Diversification of a food-mimicking male ornament via sensory drive.
ABSTRACT The evolutionary divergence of sexual signals is often important during the formation of new animal species, but our understanding of the origin of signal diversity is limited [1, 2]. Sensory drive, the optimization of communication signal efficiency through matching to the local environment, has been highlighted as a potential promoter of diversification and speciation . The swordtail characin (Corynopoma riisei) is a tropical fish in which males display a flag-like ornament that elicits female foraging behavior during courtship. We show that the shape of the male ornament covaries with female diet across natural populations. More specifically, natural populations in which the female diet is more dominated by ants exhibit male ornaments more similar to the shape of an ant. Feeding experiments confirm that females habituated to a diet of ants prefer to bite at male ornaments from populations with a diet more dominated by ants. Our results show that the male ornament functions as a "fishing lure" that is diversifying in shape to match local variation in female search images employed during foraging. This direct link between variation in female feeding ecology and the evolutionary diversification of male sexual ornaments suggests that sensory drive may be a common engine of signal divergence.
- SourceAvailable from: Molly E Cummings
Dataset: Perceptual Biases and Mate Choice[Show abstract] [Hide abstract]
ABSTRACT: Our view of the evolution of sexually selected traits and preferences was influenced radically in the 1990s by studies that emphasized how signals interact with sensory properties of receivers. Here, twenty-five years later, we review evidence that has accumulated in support of this idea. We replace the term sensory biases with perceptual biases to emphasize the growing knowledge of how cognitive processes generate selection on sexual traits. We show that mating preferences among conspecifics (e.g., sexual selection by mate choice) often are influenced by perceptual adaptations and constraints that have evolved in other contexts. We suggest that these perceptual biases need not be costly to females when they influence mate choice because in many cases they generate direct benefits. Although we do not reject a role for indirect benefits in mate choice, such as good genes, exclusive focus on eugenic mate choice limits our understanding of the evolution of the remarkable diversity of sexually selected traits. Sexual selection: variance in reproductive success that results from variance in access to mates Interacting forces: any combination of female choice, male choice, male competition, and/or female competition Sensory traps: traits that attract females because they resemble stimuli that are salient in other contexts Sensory drive: sensory and signaling trait evolution driven by ecological determinants Sensory exploitation: occurs when males evolve traits that increase their attractiveness to females due to preexisting biases of females
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ABSTRACT: Biotic and abiotic factors have been proposed to explain patterns of reproductive character displacement, but which factor is most important to character displacement of acoustic signals is not clear. Male vocalizations of the frog Pseudacris feriarum are known to undergo reproductive character displacement in areas of sympatry with P. brimleyi and P. nigrita. Despite evidence for reinforcement as an important mechanism, local adaptation via sensory drive might explain this pattern because Pseudacris breed in different habitat types and mating signals are exposed to a variety of environments. We tested the sensory drive hypothesis by playing synthesized vocalizations representing the spectrum of variation in P. feriarum at 12 different study sites. If sensory drive has occurred, then vocalizations should transmit better in the site of origin or at ecologically similar sites. We found that variation in acoustic signals did not produce better transmission in particular sites, the effect of site was uniform, and acoustic signals often transmitted better in habitats external to their origin. Ecological variation among habitats did not explain signal degradation. Our playback experiments, ecological analyses, and comparisons of different habitat types provide no support for sensory drive as a process promoting reproductive character displacement in this system. Reinforcement is the more likely primary mechanism. This article is protected by copyright. All rights reserved.Evolution 01/2014; · 4.66 Impact Factor
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ABSTRACT: Theoretical and empirical research indicates that sexual selection interacts with the ecological context in which mate choice occurs, suggesting that sexual and natural selection act together during the evolution of premating reproductive isolation. However, the relative importance of natural and sexual selection to speciation remains poorly understood. Here, we applied a recent conceptual framework for examining interactions between mate choice divergence and ecological context to a review of the empirical literature on speciation by sexual selection. This framework defines two types of interactions between mate choice and ecology: internal interactions, wherein natural and sexual selection jointly influence divergence in sexual signal traits and preferences, and external interactions, wherein sexual selection alone acts on traits and preferences but ecological context shapes the transmission efficacy of sexual signals. The objectives of this synthesis were 3-fold: to summarize the traits, ecological factors, taxa, and geographic contexts involved in studies of mate choice divergence; to analyze patterns of association between these variables; and to identify the most common types of interactions between mate choice and ecological factors. Our analysis revealed that certain traits are consistently associated with certain ecological factors. Moreover, among studies that examined a divergent sexually selected trait and an ecological factor, internal interactions were more common than external interactions. Trait-preference associations may thus frequently be subject to both sexual and natural selection in cases of divergent mate choice. Our results highlight the importance of interactions between sexual selection and ecology in mate choice divergence and suggest areas for future research.Journal of Heredity 08/2014; 105(S1):782-794. · 1.97 Impact Factor
