
Experiment 1
We conducted three separate experiments. In the first ex-
periment (n=17 replicates), we tested whether females
(standard length; mean ± SD, 62.9 ± 6.7 mm) exhibit a pref-
erence for males with mustaches. To do so, pairs of stimu-
lus males were matched for size [size difference < 2 mm
standard length (SL)], and after cooling down the males on
ice, the mustache was gently removed in one of two
stimulus males using a scalpel. No mortality was associated
with this procedure. We always removed the slightly larger
males mustache, so female choice for large male size (see
below) would not affect the results (standard lengths; males
with mustache, 59.4± 4.3 mm; mustache removed, 60.4±
5.4 mm; paired ttest: t
16
=3.23, P=0.005).
Before each trial, stimulus males were placed into the
side tanks and given several minutes for acclimatization.
Once the males were swimming calmly, a female was
introduced into the neutral zone, and we measured the time
the female subsequently spent in each preference zone during
5 min of observation. Note that females could exercise a non-
choiceby remaining in the neutral zone. To control for side
biases, the stimuli were interchanged after the first trial and the
measurement repeated. The actual choice test thus consisted
of two trials and lasted for 10 min.
Experiment 2
In the first experiment, females may not exhibit a pref-
erence for mustached males, but they could actually be
rejecting manipulated males, e.g., because handling during
the physical removal of mustaches may have altered the
malesbehavior. We thus performed a second experiment
(n=12 replicates) where preferences of females (56.0 ±
7.2 mm) for large manipulated (63.7±9.2 mm) as compared
to smaller, unmanipulated males (39.7 ± 5.2 mm) were
assessed (difference in body size, paired ttest: t
11
=8.63,
P<0.001). Preferences for large-sized males are common in
female poeciliids (Ryan and Keddy-Hector 1992) and were
confirmed by an experiment with lab-reared P. sphenops
females from the same population (paired ttest: t
16
=2.58,
P=0.02) using a standard experimental protocol. However,
if females rejected manipulated males, they should prefer
smaller males. The testing procedure was identical to that
of the first experiment.
The females used in both experiments 1 and 2 were
field-collected; hence, we had no knowledge of their
reproductive status.
Experiment 3
To unequivocally test whether mustached males really are
preferred by females and are not simply avoided after the
manipulation (i.e., surgical removal of the mustache; ex-
periments 1 and 2), we conducted a third experiment (n= 16
replicates) using video stimuli rather than live fish. For this,
monitors were placed on either side of a test tank (60 ×
40×30 cm). Water level was maintained at 25 cm, which
was also the height of the monitors, and the water tem-
perature was 25°C. Using the Zone Definitionfunction of
the Biobserve Viewer software, the tank was virtually
divided into three equal-sized sections: a central neutral
zone and two preference zones near the monitors. The
behavior and movement of each focal female was moni-
tored and tracked using a Sony camera (ExwaveHAD)
placed above the setup, connected to the PC running the
1852 Behav Ecol Sociobiol (2010) 64:18491855
Viewer program. To increase the contrast between fish and
background (i.e., making it easier for the viewer software to
track the focal fish), white opaque Plexiglas sheets covered
the bottom and long sides of the tank. Pairs of videos were
alternated between trials; hence, half of the females (n=8)
were presented with the videos of male 1 and the other half
with the videos of male 2.
A test female was placed into a transparent Plexiglas
cylinder (8.5-cm diameter) in the middle of the neutral
zone. The female was allowed to acclimate for 5 min, and
then the cylinder was carefully removed and the experiment
remotely started. The Viewer software now tracked the
focal fish for an observation period of 5 min and recorded
the time spent in each preference zone. To detect side
biases, the female was immediately placed into the cylinder
again, the video playbacks were switched, and the
procedure was repeated. After the test, the SL of the female
was measured to the closest millimeter. Females were then
transferred into another tank so that each female was only
tested once.
