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Mustached males in a tropical poeciliid fish: Emerging female preference selects for a novel male trait

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One possible mechanism for the (co-)evolution of seemingly novel male traits and female preferences for them is that males exploit pre-existing female biases, and livebearing fishes (Poeciliidae) have been at the forefront of this research for almost two decades. Here, using 13 poeciliid species from four different genera, we tested whether mustache-like rostral filaments found in males of some Mexican molly (Poecilia sphenops) populations could have evolved due to exploitation of a pre-existing female bias. While Mexican mollies were the only species with a significant female association preference for mustached males, we also did not find any species exhibiting significant aversion for mustached males; rather, variance in female preference scores was large throughout. For example, more than 25% of females spent twice as much time with the mustached male compared to the non-mustached male in most species, but even 31% of Mexican molly females spent more time near the non-mustached male. Hence, a comparison of the strength of preference was inconclusive. We discuss the possibility that the female preference of P. sphenops for mustached males could be due to a female pre-existing bias (sensu lato), even if population means were not significant for species other than P. sphenops. This highlights the importance of distinguishing between population means and individual preferences when interpreting mate choice, and thus, adds depth to the concept of mating preferences as a motor for evolutionary change.
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ORIGINAL PAPER
Mustached males in a tropical poeciliid fish: emerging female
preference selects for a novel male trait
Ellen McCoy &Norbert Syska &Martin Plath &
Ingo Schlupp &Rüdiger Riesch
Received: 13 December 2010 / Revised: 26 January 2011 / Accepted: 28 January 2011
#Springer-Verlag 2011
Abstract One possible mechanism for the (co-)evolution
of seemingly novel male traits and female preferences for
them is that males exploit pre-existing female biases, and
livebearing fishes (Poeciliidae) have been at the forefront of
this research for almost two decades. Here, using 13
poeciliid species from four different genera, we tested
whether mustache-like rostral filaments found in males of
some Mexican molly (Poecilia sphenops) populations
could have evolved due to exploitation of a pre-existing
female bias. While Mexican mollies were the only species
with a significant female association preference for mus-
tached males, we also did not find any species exhibiting
significant aversion for mustached males; rather, variance in
female preference scores was large throughout. For exam-
ple, more than 25% of females spent twice as much time
with the mustached male compared to the non-mustached
male in most species, but even 31% of Mexican molly
females spent more time near the non-mustached male.
Hence, a comparison of the strength of preference was
inconclusive. We discuss the possibility that the female
preference of P. sphenops for mustached males could be
due to a female pre-existing bias (sensu lato), even if
population means were not significant for species other than
P. sphenops. This highlights the importance of distinguishing
between population means and individual preferences when
interpreting mate choice, and thus, adds depth to the concept
of mating preferences as a motor for evolutionary change.
Keywords Female choice .Mate preferences .Pre-existing
bias .Sexual selection .Character mapping
Introduction
Sexual selection, e.g., through female mate choice, can
drive male trait exaggeration, leading to sexual dimorphism
(Darwin 1871; Andersson 1994; Ryan and Rand 1993;
Rios-Cardenas and Morris 2011). There is ample evidence
for pre-existing sensory biases in females (sensu Endler
1992), and males might evolve traits to exploit those biases
(sensory exploitation; Ryan 1990; Ryan and Keddy-Hector
1992;Shaw1995; Endler and Basolo 1998). As a
prominent example, complex mating calls (whineplus
chuck) in túngara frogs (Physalaemus pustulosus) are
thought to have evolved as a consequence of pre-existing
female preferences (for auditory tuning, see Ryan et al.
1990; Wilczynski et al. 2001; Ryan 1985 for a review), and
females of other species (like Physalaemus coloradorum)
prefer conspecific calls with an artificially added hetero-
Communicated by T. Czeschlik
E. McCoy :N. Syska :I. Schlupp :R. Riesch
Department of Zoology, University of Oklahoma,
730 Van Vleet Oval,
Norman, OK 73019, USA
N. Syska
Unit of Evolutionary Biology & Systematic Zoology,
University of Potsdam,
Karl-Liebknecht Str. 24-25,
14476 Potsdam, Germany
M. Plath
Department of Ecology & Evolution, University of Frankfurt,
Siesmayerstr. 70a,
60054 Frankfurt, Germany
R. Riesch (*)
Department of Biology & W. M. Keck Center for Behavioral Biology,
North Carolina State University,
127 David Clark Labs,
Raleigh, NC 27695-7617, USA
e-mail: ruedigerriesch@web.de
E. McCoy
College of Veterinary Medicine, Texas A&M University,
College Station, TX 77843, USA
Behav Ecol Sociobiol
DOI 10.1007/s00265-011-1154-x
specific chuck, even though conspecific males are not
known to produce chucksas part of their natural
repertoire (Ryan and Rand 1993,1995,1999).
Livebearing fishes (family Poeciliidae) are prime exam-
ples for the evolution of male traits through pre-existing
biases (Basolo 1990a,b,1995a,b; Rosenthal and Evans
1998; Rodd et al. 2002; Rios-Cardenas and Morris 2011).