Current Biology 22, 1440–1443, August 7, 2012 ª2012 Elsevier Ltd All rights reserved http://dx.doi.org/10.1016/j.cub.2012.05.050
Diversification of a Food-Mimicking
Male Ornament via Sensory Drive
Niclas Kolm,1Mirjam Amcoff,1Richard P. Mann,2
and Go ¨ran Arnqvist1,*
1Animal Ecology, Department of Ecology and Genetics,
Uppsala University, Norbyva ¨gen 18D, 75236 Uppsala, Sweden
2Department of Mathematics, Uppsala University, Box 480,
75106 Uppsala, Sweden
The evolutionary divergence of sexual signals is often
important during the formation of new animal species, but
our understanding of the origin of signal diversity is limited
[1, 2]. Sensory drive, the optimization of communication
signal efficiency through matching to the local environment,
has been highlighted as a potential promoter of diversifica-
tion andspeciation . Theswordtailcharacin (Corynopoma
riisei) is a tropical fish in which males display a flag-like
ornament that elicits female foraging behavior during court-
ship. We show that the shape of the male ornament covaries
with female diet across natural populations. More specifi-
cally, natural populations in which the female diet is more
dominated by ants exhibit male ornaments more similar to
the shape of an ant. Feeding experiments confirm that
females habituated to a diet of ants prefer to bite at male
ornaments from populations with a diet more dominated
by ants. Our results show that the male ornament functions
as a ‘‘fishing lure’’ that isdiversifying in shape to match local
This direct link between variation in female feeding ecology
and the evolutionary diversification of male sexual orna-
mentssuggests thatsensorydrive maybe acommonengine
of signal divergence.
tion systems through adaptation to local environmental condi-
tions, has been suggested to be an important promoter of
signal diversification through selection to maximize signal effi-
ciency [3–6]. Given enough variation among populations in the
ecological variables that directly or indirectly affect signal effi-
cacy, sensory drive could generate divergence in signal traits
(e.g., sexual ornaments) and cause speciation when signals
are involved in mate choice [6–11]. So far, demonstrations of
divergence through sensory drive have been restricted to vari-
ation in signals that covary with the physical and structural
properties of the habitat: the relationship between male color-
ation and local light conditions in sticklebacks and cichlid
fishes [8, 10], the relationship between body coloration and
the structural properties of the signaling background across
chameleon species , and the interspecific correlation
between male song and acoustic conditions in Amazonian
song birds . Yet, there are good reasons to believe that
biotic factors may indirectly play a key role in sensory drive
[13, 14]. This would be the case whenever signal efficacy is
affected by perception adaptations in the receiver that directly
reflect environmental variation in factors such as local food
abundance or predator fauna . It has, for example, been
suggested that evolutionary diversification of color ornamen-
tation in nectarivorous and frugivorous birds originated by
color matching to various flowers and fruits utilized as food
resources (e.g., [16, 17]). Here, we investigated whether varia-
ornament morphology in the swordtail characin (Corynopoma
riisei). This small freshwater fish is common in streams in Trini-
dad and northern Venezuela . Males are equipped with
a flag-like ornament on each operculum that they display
during courtship (Figure 1). Females react to the flag ornament
as they would to a food item, biting vigorously at the ornament
and thereby positioning themselves in a manner allowing
sperm transfer to females . Fertilization is internal, and
females store viable sperm for many months . The remark-
able sexual dimorphism in this species has been suggested to
result from sensory exploitation, whereby the male opercular
flag ornament functions as a food mimic [20–23].
Recent work on this species has revealed that Trinidadian
populations are genetically distinct and that the shape of the
male ornament varies strikingly across populations . The
swordtail characin feeds mainly on uniformly sized terrestrial
invertebrates that fall onto the water surface from the sur-
rounding vegetation, and the diet is heavily dominated by
arboreal ants, which make up about 50% of all prey items
. Other common prey items are beetles (adults and larvae),
springtails, and dipteran larvae. Importantly, female food utili-
zation varies across populations chiefly in the proportion of
prey items that are ants, ranging from about 10% to 75%
. The terrestrial input of ants varies consistently across
streams in Trinidad (see Discussion), and swordtail characin
populations inhabiting wider streams with more canopy cover
have a larger proportion of ants in the diet . Here, we
posited that the observed differentiation of the male sexual
signal  is generated by sensory drive, where variation in
the shape of the flag ornament has evolved to match environ-
mentally imposed local variation in the search images that
females employ during foraging. To test this hypothesis, we
performed (1) a comparative study of covariation between
male ornament shape and female food utilization across 17
natural populations in Trinidad and (2) a set of experiments
where we assessed whether female food habituation affects
their attraction to male ornaments.
