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: anst.uu.se[show abstract] [hide abstract]
ABSTRACT: In the sexually dimorphic swordtail characin (Corynopoma riisei, Gill), males are equipped with an opercular flag-ornament that has been suggested to function as a food-mimic since females bite at the ornament during courtship. However, virtually nothing is known about the diet in wild populations of this species. In this study, we first investigated composition of and variation in the diet of C. riisei across 18 different populations in Trinidad, using gut content analyses. We then related variation in gut content to habitat features of populations to investigate the potential link between environmental conditions and prey utilization. Our results showed that the dominating food type in the gut was various terrestrial invertebrates, both adults and larvae, but we also document substantial variation in prey types across populations. Furthermore, a canonical correlation analysis revealed a relationship between environmental characteristics and diet: populations from wider and more rapidly flowing streams with more canopy cover tended to have a diet based more on ants and mosquitoes while populations from narrow and slow flowing streams with little canopy cover tended to have a diet based more on springtails, mites and mayfly larvae. Our results add novel information on the ecology of this interesting fish and suggest the possibility of local adaptation reflecting differences in prey availability across natural populations. KeywordsSexual dimorphism–Gut content–Sensory exploitation–Sensory drive–Local adaptation–HabitatEnvironmental Biology of Fishes 01/2011; 92(2):159-166. · 1.31 Impact Factor
- [show abstract] [hide abstract]
ABSTRACT: Some of the most spectacular and diverse traits in animals are the signals used to attract mates. Closely related species often differ dramatically in signaling traits, in spite of similarity in other morphological traits. The idea that reproductive isolation arises when male mating signals and female preferences differ among populations is an old one. However, until recently, there was almost no information on what generates diversity in mating signals and preferences. This is beginning to change, with emerging results that highlight the importance of habitat differences in generating this diversity. Such differences in ecology are at the root of one hypothesis for divergence in sexual signaling – sensory drive. The sensory drive hypothesis focuses on how communication systems adapt to local environments and predicts that divergence in communication systems will occur when environments differ. Reproductive isolation can arise as a byproduct of this adaptive divergence in behavior.Trends in Ecology & Evolution. 01/2002;
- [show abstract] [hide abstract]
ABSTRACT: Much of the literature on male-female coevolution concerns the processes by which male traits and female preferences for these can coevolve and be maintained by selection. There has been less explicit focus on the origin of male traits and female preferences. Here, I argue that it is important to distinguish origin from subsequent coevolution and that insights into the origin can help us appreciate the relative roles of various coevolutionary processes for the evolution of diversity in sexual dimorphism. I delineate four distinct scenarios for the origin of male traits and female preferences that build on past contributions, two of which are based on pre-existing variation in quality indicators among males and two on exploitation of pre-existing sensory biases among females. Recent empirical research, and theoretical models, suggest that origin by sensory exploitation has been widespread. I argue that this points to a key, but perhaps transient, role for sexually antagonistic coevolution (SAC) in the subsequent evolutionary elaboration of sexual traits, because (i) sensory exploitation is often likely to be initially costly for individuals of the exploited sex and (ii) the subsequent evolution of resistance to sensory exploitation should often be associated with costs due to selective constraints. A review of a few case studies is used to illustrate these points. Empirical data directly relevant to the costs of being sensory exploited and the costs of evolving resistance is largely lacking, and I stress that such data would help determining the general importance of sexual conflict and SAC for the evolution of sexual dimorphism.Philosophical Transactions of The Royal Society B Biological Sciences 03/2006; 361(1466):375-86. · 6.23 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
1. Schluter, D. (2000). The Ecology of Adaptive Radiation (Oxford: Oxford
2. Coyne, J.A., and Orr, H.A. (2004). Speciation (Sunderland, MA: Sinauer
3. Endler, J.A., and McLellan, T. (1988). The processes of evolution—
Toward a newer synthesis. Annu. Rev. Ecol. Syst. 19, 395–421.
tion. Am. Nat. 139, 125–153.
5. Endler, J.A. (1993). Some general comments on the evolution and
design of animal communication systems. Philos. Trans. R. Soc.
Lond. B Biol. Sci. 340, 215–225.
6. Boughman, J.W. (2002). How sensory drive can promote speciation.
Trends Ecol. Evol. 17, 571–577.
7. Turelli, M., Barton, N.H., and Coyne, J.A. (2001). Theory and speciation.
Trends Ecol. Evol. 16, 330–343.
8. Boughman, J.W. (2001). Divergentsexual selection enhances reproduc-
tive isolation in sticklebacks. Nature 411, 944–948.
9. Kirkpatrick, M., and Ravigne ´, V. (2002). Speciation by natural and sexual
selection: models and experiments. Am. Nat. 159 (Suppl 3), S22–S35.