For example, swords (colorful extensions of the lower
caudal fin in the male sex) within the genus Xiphophorus
are thought to have evolved in response to a pre-existing
female preference for this trait in poeciliids (Basolo 1990a,
b,1995a,b;Basolo2002; but see Rosenthal and Evans
1998), even though swordtail-predators (like Astyanax
mexicanus, Characidae) also prefer males with long
swords as prey (Rosenthal et al. 2002). However, not all
poeciliid females express this preference (Basolo 2002;
Rosenthal et al. 2002; Witte and Klink 2005)andfemales
mayevenshowdisdainforswords(Basolo2002;Wong
and Rosenthal 2006).
In the present study, we use a comparative approach to
investigate the potential role of pre-existing bias for the
evolution of an unusual trait in male poeciliids: mustache-like
rostral filaments, as found in some populations of Mexican
mollies, P. sphenops (Schultz and Miller 1971; Schlupp et al.
2010). We could show beforehand that the mustache-like
structures on the rostrum of P. sphenops consist of epidermal
outgrowths on the edges of scales that appear to have no
sensory function (for functional analyses using EM micros-
copy see Schlupp et al. 2010). When given a choice between
mustached and mustache-less males, wild-caught P. sphe-
nops females prefer the mustached phenotype over males
that had their mustaches removed, suggesting that inter-
sexual selection by female choice indeed drives the evolution
of this unusual trait (Schlupp et al. 2010).
In the present study, we tested for a female preference
for males exhibiting (artificially added) mustache-like
rostral filaments in 13 species of poeciliid fishes from
various phylogenetically distant lineages using association
Fig. 1 Mate choice experiments using video-animated males with or
without mustache-like rostral filaments: aexample of video images
used for X. hellerii;bcladogram of the 13 poeciliid species included
in this study colors correspond to character history reconstruction
based on maximum parsimony analysis; cresults from the female
choice experiments depicting the strength of preference (SOP, see
main text), the percentage of females that spent at least twice as much
time near mustached males (SOP 0.25), and paired t-tests on
association time
Behav Ecol Sociobiol
preference tests and video-animated stimuli (Fig. 1). Fe-
male association preferences are good indicators of female
mate choice, e.g., in green swordtails (Xiphophorus hellerii,
Walling et al. 2010). We show that females tend to exhibit a
preference for mustachedmales in most species of
Poecilia, as indicated by positive strength of preference
(SOP) values. However, a significant preference for
mustachedmales was only discovered in P. sphenops
the species in which males naturally express the trait.
Hence, it would seem that the female preference for the trait
emerged from a latent tendency to associate with mustached
males that at least within the genus Poecilia, was already
present prior to the expression of the actual trait.
Material and methods
Study organisms and their maintenance
We examined female preferences in 13 species of poeciliid
fishes (Fig. 1b). Mexican mollies (P. sphenops) stemmed
from El Limon, Veracruz, Mexico [35.8 ±1.9 mm standard
length (SL), N=16]. Two further representatives of short-
fin mollieswere included: Atlantic mollies (Poecilia
mexicana) originated from Río Amatan in Tabasco in
southern México (35.9±0.9 mm, N=20) and from site VI/
17 (Río Purificacion) in Tamaulipas in central México
(35.9±1.6 mm, N= 15), and mangrove mollies (Poecilia
orri) came from Roatan Island off Honduras (33.4± 2.0 mm,
N=14). We included two representatives of long-fin
mollies: Sailfin mollies (Poecilia latipinna)werecollected
from Lincoln Park in Texas, USA (41.5±1.9 mm, N=12),
while Tamesi mollies (Poecilia latipunctata)werecollected
near Ciudad Mante in Tamaulipas (internal lab code III/9),
México (34.1±1.8 mm, N= 14). Gynogenetic Amazon
mollies (Poecilia formosa;populationfromLincolnPark,
37.6± 1.5 mm, N=14; and from VI/17, 38.5±2.5 mm, N=
10) are an all-female species (see below) and were either
tested with P. mexicana stimulus males (see above), or with
P. latipinna videos (Lincoln Park, 43.5±1.3 mm, N=15;
population from VI/17, 40.0 ±2.6 mm, N=9). Guppies
(Poecilia reticulata), stemmed from a feral population in
San Antonio in Texas, USA (17.6± 1.7 mm, N=15). We
included two species of Limia: laboratory-raised sulfur
limia (Limia sulphurophila) from the sulfidic Zufrada
Springs (35.4 ± 3.2 mm, N=9) and an aquarium stock of
Hispaniola limia (Limia perugiae) from the Dominican
Republic (28. 1.2 mm, N=14). Two species of Xipho-
phorus were obtained from the Xiphophorus genetic stock
center in San Marcos (Texas, USA); green swordtails
(Xiphophorus hellerii) stemmed from Río Sarabia near
Oaxaca in México (33.0± 2.2 mm, N=13); variable platyfish
(Xiphophorus variatus) came from Encino in Tamaulipas,
México (34.8±0.7 mm, N=13). Finally, we included western
mosquitofish (Gambusia affinis), which originated from a
feral population that thrives in a pond at the Aquatic
Research Facility of the University of Oklahoma, USA
(36.8±0.9 mm, N= 15), and widemouth mosquitofish
(Gambusia eurystoma), which are endemic to the highly
sulfidic Baños del Azufre near Teapa in Tabasco, Mexico
(26.8±1.2 mm, N=12).