Covariation between Female Diet and Male Ornamentation
across Wild Populations
We characterized the shape of male ornaments from different
populations using elliptic Fourier analysis  and then tested
for an association between the shape of the flag ornament and
female diet across populations, using canonical correlation
analysis (see Supplemental Experimental Procedures for full
descriptions of shape and gut content analyses). We found
that female food utilization indeed covaried with the shape of
the male ornament across populations (whole set correlation
R2X,Y = 0.986, Rao’s F25,27.5 = 2.367, p = 0.015). A closer
inspection of this covariation revealed a tight correlation
between the first pair of canonical variables (see Figure 2)
and showed that ornaments in populations where females
forage more on ants were more tapered and curved toward
the distal end compared to populations where females forage
primarily on other prey items. These precise shape character-
istics also define the outline of a typical ant, where the thick
abdomen tapers off toward the anterior end and the ventral
margin is concave whereas the dorsal is convex  (Figure 2).
This contrasts with the shape of beetles, the second most
common prey item , which is oval and more uniform.
However, a covariation across populations between orna-
ment morphology and female diet is necessary but not suffi-
cient evidence for our hypothesis. A direct comparative test
of sensory drive through food mimicry must also demonstrate
that such a covariation describes a resemblance between the
male ornament and the mimicked food item, using objective
measures of resemblance. In order to provide a comparative
test of whether the male flag ornament of the swordtail char-
acin mimics an ant, we assessed the relationship between (1)
shape similarity between the population-specific average
ornament and the average shape of an ant (extracted from
female guts) on one hand and (2) proportion of ants in the
female diet on the other. We found that the overall shape
similarity between the flag ornament and an ant was signifi-
cantly correlated with the proportion of prey items that were
ants across populations (Figure 3). Thus, ornaments were
indeed most ant-like in populations where females forage
most on ants.
Female Foraging Experience and Preference for Male
We performed two laboratory experiments testing the shared
prediction that male flag ornaments from populations where
female diet is dominated by ants are more efficient at attract-
ing the attention of females that have been habituated to
forage on ants. For this, we used captive-reared animals
from an aquarium stock that were naive to foraging on ants
prior to the experiment, to standardize previous female
feeding history, thus ensuring that any effect would be due
to food habitation during the experiment. We allowed one
group of adult females to feed on ants by presenting ants
onto the water surface while a second group of females were
fed other food items. We then recorded the behavior of these
females in choice tests where they were presented with two
ablated male ornaments simultaneously: one from a male of
a population where the diet consisted mostly of ants, and
another from a male of a population with few ants in the diet
(see Supplemental Experimental Procedures for full descrip-
tion of experimental design). As predicted, females habituated
toeatingants directed alarger proportion of bitestoward male
flag ornaments derived from populations in which the female
diet was dominated by ants (Figure 4). These experiments
thus confirmed the hypothesis that male flag ornaments from
populations where females eat more ants not only are more
similar to ants but are actually more efficient at attracting the
attention of females that are habituated to eating ants.
Whenever male signals have evolved to mimic female food
through sensory drive is predicted when female food utiliza-
tion varies across populations. We first note that our results
provide evidence for sensory exploitation. They suggest that
the shape of the male flag ornament of the swordtail characin
has evolved to track the search images that females employ in
foraging and that the ornament thus essentially functions as
a ‘‘fishing lure’’ aimed at attracting the attention of females.
Figure 1. Courtship in the Swordtail Characin
Male (right) displaying his opercular flag ornament in front of a female (left),
who moves in to bite at the ornament.
Figure 2. Female Diet Covaries with Male Ornament Morphology across
Populations are ordinated along the first pair of canonical variables
(Rc= 0.918, c225= 44.77, p = 0.009), and symbols depict the mean outline
of the male ornament in each population. Here, female food utilization
(CV1X) is positively correlated across populations with the average propor-
tion of female prey items that are ants (r = 0.66, p = 0.004), such that females
inpopulation locatedfurthertotherightinthisordination spaceforagemore
on ants, whereas those in populations further to the left forage more
on other invertebrate prey items (e.g., beetles [r = 20.42]). The second
pair of canonical variables (data not shown) was not statistically significant
(c216= 25.31, p = 0.065). Inserted at the lower right, outside of the ordination
space, is the mean outline of an ant (from a sample of ants from female guts)
for comparison. See Supplemental Experimental Procedures for full
description of analyses.
Diversification via Sensory Drive
Several related fish species within the family Glandulocaudi-
nae exhibit analogous, but not homologous, male ornaments
. Physical proximity and appropriate positioning of the
female is important for successful sperm transfer in these
internally fertilizing fish that lack external genitalia in males
,and these male ornaments have likely evolved as a means
for males to achieve the necessary proximity to their mates.