We decided a priori to exclude side biases (more than
80% of time during both parts of a trial in only one
preference zone) and trials with low response (<50% of the
time inside the preference zones). We assumed such
females not to be motivated to choose (Landmann et al.
1999); however, neither side biases nor low response
occurred during this experiment.
For all three experiments, we summed the time spent in
the preference zone near each stimulus male for both trials.
Association times with the two stimulus males were
compared using paired ttests.
Results
Distribution of P. sphenops populations with mustaches
Males with mustaches were detected in 18 out of the 26
examined sites (Table 1and Fig. 2). There was no clear
geographical pattern, although males with mustaches were
absent among the specimens examined from the two sites
on the Pacific versant of Mexico.
Frequency and distribution of males with mustaches
within populations
We examined 101 individuals from El Limon to assess the
distribution of mustaches within a population. None of the
72 females (mean SL ± SD, 60.2 ± 15.4 mm) exhibited a
mustache. However, 17 of the 29 males (59%) had
mustaches. There was no significant difference in the size
of males with and without a mustache (SL of males with
mustache, 62.0±17.4 mm; males without mustache, 57.3 ±
9.3 mm; independent ttest for samples with unequal
variances: t
28
=0.95, P=0.35).
Electron microscopy of mustaches
The EM examination of P. sphenops mustaches showed that
they consist of epidermal filaments that emerge from the
anterior edges of the scales located across the rostrum
(Fig. 1). Most filaments appear to be unbranched, but some
branched filaments were recorded. EM did not reveal any
sensory structures in the filaments.
Mate choice experiments
Experiment 1
In the first behavioral experiment, focal females could
choose between a male with a mustache and a male whose
mustache had been removed. Females displayed a strong
preference for males with mustaches: They spent 319.6 ±
78.5 s (mean ± SD) near the mustached male vs. 200.4 ±
96.2 s near the non-mustached male (paired ttest: t
16
=2.74,
P=0.015; Fig. 3a).
Experiment 2
In a second experiment, focal females could choose be-
tween a larger male with his mustache removed and a smaller
mustached (i.e., non-manipulated) male. Females spent
Fig. 2 Locations of P. sphenops examined for this study (see Table 1).
Black circles indicate populations in which males with mustaches
were found; gray circles are populations without mustaches. The inset
highlights the location of the enhanced section within Mexico
Behav Ecol Sociobiol (2010) 64:18491855 1853
significantly more time near the manipulated, larger male
(410.3±73.6 s) compared with the unmanipulated, smaller
one (144.5±64.8; paired ttest: t
11
=6.25, P<0.001; Fig. 3b).
Experiment 3
In a third experiment, focal females could choose between
videos of the same male; however, one video-male sported
a mustache, while the other one did not. Again, females
spent significantly more time near the mustached male
(323.5±78.5 vs. 240.9±64.7 s; paired ttest: t
15
=2.38, P=
0.031; Fig. 3c).
Discussion
The mustache-like structures on the rostrum of P. sphenops
consist of epidermal outgrowths on the edges of scales and
seem to be an as yet unrecognized sexually selected trait in
poeciliid fishes. Epidermal outgrowths on the snout have
previously been reported for several other fishes (Collette
1977); however, compared to the structure in P. sphenops,
epidermal contact organs are hard structures usually based
on keratin or bone. Soft and fleshy filaments are otherwise
only known from male armored suckermouth catfish of the
genus Ancistrus (Sabaj et al. 1999). For these, it was
speculated that male tentacles might mimic larvae, which
may provide males with a mating advantage since females
prefer spawning with males that already guard a clutch of
hatched larvae (Sabaj et al. 1999).