The Amazon molly (P. f o r m o s a ) is an all-female,
ameiotic species that originated through natural hybridiza-
tion of a P. mexicana-like female and a P. latipinna-like
male around 100,000 generations ago (Avise et al. 1991;
Schartl et al. 1995). Amazon mollies are gynogenetic and
thus rely on sperm of host speciesto trigger embryogen-
esis, but normally no paternal DNA is transmitted; hence,
inheritance is clonal (Schlupp 2005). P. formosa naturally
forms mixed-species shoals with one or both of two host
species (Schlupp and Ryan 1996). In this unusual mating
system, Amazon mollies need to interact with heterospe-
cific males. Interestingly, female mating preferences have
been recorded even though indirect (genetic) benefits of
mate choice can be ruled out (Marler and Ryan 1997;
Tobler et al. 2006; Poschadel et al. 2009). Given its unique
ancestry as a natural hybrid of a long-fin and a short-fin molly,
we included the Amazon molly to test for the influence of
conflictinggenomes on the specificity of a female prefer-
ence. We predicted that if both ancestral species (P. latipinna
and P. m e x i ca n a ) differed in their preference for bearded
males, Amazon mollies should show an intermediate
preference score relative to its parental species.
Preference data for Mexican mollies (P. sphenops) were
reanalyzed from a previous study (Schlupp et al. 2010). All
species/populations included in this study were maintained
as randomly outbred stocks in tanks (2501,000 l) in a
greenhouse of the University of Oklahoma in Norman. The
tanks contained naturally growing algae and other sub-
merged plants as well as a variety of naturally occurring
invertebrates like chironomid larvae, copepods, and amphi-
pods, on which the fish could feed. In addition, they 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.
Mate-choice experiments
We used video playback techniques to assess female
preference (or avoidance) of mustached and non-mustached
males. To generate the video stimuli, we employed estab-
lished protocols (see Schlupp et al. 2010). In short, digital
images of individual males were taken while a male was
swimming in a small tank using a Nikon D70 digital
camera. The image was then extracted from the background
Behav Ecol Sociobiol
in Adobe® Photoshop Elements 6.0, duplicated, and
mustache-like rostral filaments were pasted onto the snout
region of one copy of the male picture (Fig. 1a). Conse-
quently, the pairs of animation showed two identical males
differing only in the presence or absence of a mustache
(Fig. 1a; Schlupp et al. 2010).
The resulting images were then animated and converted
to an AVI-file (resolution 800× 600) using Pencil v.0.4.4b
for Mac. 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. Simultaneous
playback was performed using two identical computer
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).
All females were only exposed to video stimuli of their
own males, the lone exception being the all-female Amazon
mollies. As a result of their hybrid origin, we tested
Amazon mollies with stimuli of both parental species.
However, individual Amazon mollies were only presented
with one set of video stimuli: either a set of videos
depicting P. latipinna males or a set of videos depicting P.
mexicana males.
Measuring female preferences
The 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
temperature was 25°C. Using the Zone Definition
function of the 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 (Exwave HAD)
placed above the setup, connected to the PC running the
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.
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, then
the cylinder was carefully removed, and the experiment was
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.
For some species (e.g., both Gambusia sp.), focal
females were often smaller than 25 mm (SL), which is the
lowest cut-off for reliable tracking with the viewer system.
For these females, times spent in either preference zone
were recorded using stopwatches, while visually tracking
fish movement on-screen of the PC monitor while running
the Viewer program.
We decided a priori to exclude side biases if females
spent more than 80% of their time in the same compartment
of the tank (i.e., the females did not follow the initially
preferred male during the course of the trial), 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). Side biases occurred in 14
cases (out of 408 trials total). No trials were excluded due
to low response.
Statistical analyses
The statistical analyses were carried out on a species-wise
level. We tested that populations did not differ in strength
of preference in those cases in which more than one
population per species were included (independent samples
t-tests, P. mexicana t
32
=0.23, P=0.82; P. formosa tested
with P. mexicana t
22
=0.52, P=0.61; P. formosa tested with
P. latipinna t
22
=-0.64, P=0.53). In a first step, we tested for
female preferences within each species separately; to do so,
association times near both types of stimulus males were
compared using paired t-tests. In a second approach, we
compared the proportion of females that preferred the
mustached-male across species (0 =female spent more time
near non-mustached male; 1=female spent more time near
mustached male) using a logistic regression with species
and log-transformed female SL as covariates. The interac-
tion term of SL by specieswas not significant (B= 0.04,
SE=0.44, Wald=0.01, df =1, P=0.93) and was therefore
removed from the final model (2 log likelihood =311.19).
We further compared the proportion of females that spent
approximately twice as much time or more with the
mustached male (i.e., SOP0.25) across species using a
similar model as before. Again, the interaction term of SL
by specieswas not significant (B=0.32, SE=0.44, Wald=
0.55, df=1, P=0.46) and was therefore removed from the
final model (2 log likelihood=260.67). Finally, we
compared the strength of preference [SOP, (time spent near
mustached maletime spent near non-mustached male)/
(time near mustached+time near non-mustached)] across
species using a general linear model, while including
female SL as a covariate. However, neither SL (F
1, 204
=
Behav Ecol Sociobiol
0.46, P=0.50) nor the interaction term of SL by species
(F
12, 204
=0.47, P=0.93) had a significant effect; thus, we
excluded SL from the final model.