The form of sensory exploitation  involved in the evolution
of male ornaments in the swordtail characin bears similarities
to male signals in, for example, water mites (where males
vibrate their legs near females to mimic the movements of
the copepod prey that females feed on ), Goodeinae fishes
(where males in some species bear a larvae-like terminal
yellow band on the tail that evokes feeding responses in
females [28, 29]), guppies (where orange coloration in males
may resemble orange-colored fruits that females occasionally
feed upon ), and orchid bees (where males collect and emit
fragrances of those flowers thatfemales use as nectarsources
). Sensory exploitation is, however, not synonymous with
sensory drive [6, 14]. Future studies of systems such as those
above, where signals have evolved at least in part by sensory
exploitation, could test whether sensory drive is a common
outcome of biotic variation.
The results of our experimental food habituation show that
the modulation of female food preference for male flag orna-
ments reflects, at least initially, a phenotypically plastic re-
sponse to local food abundance. After even a brief period of
food habituation (10 days), previously naive females re-
sponded to the food habituation treatment. This is in line
with a general role for phenotypic plasticity in diversification
. Here, plastic responses in the signal receiver would
generate variation in the sexual selection regimes experienced
by the signalers. For this mechanism to result in signal diversi-
fication, two conditions must be met. First, some level of
temporal stability in food composition is required for signal
diversification to evolve. This condition is met in the swordtail
characin: ants represent a large proportion of the terrestrial
invertebrate input into Trinidadian streams, and there are
marked and significant differences across streams in this
proportion . Moreover, this variation is consistent over
time when seasonal variation in terrestrial input is taken into
account . In fact, physical environmental features of
streams predict terrestrial invertebrate input and, conse-
quently, the composition of female diet across populations
[24, 33]. Second, gene flow between populations must be
limited, to allow for genetic differentiation. Again, this condi-
tionismet in thestudied populations of the swordtail characin:
analyses based on neutral genetic markers have revealed
extensive genetic structuring even within single river drain-
The results of our study of the swordtail characin are consis-
tent with the predicted effect of variation in feeding ecology
on diversification of a sexual signal through sensory drive.
This suggests that interpopulation environmental variation in
sensory drive even in the absence of differences in abiotic
factors. Furthermore, our results also blur the distinction
between female food preferences and female mate prefer-
ences  and provide an example of how the concerted
effects of natural and sexual selection can generate signal
divergence . In light of the fact that environmental variation
is omnipresent, variation in variables such as food abundance
or predator/parasite fauna may commonly trigger the diver-
gent evolution of signal design through its effect on signal
perception among receivers. We suggest that this form
of sensory drive is an unappreciated source of signal
Supplemental Information includes one figure, one table, and Supplemental
Experimental Procedures and can be found with this article online at http://
Figure 4. Females Habituated to Feeding on Ants Bite More Often at Flag
Ornaments of Males from Populations with a Female Diet Rich in Ants
ants in two independent experiments (C, experiment 1; B, experiment 2),
when females were given a choice between an ornament from a population
with a diet rich in ants and an ornament from a population with a diet con-
taining few ants. Females habituated to a diet of ants prior to these trials
showed a preference for biting at ornaments from populations with a higher
proportion of ants in the female diet, compared to females habituated to
other food items (experiment 1 [ants versus flake food]: c21= 3.49; experi-
ment 2 [ants versus Drosophila larvae]: c21= 1.57) (two-tailed weighted Z
combined probability; p=0.031).Errorbarsrepresentestimatesofstandard
error. See Supplemental Experimental Procedures for full description of
experimental design and statistical analyses.
Figure 3. Male Ornaments Are More Ant-like in Populations Where Females
Forage More on Ants
Relationship across populations between the proportion of ants in the
diet of adult females and the similarity in average shape between the male
ornament and an ant (r17= 0.60, p = 0.011).
Current Biology Vol 22 No 15
This work was funded by the Swedish Research Council (N.K. and G.A.) and
by a European Research Council AdG grant (G.A.). We thank Mary Alkins-
Koo and Dawn Phillip for invaluable practical advice and Stan Weitzman
for sharing his knowledge on the swordtail characin. We also thank Denise
Dowlath, Trina Halfhide, and Devon Ramoo for assistance in the field; Diana
Steiner for laboratory assistance; and Anna Moosegard Schmidt for
providing ants. Anders Berglund and Locke Rowe provided constructive
comments on an earlier draft of the manuscript.
Received: March 16, 2012
Revised: May 2, 2012
Accepted: May 29, 2012
Published online: July 12, 2012
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Diversification via Sensory Drive