The presence of the mustaches in P. sphenops seems to
be facultative even within populations. Whether this reflects
a genetic polymorphism or phenotypically plastic expres-
sion of the trait (which could be lost and regrown) remains
to be examined. It also remains unclear whether populations
in which we were not able to record mustached males
indeed lack them or whether these just occur at very low
frequencies. Unlike other ornaments in poeciliids, such as
the presence of swords in some Xiphophorus species
(Zimmerer 1988), the presence of mustaches in P. sphenops
is not restricted to large males as no differences in the mean
size between mustached and non-mustached males were
found.
The female choice experiments indicated a visually
based mating preference for males exhibiting a mustache.
At this time, we cannot assess the effect that the removal of
the ornament per se had on the stimulus males, but our two
follow-up experiments support the idea that males were not
rejected simply because they were manipulated. It is also
noteworthy that the widespread preference for larger males
overrides the preference for the mustache.
Although the preference we documented is visual, the
structure of the ornament, its position on the males snout,
and the mating behavior of Poecilia males make it likely
that mustaches also provide tactile information for the
females. Males of P. sphenops and several other poeciliids
typically follow the female and touch their genital region
with the snout prior to copulation attempts (a sexual
behavior known as nipping; Rosen and Tucker 1961;
Parzefall 1969). Given the size of the filaments, the
structure likely will be felt by the females during nipping.
In another species of the genus Poecilia, the cave molly
(Poecilia mexicana) females have evolved an enlarged
genital pad whichbesides its function of secreting
pheromonesis presumed to also have a sensory function
in the perception of scale protuberances located on the head
of the males (Parzefall 2001).
In fishes, tactile signals and stimulation as a means of
sexual signaling have not been investigated in depth so far,
and this phenomenon clearly requires additional investiga-
tion (Coleman 2009). If females indeed perceive tactile
information by mustaches and integrate the information into
the decision-making process during mate choice, mustaches
in P. sphenops, along with male size, coloration, phero-
mones, and behavior, may contribute to a multimodal signal
addressing visual, olfactory, and tactile sensory channels
(Hölldobler 1999; Uetz and Roberts 2002; Candolin 2003;
McLennan 2003; Partan and Marler 2005). Multimodal
signals are especially interesting to study because both
senders and receivers face trade-offs as these signals are
hard to perfect for different sensory modalities. Many
multimodal signals studied so far are bimodal, i.e., combine
sensory input from two sensory modalities like vision and
hearing (Cooper and Goller 2004) or vision and seismics
(Hebets et al. 2006).
Based on the present study, we hypothesize that the
mustachein P. sphenops could be such a multimodal
signal, combining a visual and a tactile component. Future
studies will have to elucidate the proposed tactile function,
but also ask what maintains the interesting polymorphism
for this trait.
0
160
320
480
AC
Time (s)
mustached mustache
removed large,
mustache
removed
small,
mustached video,
mustached video,
no mustache
B
Fig. 3 Results of the behavioral experiments (mean ± SD association
times near the two types of males). aFemale choice for males with
and without mustaches. bLarge males with mustaches removed and
small unmanipulated stimulus males. cVideo images of the same male
with and without a mustache
1854 Behav Ecol Sociobiol (2010) 64:18491855
Acknowledgments We thank Marion Döbler, Kay Körner, and
Dunja Lamatsch for their help in the field. Jens Poschadel helped
with laboratory analyses and experiments. Ellen McCoy performed
parts of the video playback experiment, and Anne Hansen kindly
performed electron microscopy. We thank William Matthews for
discussion. Nathan Franssen made the map in Fig. 2. Financial support
came from the Deutsche Forschungsgemeinschaft, the University of
Oklahoma, and the Swiss National Science Foundation.
Ethical note The experiments comply with the current laws of the
country in which they were performed.
The authors declare that they have no conflict of interest.
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... The only exception to this general pattern is that males in the M social context nipped more at females. In poeciliids, males nipping females is generally interpreted as a reproductive behavior, not aggression (Sumner et al. 1994;Houde 1997;Plath et al. 2007;Schlupp et al. 2010). ...