To investigate how Amazon mollies would behave
relative to their parental species, we first screened the two
parental species (P. mexicana and P. latipinna) for differ-
ences in SOPs using independent t-test (t
45
=0.36, P=0.72),
and then conducted a one-sample t-test to compare Amazon
molly SOPs with the mean SOP of both parental species
(mean SOP= 0.0685).
We used a phylogenetic approach to map character
states, i.e., strength of preference (Basolo 1995b; Shaw
1995). A cladogram of the included taxa was created
(Fig. 1b); relative topologies were inferred from recent
molecular phylogenetic analyses of the entire family
Poeciliidae and of the genus Poecilia (Ptacek and Breden
1998; Breden et al. 1999; Hrbek et al. 2007). However, it is
important to note that the original phylogenies our
cladogram is based upon clearly warrant additional phylo-
genetic analysis.
For heuristic purposes, we also traced the potential
character history (i.e., the tendency to spend more time with
a mustached male) on our cladogram by conducting
maximum parsimony analysis as implemented in Mesquite
2.74 (19972010 W. & D. Maddison). For this analysis,
population means of SOP were assigned to one of four
different discrete categories [(0) aversionSOP <0.01; (1)
neutral0.01<SOP < 0.01; (2) weak preference0.1 >
SOP>0.01; (3) strong preferenceSOP> 0.1].
All reported variables are given as means ± standard error
(SE). Unless noted otherwise, all statistical analyses were
conducted using SPSS 16.0.2 for Mac (2008 SPSS Inc.).
Results
When testing for a female preference for mustached males
within each species separately, we found females to spend
significantly more time near the mustached male in P. sphenops
(t
15
=2.38, P=0.031), but not in any other taxon examined (t
1.34, P0.19; Fig. 1c). Congruently, there was a significant
difference among species in the proportion of females that
spent more time with the mustached male (logistic regression:
B±SE=0.09± 0.04, Wald=5.60, df=1, P=0.018). SL had no
significant effect in the logistic regression (B±SE=2.08±
1.16, Wald=3.20, df=1, P=0.074). Species still differed
significantly from one another when P. sphenops was removed
from the analysis (species B±SE=0.08± 0.04, Wald= 5.93,
df=1, P=0.015; SL B±SE=2.01± 1.16, Wald=3.00, df=1,
P=0.083). On the other hand, when comparing the proportion
of females that spent at least twice as much time with the
mustached male (SOP0.25), the significant difference
between species disappeared (B±SE=0.07± 0.04, Wald=
2.67, df=1, P=0.10; SL B±SE=1.44± 1.23, Wald=1.37,
df=1, P= 0.24). Yet, when plotting this percentage on a
cladogram based on the phylogenetic relationships among the
observed taxa, it appears that proportionally more fish of the
genus Poecilia had a tendency to strongly prefer mustached
males (i.e., at least 25% of the females examined per species).
However, the consistency of this pattern is broken up by the
low values for P. f o r m o s a and high proportions of X. variatus
and G. eurystoma females (Fig. 1c). Interestingly, even though
the SOP for Amazon mollies was negative relative to positive
SOPs in P. mexicana and P. latipinna, Amazon mollies did not
differ significantly from the mean SOP value of the two
parental species (one-sided t-test, t
47
=1.97; P=0.054).
No clear directional pattern of trait evolution was discern-
able when simply plotting SOP values on the cladogram; e.g.,
the second largest SOP value following P. sphenops was not
found in the closely related other short-fin molliesP.
mexicana and P. orri, but rather in Poecilia latipunctata (a
member of the long-fin mollyclade; Fig. 1). There was
considerable variance within most examined species (see
standard errors in Fig. 1c), suggesting that females of those
species did not behave uniformly. For example, females in
G. eurystoma showed a net preference close to zero along
with pronounced variance (Fig. 1c); in other words, some
females preferred the mustached male while others preferred
the non-mustached one. Due to this pronounced variance
within most species, no significant difference among the
examined taxa in the expression of the female preference
(strength of preference) was detected (one-way ANOVA
F
12,217
=0.56, P=0.87).
Finally, when applying maximum parsimony an interesting
pattern emerged: for all genera other than Poecilia,itwas
equally likely that the ancestral state was aversionor a
weaktendency to associate with the mustached males.
Furthermore, there was an almost equal number of decreases
(resulting in an aversion) and increases in the strength of the
preference. At the same time, maximum parsimony analysis
predicted that within the genus Poecilia, the ancestral state is
aweakpositive SOP (Fig. 1b), with two independent
increases resulting in strongpositive SOPs (P. sphenops
and P. latipunctata) and one decrease resulting in a neutral
SOP in P. orri. Overall, this analysis clearly reveals the lack
of a linear drive towards increasing preference strength (that
is, there is no linear movement from character state 0 to 1 to
2 to 3), instead, the pattern jumps from 0 to 1, 0 to 2, 2 to 3
and/or 2 to 1 (Fig. 1b).