Miyagi, R., van der Sluijs, I., Schneider, M.V., Maan, M.E., Tachida, H.,
et al. (2008). Speciation through sensory drive in cichlid fish. Nature
11. Tobias, J.A., Aben, J., Brumfield, R.T., Derryberry, E.P., Halfwerk, W.,
Slabbekoorn, H., and Seddon, N. (2010). Song divergence by sensory
drive in Amazonian birds. Evolution 64, 2820–2839.
12. Stuart-Fox, D., Moussalli, A., and Whiting, M.J. (2007). Natural selection
on social signals: signal efficacy and the evolution of chameleon display
coloration. Am. Nat. 170, 916–930.
13. West-Eberhard, M.J. (1984). Sexual selection, competitive communica-
tion and species-specific signals in insects. In Insect Communication,
T. Lewis, ed. (New York: Academic Press), pp. 283–324.
14. Ryan, M.J. (1990). Sexual selection, sensory systems and sensory
exploitation. Oxf. Surv. Evol. Biol. 7, 157–195.
15. Arnqvist, G. (2006). Sensory exploitation and sexual conflict. Philos.
Trans. R. Soc. Lond. B Biol. Sci. 361, 375–386.
16. Madden, J.R., and Tanner, K. (2003). Preferences for colored bower
decorations can be explained in a non-sexual context. Anim. Behav.
17. Schaefer, H.M., Schaefer, V., and Levey, D.J. (2004). How plant-animal
interactions signal new insights in communication. Trends Ecol. Evol.
18. Weitzman, S.H., and Menezes, N.A. (1998). Relationships of the tribes
and genera of the Glandulocaudine (Ostariophysi: Characiformes:
Characidae) with a description of a new genus, Chrysobrycon. In
Phylogeny and Classification
Characiformes, L.R. Malabarba, R.E. Reis, R.P. Vari, Z.M.S. Lucena,
and C.A.S. Lucena, eds. (Porto Alegre, Brazil: EdiPUCRS), pp. 171–192.
19. Nelson, K. (1964). Behavior and morphology in the glandulocaudine
fishes (Ostariophysi, Characidae). Univ. Calif. Publ. Zool. 75, 59–152.
20. Wickler, W. (1968). Mimicry in Plants and Animals (New York:
21. Arnqvist, G., and Rowe, L. (2005). Sexual Conflict (Princeton, NJ:
Princeton University Press).
22. Amcoff, M., Arnqvist, G., and Kolm, N. (2009). Courtship signaling with
a labile bilateral signal: males show their best side. Behav. Ecol.
Sociobiol. 63, 1717–1725.
23. Arnqvist, G., and Kolm, N. (2010). Population differentiation in the
swordtail characin (Corynopoma riisei): a role for sensory drive?
J. Evol. Biol. 23, 1907–1918.
24. Kolm, N., and Arnqvist, G. (2011). Environmental correlates of diet in
the swordtail characin (Corynopoma riisei, Gill). Environ. Biol. Fish. 92,
25. Rohlf, F.J. (1992). The analysis of shape variation using ordinations of
fitted functions. In Ordinations in the Study of Morphology, Evolution
and Systematics of Insects: Applications and Quantitative Genetic
Rationales, J.T. Sorensen and R. Foottit, eds. (Amsterdam: Elsevier),
26. Ho ¨lldobler, B., and Wilson, E.O. (1990). The Ants (Cambridge, MA:
Harvard University Press).
27. Proctor, H.C. (1991). Courtship in the water mite Neumania papillator:
males capitalize on female adaptations for predation. Anim. Behav.
28. Garcia, C.M., and Ramirez, E. (2005). Evidence that sensory traps can
evolve into honest signals. Nature 434, 501–505.
29. Garcia, C.M., and Lemus, Y.S. (2012). Foraging costs drive female resis-
tance to a sensory trap. Proc. Biol. Sci. 279, 2262–2268.
30. Rodd, F.H., Hughes, K.A., Grether, G.F., and Baril, C.T. (2002). A
possible non-sexual origin of mate preference: are male guppies
mimicking fruit? Proc. Biol. Sci. 269, 475–481.
31. Eltz, T., Zimmermann, Y., Pfeiffer, C., Pech, J.R., Twele, R., Francke, W.,
Quezada-Euan, J.J.G., and Lunau, K. (2008). An olfactory shift is asso-
ciated with male perfume differentiation and species divergence in
orchid bees. Curr. Biol. 18, 1844–1848.
32. Pfennig, D.W., Wund, M.A., Snell-Rood, E.C., Cruickshank, T.,
Schlichting, C.D., and Moczek, A.P. (2010). Phenotypic plasticity’s
impacts on diversification and speciation. Trends Ecol. Evol. 25,
33. Owens, D.C. (2010). Seasonal variation in terrestrial insect subsides to
tropical streams and implications for the diet of Rivulus hartii. MSc
thesis, University of Nebraska, Lincoln, Lincoln, NE.
34. Maan, M.E., and Seehausen, O. (2011). Ecology, sexual selection and
speciation. Ecol. Lett. 14, 591–602.
Diversification via Sensory Drive