... The only "aggressive" behavior that was frequent enough in focal males to include in the analysis was nipping of female social partners. In many poeciliids, this behavior is a normal part of mating, not aggression (Sumner et al. 1994;Houde 1997;Plath et al. 2007;Schlupp et al. 2010). Moreover, M males nipped females less than did S males (Figure 3d). ...
Article
The social environment can dramatically influence the development and expression of individual behavior. Indirect genetic effects (IGE) arise when variation in the social environment depends on genotypic differences among social partners. Their role in generating variation and influencing evolutionary dynamics has become increasingly recognized in recent years, but less attention has been paid to how IGE arise during development. We measured the development of IGE using a discrete natural polymorphism in male coloration and associated behaviors in eastern mosquitofish (Gambusia holbrooki). We observed substantial IGE and direct genetic effects on behavior. For some behaviors, IGE changed and even reversed direction over the 16 weeks of the experiment, indicating important developmental dynamics. Interaction between IGE and direct genetic effects for some behaviors suggests that melanistic males were less responsive to a genetic change in their social environment than nonmelanistic males were. Alternately, social partners might vary less in the behavior they direct toward melanistic males. Color morphs differed in mating behavior and in aggressive behavior they received from social partners, but not in direct measures of aggression. Therefore, even apparently innate differences in behavior between morphs could arise as indirect effects of differences in behavior directed toward them by social partners. These results indicate that some differences attributed to melanism in this and other species might result from color morphs experiencing different social environments. Deducing the developmental and social origins of these indirect effects is therefore critical for understanding melanism-Associated behavioral variation in the many species in which it occurs. © The Author(s) 2017. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: [email protected]
... Basolo and Trainor, 2002;Cummings et al., 2003;Kodric-Brown and Johnson, 2002;Schlüter et al., 1998), structural ornaments (e.g. Basolo, 1990a;Benson and Basolo, 2006;MacLaren et al., 2004;Rosenthal and Evans, 1998;Schlupp et al., 2010) or courtship displays (e.g. Kodric-Brown and Nicoletto, 2001;Kodric-Brown, 1993;Rosenthal and Evans, 1998). ...
Article
Full-text available
Among fishes in the family Poeciliidae, signals such as colour patterns, ornaments, and courtship displays play important roles in mate choice and male-male competition. Despite this, visual capabilities in Poeciliids are understudied, in particular visual acuity, the ability to resolve detail. We used three methods to quantify visual acuity in male and female green swordtails (Xiphophorus helleri), a species in which body size and the length of the male's extended caudal fin (‘sword’) serve as assessment signals during mate choice and agonistic encounters. Topographic distribution of retinal ganglion cells (RGC) was similar in all individuals and characterized by areas of high cell densities located centro-temporally and nasally, as well as a weak horizontal streak. Based on the peak density of RGC in the centro-temporal area, anatomical acuity was estimated to be approximately 3 cycles/degree (cpd) in both sexes. However, a behavioural optomotor assay found significantly lower mean acuity in males (0.8 cpd) than females (3.0 cpd), which was not explained by differences in eye size between males and females. An additional behavioural assay, in which we trained individuals to discriminate striped gratings from grey stimuli of the same mean luminance, also showed lower acuity in males (1-2 cpd) than females (2-3 cpd). Thus, although retinal anatomy predicts identical acuity in males and females, two behavioural assays found higher acuity in females than males, a sexual dimorphism which is rare outside of invertebrates. Overall, our results have implications for understanding how Poeciliids perceive visual signals during mate choice and agonistic encounters.
... Our experiment would have benefited from allowing sensory cues other than only visual. Poeciliiids such as Poecilia chica and P. sphenops use chemical and tactile feedback, respectively, when assessing mates (Brett & Grosse, 1982;Schlupp et al., 2010). Although, the bulk Note: Explanatory variables were male size and species. ...