Discussion
In our current study, we tested for a potential role of pre-
existing female bias for mustached males within livebearing
fishes (family Poeciliidae). If pre-existing biases (sensu
Behav Ecol Sociobiol
stricto) played a role here, we would have expected a
female preference for mustached males also in some close
relatives of P. sphenops (e.g., within the short-fin molly-
clade; Fig. 1b, c), but no such pattern was discernible.
However, it appears thatwith a few exceptionsmainly
females of the genus Poecilia tend to associate with a
mustached rather than a non-mustached male. This indi-
cates that the female preference for mustached mollies in P.
sphenops could be an emerging preference that built on an
already present tendency for mustached males even in
species other than P. sphenops. As we will argue below, if
one applied a slightly broader definition of pre-existing bias
(sensu lato) that takes into account variability of female
preferences within populations rather than interpreting
population means as species-specific stereotypic traits that
apply to all individuals, we actually find some support for it
in our data set.
This leads to the question as to how this novel trait and
the emerging female preference for it could have arisen.
The theory of sensory exploitation posits that female
preferences predate male traits, and preferences evolve
under selection other than sexual selection (Ryan 1990;
Shaw 1995; Endler and Basolo 1998; Rios-Cardenas and
Morris 2011). For example, the female preference for male
orange coloration in Trinidadian guppies (P. reticulata)is
thought to have evolved as a feeding preference [Rodd et
al. 2002; see also Madden and Tanner (2003) for male
bower decoration matching color preferences of females'
preferred food items in the regent bowerbird, Sericulus
chrysocephalus]. Likewise, it is tempting to speculate that
P. sphenops females may perceive the mustache as if the
male is ingesting food, thus indicating the presence of
resources, and making it more likely for females to
approach. In various invertebrates, nuptial feeding can
evolve when the male exploits the female's foraging
motivation in a sexual context [e.g., Sakaluk (2000) for
crickets; Bilde et al. (2007) and Andersen et al. (2008) for
spiders, Pisaura mirabilis].
Then again, in a logical extension to this hypothesis, one
would have expected other female poeciliids to also exhibit
the preference. Why then did only P. sphenops females
express a significant preference for male mustaches? We
can only speculate at this pointpossible explanations
range from thus far unknown differences in feeding ecology
to differences in the sensory environment in which female
preferences and the male trait have co-evolved. For
example, if mustaches were really perceived as worm- or
insect larvae-like prey, then a preference for male mustaches
would be more likely to evolve in insectivorous species. It
could be that P. sphenops relies more strongly on invertebrate
prey as opposed to more algivorous and detritovorous
Poecilia species (e.g., Darnell 1962; Winemiller 1993;
Kramer and Bryant 1995; Tobler 2008), but future gut-
content analyses will need to be conducted to answer this
question. The fact that no preference (nor even a positive
mean SOP) was detected in the insectivorous Gambusia
species does not preclude this hypothesis, but also does not
lend any support to it.
In this context, it is important to note that all species
investigated in the present study did show a large degree of
variance in their SOP scores (including P. sphenops,in
which 5 out of 16 females actually had a negative SOP).
While for a variety of animals, female mate choice has been
shown to vary from trial to trial (e.g., Jennions and Petrie
1997; Bell et al. 2009); several studies have demonstrated
that it is usually highly repeatable in poeciliids (e.g., Godin
and Dugatkin 1995; Brooks 1996,2002; Jennions and
Petrie 1997; Brooks and Endler 2001; Aspbury and Basolo
2002) in particular when video stimuli are presented
(Kodric-Brown and Nicoletto 1997). Still, future experi-
ments will need to confirm that the variance detected in our
study is indeed based on repeatable, and thus, potentially
heritable (but see Jennions and Petrie 1997; Brooks and
Endler 2001; Brooks 2002) individual performance or
whether it stems from ad hoc variability, in which females
sometimes prefer a mustache and sometimes not. If the
former were true, then those females with a heritable
preference for mustached males would be easy targets for
Fisherian runaway selection in the Mexican molly. Yet
again, even if the latter were true and female preferences
would vary unpredictably over time, an emerging male trait
(e.g., a mustache) may persist in a population as long as
there is (a) no uniform and strong female discrimination
against mustached males, (b) no strong natural selection
against them via other selective agents (e.g., predators), or
(c) no genetic drift events immediately removing the novel
trait from a population in which it arises. In fact, in many
poeciliids, females prefer rare male phenotypes (e.g.,
Schlupp et al. 1999; Eakley and Houde 2004), and females
are known to copy the mate choice of other females (e.g.,
Witte and Ueding 2003; Godin and Hair 2009). Conse-
quently, one could even make the argument that a novel
trait like male mustaches is actually expected to (at least
initially) spread until it reaches a certain frequency within a
population. Future experiments will need to examine this
further, for example, by measuring individual repeatability
of preference scores or by conducting selection experiments
to test whether the preference for mustached males can be
artificially selected for in species in which the trait does not
naturally occur.
The confusing case of the Amazon molly
We originally predicted that unisexual Amazon mollies,
being of hybrid origin, would show an SOP intermediate to
that of the two parental species P. latipinna and P.
Behav Ecol Sociobiol
mexicana. However, our results do not support this,
because preferences of Amazon mollies were opposite in
direction (albeit not significantly different) compared to
both parental species. How can this be explained? One
could argue that since Amazon mollies are the product of a
single hybridization event (Stöck et al. 2010) and have
clonal inheritance (Schlupp and Riesch 2011), the two
individuals that actually hybridized could have been
representatives of the fraction of individuals that exhibit(ed)
a tendency to avoid mustached males. For this scenario
to work, one would have to assume that Amazon mollies
lacked the capability to evolve [as proposed by the often
postulated hypothesis that assumes that they (and similar
species) are F
1
s frozen in time; e.g., Vrijenhoek 1979;
Rogers and Vamosi 2010]. However, recent studies have
called this result into question. For example, Amazon
mollies exhibit extensive MHC loci polymorphism, albeit
reduced relative to the two parental species (Schaschl et
al. 2008; Lampert et al. 2009),andtheyalsodiffer
morphologically and behaviorally depending on which
sexual species they co-occur with (M. Tobler, I. Schlupp
unpublished data).
Another hypothetical argument could revolve around
the fact that Amazon mollies have existed for more than
100,000 generations (Schartl et al. 1995;seeLampertand
Schartl 2008 for an even higher estimate). So, couldn't it
be that both parental species had historically been
characterized by an aversion to the mustache-like trait? If
that were the case, and again assuming that Amazon
mollies lack the ability for evolutionary change, the
tendency to prefer the mustache would then have evolved
in the parental species after the hybridization but remained
the ancestral preference in asexual Amazon mollies.
Again, we think that this is extremely unlikely because
as we argued above, there is quite convincing evidence
that Amazon mollies are capable of evolutionary change.
Furthermore, the other lineages of Poecilia that we tested
in the present study are clearly older than this particular
hybridization event (e.g., Hrbek et al. 2007), so if this
scenario were true, the tendency of some females to prefer
the mustache must have independently evolved in all
Poecilia only after the hybridization event. Once more,
this scenario seems highly unlikely.
What could be a factor, however, is that Amazon
mollies have previously been demonstrated to avoid
certain parasitized males that the two parental species
do not discriminate against (Tobler et al. 2006), while at
the same time not exhibiting the same significant
preferences for novel male traits that P. latipinna and P.
mexicana show (Schlupp et al. 1999). Potentially,
Amazon mollies are simply unsure as to whether the
unknown male trait (i.e., mustache-like rostral filaments)
is an indication of parasitization and therefore rather
play it safeby showing signs of avoidance behavior.
This scenario is clearly plausible, but our data are
unfortunately not suitable to specifically test for this.
We thus simply have to admit that at present, we do not
have a compelling explanation for the pattern our study
uncovered.
Conclusions
The present study highlights the importance of under-
standing a female preference not as an absolute trait in
the sense that it is either presentor absent.Rather,a
preference can arise as a tendency, even a very weak
one, that is acted upon by selection in nonlinear ways to
become stronger in some species, remain the same in
others, or even become weaker (e.g., P. o r r i )insome
cases. Indeed the majority of reviews on preferencetrait
coevolution stress the importance of considering prefer-
ence functions(e.g., Jennions and Petrie 1997;Brooks
and Endler 2001; Brooks 2002)orstrength of preference
(e.g., Van de Weerd et al. 1998; Higgins and Waugaman
2004); yet, the fact that preferences are a continuum rather
than discrete categories, and that small fractions of
females within a population may actually exhibit a
preference even if the population mean is neutral or
negative, is often overlooked in studies of mate choice.
Our results, therefore, add further depth to the concept of
an individual's preference as a motor for evolutionary
change.
Furthermore, we do not think that the pre-existing bias
hypothesis requires that close relatives share the bias to the
same degree or intensity as the species in which the male
trait has originated (Endler and Basolo 1998). Rather, it is
important that the origin of the female bias in whatever
strength must have predated the origin of the male trait.
Hence, even though the female preference for a mustache in
Mexican mollies is clearly not based on a pre-existing bias
in a way that close relatives share a significant preference, it
does seem to emerge from some latent tendency for
mustached males already present in a certain proportion of
females in some close relatives (and other poeciliids).
Whether this tendency to associate with mustached males is
linked to food acquisition remains to be tested. For
example, experiments investigating whether P. sphenops
females are indeed more likely to approach a male if it
carries food items in his mouth (especially if the female is
starved) are underway.
Finally, it is important to stress that the details of
preference evolution may change as more species are added
to the analysis and future studies provide us with a more
robust phylogenetic tree, but the general conclusions (as
stated above) are likely to be retained.
Behav Ecol Sociobiol
Acknowledgments We thank R. B. Langerhans for his introduction to
Mesquite and helpful discussions, as well as D. McLennan, and an
anonymous reviewer for comments that greatly helped to improve this
manuscript. The Mexican Government and the Municipal of Tacotalpa
kindly issued permits to collect fish. Financial support came from NSF
(DEB-0743406; to I. S.), and DFG (Deutsche Forschungsgemeinschaft;
PL 470/12; to M.P.).
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Behav Ecol Sociobiol
... Such variation among females in their choosiness has also been documented before [e.g., (72)(73)(74)], indicating that it is important to distinguish between population-and individual-level preferences when interpreting the mating behavior of a species. With respect to A. fasciatus, a large male body size alone may not be a strong . ...