Article
Female preference is widely described in various taxa, and the underlying mechanisms shaping preferences remain a major focus of sexual selection studies, particularly in species where males contribute minimally to offspring. Female preference is associated with maintaining male secondary sexual traits (SST). However, how male SST impact female preference is less‐understood. We hypothesized the strength of female preference should scale with the expression of male SST. To test this prediction, we compared female preference for male body size (an easily quantifiable trait that scales with other SST) in three species of Limia (Poeciliidae) varying in secondary sexual traits: L. perugiae, L. dominicensis and L. zonata. The degree of SST was assessed based on the amount of ornamentation and the presence of courtship in the species. Limia perugiae, L. dominicensis and L. zonata were designated as possessing high, intermediate and low male SST, respectively. Female preference was quantified as the relative amount of time females associated with males of various size classes: small, intermediate and large. Therefore, we predicted because L. perugiae males have the most SST, females would associate more strongly with large males. Limia perugiae females were the only species to display female preference in relation to male body size, but they preferred small males. Although preference was observed, the direction of preference was unexpected. Moreover, the lack of preference for large male size and thereby other SST in the species suggests pre‐copulatory female preference is unimpacted by male SST. We suggest cryptic female choice (i.e. preference enacted during or after copulation) may maintain costly male traits. However, future work remains necessary. The present study provides foundational behavioural work on Limia and examines the ubiquity of the evolution of female preference in poeciliids.
... The used swimming speeds were the lower and upper 10% percentiles of females from experiment 1. This technique is well established in the evaluation of mating preferences in fish per se [49][50][51][52][53] and has been used successfully by the authors in previous studies [48,54]. ...
Article
Full-text available
Mate choice that is based on behavioural traits is a common feature in the animal kingdom. Using the Trinidadian guppy, a species with mutual mate choice, we investigated whether males use female swimming activity—a behavioural trait known to differ consistently among individuals in many species—as a trait relevant for their mate choice. In the first experiment, we assessed male and female activity in an open field test alone (two repeated measures) and afterwards in heterosexual pairs (two repeated measures). In these pairs, we simultaneously assessed males’ mating efforts by counting the number of sexual behaviours (courtship displays and copulations). Male and female guppies showed consistent individual differences in their swimming activity when tested both alone and in a pair, and these differences were maintained across both test situations. When controlling for male swimming behaviour and both male and female body size, males performed more courtship displays towards females with higher swimming activity. In a second experiment, we tested for a directional male preference for swimming activity by presenting males video animations of low- and high-active females in a dichotomous choice test. In congruence with experiment 1, we found males to spend significantly more time in association with the high-active female stimulus. Both experiments thus point towards a directional male preference for higher activity levels in females. We discuss the adaptive significance of this preference as activity patterns might indicate individual female quality, health or reproductive state while, mechanistically, females that are more active might be more detectable to males as well.
... The used swimming speeds were the lower and upper 10% percentiles of females from experiment 1. This technique is well established to evaluate mating preferences in fish per se [49][50][51][52][53] and has been used successfully by the authors in previous studies ( [48,54]. ...
Preprint
Mate choice that is based on behavioural traits is a common feature in the animal kingdom. Using the Trinidadian guppy, a species with mutual mate choice, we investigated whether males use female swimming activity – a behavioural trait known to differ consistently among individuals in many species – as a trait relevant for their mate choice. In a first experiment, we assessed male and female activity in an open field test alone (two repeated measures) and afterwards in heterosexual pairs (two repeated measures). In these pairs, we simultaneously assessed males’ mating efforts by counting number of sexual behaviours (courtship displays and copulation). Male and female guppies showed consistent individual differences in their swimming activity when tested both alone and in a pair, and these differences were maintained across both test situations. When controlling for male swimming behaviour and both male and female body size, males performed more courtship displays towards females with higher swimming activity. In a second experiment, we tested for a directional male preference for swimming activity by presenting males video animations of low and high active females in a dichotomous choice test. In congruence with experiment 1, we found males to spend significantly more time in association with the high active female stimulus. Both experiments thus point towards a directional male preference for higher activity levels in females. We discuss the adaptive significance of this preference as activity patterns might indicate individual female quality, health or reproductive state while, mechanistically, females that are more active might be more detectable to males as well.