... However, we think this to be unlikely for two reasons. First, the use of animations for investigating mate-choice has been validated in multiple systems, including Poeciliidae [e.g., swordtails: (59,77); guppies: (78); mollies: (72,79); western mosquitofish: (24,68)]. Second, we conducted several trial runs of this experimental setup using our laboratory stocks of G. holbrooki (an invasive population from southern Italy) at Royal Holloway, University of London, in the summer of 2021. ...
... Nonetheless, we acknowledge that a computer image may not allow size-or parasitization-perception as clearly as a real conspecific would be and so this is a potential limitation of the employed methods. Additionally, we used testing protocols with 2 × 5 min observation periods and video animations that are well-established for poeciliid fishes [e.g.,: (81)(82)(83); including previous studies used in our lab, such as (72,84)], but we cannot completely rule out that this is not long enough, or that the rather uniform movement of the animated fish is not stimulating enough, to elicit a response for A. fasciatus. ...
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... Furthermore, even in the presence of clear preferences, heterospecific matings may occur (e.g., Domínguez-Castanedo & Schlupp, 2023). This was argued in a study by McCoy et al. (2011), that investigated preferences for a novel trait, a mustache , that is only present in one of the species studied. Only that species, Poecilia sphenops, showed a significant preference for the mustache, but females from several other species showed some preference for the novel trait (McCoy et al., 2011). ...
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The role of hybridization as a formative process in evolution has received much attention in the past few decades. A particularly fascinating outcome of hybrid speciation is the formation of asexual hybrid species. This is the case in the Amazon molly (Poecilia formosa). It is of hybrid origin and had a P. mexicana female as mother and a P. latipinna male as father. This implies that at the beginning of the existence of Amazon mollies, a heterospecific mating must have occurred, indicating a breakdown of any potential prezygotic isolation between parental species. We studied the female mate choice behavior with present day P. mexicana and P. latipinna from several populations using standard binary choice tests. Overall, our results show that in extant P. mexicana and P. latipinna no female choice for conspecific males was detectable. Consequently, heterospecific matings are possible, even likely, and not hindered by any apparent behavioral prezygotic isolation. If female preferences in these species were comparable around the time the Amazon molly originated as a hybrid species ca. 100.000 years ago, matings leading to hybrids would be very likely. Furthermore, for the first time we tested the mating preferences of F1 hybrid females and found that they also have no discernable mating preferences, potentially leading to F2 individuals and/or backcrosses.
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Sexual selection research has long focused on the evolution of female mate preferences. Most of the models that have been developed posit that mate preferences evolve in a mating context. In contrast, the sensory bias model proposes that mate choice preferences arise in a non-mating context, as a by-product of natural selection acting on a female’s perceptual system. Recent research has shown that many species of fishes, from across a large clade including poeciliids, goodeids, and medaka, have a bias for long wavelength (LW) colors (yellow, orange, red) in a non-mating context. Even species that do not have LW-colored ornaments, apparently because they have been lost secondarily, retain this latent bias for LW colors. Here, we predicted that female Oryzias latipes (Japanese medaka), a drab species with a latent preference for LW colors, would show a mate choice preference for males with an artificial secondary sexual trait—a colored stripe added to their flank. We confirmed that females were more responsive to red and orange objects in a non-mating context than to other colors. We also showed that females were less resistant towards males with an LW-colored stripe than to those enhanced with a non-LW stripe and that, for many females, responses towards specific LW colors were consistent across these non-mating and mating contexts. Therefore, our results provide support for the sensory bias model by providing a link between a sensory bias in a non-mating context and a mate choice preference in a drab species like medaka.
Article
The initial purpose of the project described herein was to assess the preference of female Poecilia latipinna for an artificial novel male trait—an orange‐colored distal fringe added to the caudal fin of an otherwise wild‐type conspecific. Analysis of the preliminary data revealed consistent individual differences in the strength of female preference for either orange‐tailed or wild‐type males. This finding inspired the study's second aim—to evaluate whether the preference for orange‐tailed males observed among a subset of females could spread via mate choice copying to others in the population that initially preferred wild‐type males. Two experiments and a control were conducted wherein females were simultaneously presented with an orange‐tailed and a wild‐type dummy male using a standard dichotomous choice design. In the first experiment, female preference was assessed on two separate occasions in order to characterize the variability and consistency in preference for orange‐tailed versus wild‐type males. The second experiment addressed mate choice copying: Female preference was again assessed on two separate occasions, but involved pairing a model female with the non‐preferred male for a period of time between preference tests. A third set of control tests were conducted using the same protocol as the copying experiment except that subject females were unable to see the model paired with the non‐preferred male. Results showed that, although females collectively preferred neither the orange‐tailed nor the wild‐type dummy male in the first round of preference tests, the majority showed relatively strong individual preferences. The subset of females that preferred the orange‐tailed over the wild‐type male in the first round of testing all maintained their preferences in the second round whether or not they had observed a model in association with the non‐preferred wild‐type male between tests. However, females that preferred the wild type over the orange male in the first round of testing copied the model's choice of the non‐preferred orange‐tailed male in their second round of preference testing. These results highlight the importance of recognizing the likelihood that only a subset of females will express a preference as it first emerges within a population. In such instances, the preference may not be detected at the population level—a point frequently overlooked in studies of mate choice. Additionally, these data highlight the importance of assessing the preferences of individual females and their capacity to drive evolutionary change within populations. Lastly, this study offers evidence of a possible mechanism by which a novel male trait might spread via mate choice copying by exploiting an emerging sensory bias within a subset of females in the population.
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Male reproductive biology can by characterized through competition over mates as well as mate choice. Multiple mating and male mate choice copying, especially in internally fertilizing species, set the stage for increased sperm competition, i.e., sperm of two or more males can compete for fertilization of the female’s ova. In the internally fertilizing fish Poecilia mexicana, males respond to the presence of rivals with reduced expression of mating preferences (audience effect), thereby lowering the risk of by-standing rivals copying their mate choice. Also, males interact initially more with a non-preferred female when observed by a rival, which has been interpreted in previous studies as a strategy to mislead rivals, again reducing sperm competition risk (SCR). Nevertheless, species might differ consistently in their expression of aggressive and reproductive behaviors, possibly due to varying levels of SCR. In the current study, we present a unique data set comprising ten poeciliid species (in two cases including multiple populations) and ask whether species can be characterized through consistent differences in the expression of aggression, sexual activity and changes in mate choice under increased SCR. We found consistent species-specific differences in aggressive behavior, sexual activity as well as in the level of misleading behavior, while decreased preference expression under increased SCR was a general feature of all but one species examined. Furthermore, mean sexual activity correlated positively with the occurrence of potentially misleading behavior. An alternative explanation for audience effects would be that males attempt to avoid aggressive encounters, which would predict stronger audience effects in more aggressive species. We demonstrate a positive correlation between mean aggressiveness and sexual activity (suggesting a hormonal link as a mechanistic explanation), but did not detect a correlation between aggressiveness and audience effects. Suites of correlated behavioral tendencies are termed behavioral syndromes, and our present study provides correlational evidence for the evolutionary significance of SCR in shaping a behavioral syndrome at the species level across poeciliid taxa.
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The appearance of vertebrate species that reproduce without genetic recombination has been explained by their origin from a rare hybridization event between members of two distantly related species. For the first recognized vertebrate unisexual, the Amazon molly Poecilia formosa, mostly morphological and biochemical genetic information has been available so far with respect to its evolutionary origin. DNA sequence analyses of transcribed portions of the genome (tyrosine kinase proto-oncogenes) demonstrated its hybrid state unequivocally. Both alleles can be traced in a DNA sequence-based phylogenetic tree to extant species that represent the parental species or that are closely related to the corresponding extinct forms, namely P. mexicana limantouri and a so far taxonomically ill-defined north Mexican subspecies of the P. latipinna/P. velifera complex. A rough estimate from the mutation rates dates the hybridization event further back than would have been predicted on the basis of "Muller's ratchet" for an ecologically successful species.
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We investigated the role of maintenance and origin of female mating preferences in three species of fish. Poecilia latipinna and P. mexicana are sexual species that hybridized to form the gynogenetic clonal P. formosa, which reproduces asexually but requires sperm to initiate embryogenesis. We demonstrate that all three species display almost identical and statistically indistinguishable preferences for large males. Although processes of good genes, runaway sexual selection, and direct selection could maintain preferences in the sexual species, good genes and runaway sexual selection are unlikely to operate in the asexual species. Furthermore, we found that the most likely direct selection benefit, an increase in fecundity, can also be excluded in the gynogens. We conclude that the most parsimonious explanation for this P. formosa preference is that it was inherited from the parental species and is maintained without forces generated by good genes, runaway selection, or direct selection for increased fecundity. This preference may be maintained because of pleiotropic effects (e.g., sensory bias) or mate searching costs.
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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.
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Michael J. Ryan attended Glassboro State College in New Jersey, 1971–75, with the intention of being a high school teacher, but his interests were highjacked by field biology. A master’s degree from Rutgers in 1977 shored up his interests in herpetology and animal behavior, and a Ph.D. from Cornell University in 1982 schooled him in the fundamentals of behavioral ecology and taught him how these interests could be fused with an understanding of the underlying neural mechanisms. While at Cornell, he began a life-long association with the Smithsonian Tropical Research Institute in 1978, where he is currently a research associate and where he met Stan Rand, a valuable colleague and friend until he passed away in 2005. He was a Miller Fellow at the University California, Berkeley, from 1982 to 1984, and this is where he learned the value of incorporating comparative approaches and thus brought to fruition his continuing interests in brain, behavior, and evolution. He became as assistant professor at the University of Texas, Austin, in 1984 and has remained there since.
Article
The appearance of vertebrate species that reproduce without genetic recombination has been explained by their origin from a rare hybridization event between members of two distantly related species. For the first recognized vertebrate unisexual, the Amazon molly Poecilia formosa, mostly morphological and biochemical genetic information has been available so far with respect to its evolutionary origin. DNA sequence analyses of transcribed portions of the genome (tyrosine kinase proto-oncogenes) demonstrated its hybrid state unequivocally. Both alleles can be traced in a DNA sequence-based phylogenetic tree to extant species that represent the parental species or that are closely related to the corresponding extinct forms, namely P. mexicana limantouri and a so far taxonomically ill-defined north Mexican subspecies of the P. latipinna/P. velifera complex. A rough estimate from the mutation rates dates the hybridization event further back than would have been predicted on the basis of ''Muller's ratchet'' for an ecologically successful species.