... Our experiment would have benefited from allowing sensory cues other than only visual. Poeciliiids such as Poecilia chica and P. sphenops use chemical and tactile feedback, respectively, when assessing mates (Brett & Grosse, 1982;Schlupp et al., 2010). Although, the bulk Note: Explanatory variables were male size and species. ...
Article
Reproductive investment was initially thought to be the key selective force behind male mate preference for female characters, like size or ornamentation (i.e., the preference by males for certain females). Yet, evidence of polygynous species, where male reproductive investments are often inexpensive compared to those of females, have also been described to possess male preference. Our study aims to understand how reproductive investment influences the selection of choosy males in polygynous systems using two species of livebearing fishes varying in reproductive investment: Limia perugiae, in which males invest heavily into reproduction, and L. zonata in which males invest minimally into reproduction. We hypothesized that male reproductive investment when combined with fecundity selection will favour the evolution of male mate preference and thereby lead to males that invest heavily into reproduction being choosier than males that invest minimally. When male Limia were exposed to two females simultaneously, one from the small size class and one from the large size class, L. zonata chose large females over small ones, whereas L. perugiae allocated the same amount of time regardless of female size class. Although we fail to find support for our original hypotheses, our study highlights the need for a more thorough examination of non-model species like Limia. We suggest future studies analyse of reproductive investment as it interacts with cryptic choice, multiple sensory cues as well as expand comparisons to multiple Limia species, especially those endemic to Cuba, Grand Cayman, and Jamaica.
... Female mate choice has long been recognized as a major driver for character displacement [1][2][3], or the evolution of novel male traits [4,5], but can also play a vital role during speciation processes by promoting reproductive isolation through assortative mating [6,7]. Many mating preferences are innate [1]; still, various extrinsic factors (ecological constraints) may affect individual mating decisions [8][9][10], such as altered possibilities for mate quality assessment due to increased costs of mate searching [11,12]. ...
Article
Full-text available
Background In many species males face a higher predation risk than females because males display elaborate traits that evolved under sexual selection, which may attract not only females but also predators. Females are, therefore, predicted to avoid such conspicuous males under predation risk. The present study was designed to investigate predator-induced changes of female mating preferences in Atlantic mollies (Poecilia mexicana). Males of this species show a pronounced polymorphism in body size and coloration, and females prefer large, colorful males in the absence of predators. Results In dichotomous choice tests predator-naïve (lab-reared) females altered their initial preference for larger males in the presence of the cichlid Cichlasoma salvini, a natural predator of P. mexicana, and preferred small males instead. This effect was considerably weaker when females were confronted visually with the non-piscivorous cichlid Vieja bifasciata or the introduced non-piscivorous Nile tilapia (Oreochromis niloticus). In contrast, predator experienced (wild-caught) females did not respond to the same extent to the presence of a predator, most likely due to a learned ability to evaluate their predators' motivation to prey. Conclusions Our study highlights that (a) predatory fish can have a profound influence on the expression of mating preferences of their prey (thus potentially affecting the strength of sexual selection), and females may alter their mate choice behavior strategically to reduce their own exposure to predators. (b) Prey species can evolve visual predator recognition mechanisms and alter their mate choice only when a natural predator is present. (c) Finally, experiential effects can play an important role, and prey species may learn to evaluate the motivational state of their predators.
... We can evaluate this idea through a comparison between two clades that differ in the intensity of sexual selection acting on males and in the prevalence of female bright colour patterns. Sexually dichromatic species are common in two fish Subfamilies, Poeciliinae and Goodeinae, in which both the occurrence and the costs of male ornaments have been frequently studied (Arellano-Aguilar & Macías Garcia, 2008;Bisazza, Grapputo, & Nigro, 1997;Devigili, Kelley, Pilastro, & Evans, 2012;Endler, 1983;Karino & Haijima, 2001;Kodric-Brown, 1989;Macías Garcia, 2014;Macías Garcia & Burt de Perera, 2002;Macías Garcia & Ramírez, 2005;Moyaho, Garcia, & Manjarrez, 2004;Ritchie et al., 2007;Rosen & Tucker, 1961;Rosenthal, Flores Martínez, García de León, & Ryan, 2001;Schlupp et al., 2010), whereas studies of female colouration in species of either family are scarce. ...
Article
By preferring mates with increasingly costly ornaments or courtship displays, females cause an escalation of male reproductive costs. Such increased costs should promote male selectivity based on fecundity‐linked female attributes, leading to female ornamentation in species with traditional sex roles. Consequently, female ornamentation should evolve more frequently in taxa where male reproduction is costly than in comparable taxa where it is cheaper. We assessed the prevalence of female ornamental colouration in two clades of viviparous cyprinodontid fish; the Goodeinae, where stringent female choice imposes male mating costs, and the Poeciliinae, whose males can circumvent female mate choice. We found that while in the Poeciliinae female ornamental colour is a paler version of, and correlated with, male colour, females of the Goodeinae often display vivid ornamental colours that are distinct from those of males. Thus, male and female ornaments are not (phylo)genetically correlated in the Goodeinae. Furthermore, phylogenetic signal on male and female colour is clearly detectable in the Poeciliinae, but absent in the Goodeinae, suggesting that ornamental colour of males and females in the latter may be the consequence of selection. Given that enforceable female choice has promoted male ornaments, we propose that evolutionary retribution has promoted distinct female ornaments in the Goodeinae. This article is protected by copyright. All rights reserved.
... The males used to create the stimulus tapes were of similar size (within 2 mm) and were typical in terms of spotting patterns for each population. We conservatively chose a 2 mm size difference threshold because it is smaller than the 3 mm difference shown to be necessary to have an effect on mate choice in similar studies of poeciliid fish mating preferences [57][58][59]. In addition, males used to make the videos were chosen to be as similar as possible, with the primary difference being the number and character of spots. ...
Article
Full-text available
In this study, we explored the possibility that differences in pigmentation patterns among populations of the fish Poeciliopsis baenschi were associated with the presence or absence of the closely related species P. turneri. If reproductive character displacement is responsible, spotting patterns in these two species should diverge in sympatry, but not allopatry. We predicted that female P. baenschi from sympatric sites should show a preference for associating with conspecifics vs. heterospecific males, but females from allopatric sites should show no such preferences. To evaluate these predictions, we compared spotting patterns and female association behaviors in populations of P. baenschi from Central Mexico. We found that both of our predictions were supported. Poeciliopsis baenschi that co-occured with P. turneri had spotting patterns significantly different than their counterparts from allopatric sites. Using a simultaneous choice test of video presentations of males, we also found that female P. baenschi from populations that co-occured with P. turneri spent significantly more time with males of their own species than with P. turneri males. In contrast, females from allopatric populations of P. baenschi showed no differences in the amount of time they spent with either conspecific or heterospecific males. Together, our results are consistent with the hypothesis that reproductive character displacement may be responsible for behavioral and spotting pattern differences in these populations of P. baenschi.
Article
Full-text available
Assortative mating is critical for reproductive isolation during speciation, however, the mechanisms underlying mating preferences are often unknown. Assortative mating can be mediated through preferences for condition-dependent and adaptive (“magic”) traits, but rigorously testing these hypotheses has been impeded by trait covariation in living organisms. We used computer-generated models to examine the role of body shape in producing association preferences between fish populations undergoing ecological speciation in different habitat types. We demonstrate that body shape can serve as an adaptive trait (variation in head size between populations) and a condition-dependent signal (variation in abdominal distention among individuals). Female preferences for stimuli varying in only one aspect of body shape uncovered evidence for body shape as a magic trait across population pairs, but no evidence for body shape serving as a condition-dependent signal. Evolution of preferences only in females from one habitat type as well as stronger preferences in sympatric non-sulfidic as opposed to allopatric non-sulfidic populations suggests that reinforcement may have played a role in producing the observed patterns.
Article
Studies of mate choice evolution tend to focus on how female mating preferences are acquired and how they select for greater elaboration of male traits. By contrast, far less is known about how female preferences might be lost or reversed. In swordtail fish Xiphophorus, female preference for the sword ornament is an ancestral trait. Xiphophorus birchmanni, however, is one species that has secondarily lost the sword. Using synthetic animation playback of “virtual” males, we found that female X. birchmanni preferred a swordless conspecific over a sworded heterospecific. Moreover, when offered the choice between a conspecific without a sword and one with a digitally attached sword, females preferred the former. These results suggest female preferences need not always select for elaboration of male traits, and they provide a plausible explanation for the lack of introgression of a sexual trait in a naturally occurring hybrid zone.
Chapter
In poeciliid fishes, sexual dichromism is associated with larger size and larger broods, but there is no relationship between sexual size dimorphism and sexual dichromism, or between degree of dichromism and color pattern polymorphism. Factors are discussed which influence the evolution of color pattern polymorphisms, sexual dimorphism and dichromism. Detailed studies of South American species have shown that the color patterns of poeciliid fishes have predictable effects in (1) avoiding diurnal visually hunting predators; (2) mating success; and (3) species recognition. Data from some Central American species indicate that some color pattern elements may be closely linked to physiologically variable loci, which further affect the variation in color patterns. Different elements of any given color pattern can be influenced by different modes of natural selection; in guppies the relationship between predation intensity and color pattern is different for melanin, carotenoid, and structural colors. Different color patterns have different degrees of conspicuousness on different backgrounds, and may appear differently to predators and mates with differing visual abilities.
Article
The males of the Rio Coy population of Xiphophorus nigrensis, San Luis Potosi, Mexico, exhibit a vertical bar pattern on the flank. During aggressive encounters there is an intensification of the bars as the pigment becomes dispersed throughout the melanophores whereas in submissive individuals the pigment becomes concentrated in the center of the cells and the pattern fades. The Rio Choy population of X. nigrensis, X. pygmaeus and an undescribed species from the Rio Ojo Frio, all in San Luis Potosi, lack this pattern. Within the Rio Coy population there are four size genotypes of males controlled by variation at a Y-linked locus. The pattern is strongly expressed in all males of the three larger size genotypes, but virtually absent from the small size class. In the area of size overlap between the largest males of the genetically small size class and the smallest males of the genetically next larger size class, the expression of the pattern is correlated with genotype not size. The inheritance of the pattern in F1 and backcross hybrids with the Choy population and with X. pygmaeus indicates that the trait has a polygenic basis and that the Y chromosome of the Coy stock with the factor for small size has a suppressor gene for bars. The suppressor is absent from all other X and Y chromosomes. Similar patterns are present in 14 of the 19 species of Xiphophorus, and species with and without this trait are found in each of the three major subdivisions of the genus. It is suggested that the pattern has evolved independently in different species.
Article
Poecilia sphenops alternately has been cast as several (or many) species, or as a single polytypic species. Laboratory, field, and morphological evidence gathered mainly from a mixed population of mollies in southern México, but also from other parts of México and Guatemala, indicates that "Poecilia sphenops" is not a single species but a complex of unknown magnitude. The name Poecilia butleri is resurrected from synonymy for the Pacific representative of P. mexicana in México and southern Guatemala. A natural hybrid between P. sphenops and P. butleri is described.