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The use of multiple cues in mate choice
Candolin, Ulrika
Cambridge University Press
2003-11
Biological Reviews 78 (4): 575-595
http://hdl.handle.net/1975/138
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The use of multiple cues in mate choice
ULRIKA CANDOLIN
Department of Ecology and Systematics, P.O. Box 65, University of Helsinki, Helsinki FIN-00014, Finland
(e-mail: ulrika.candolin@helsinki.fi)
(Received 28 February 2002 ; revised 12 December 2002 ; accepted 18 December 2002)
ABSTRACT
An increasing number of studies find females to base their mate choice on several cues. Why this occurs is debated
and many different hypotheses have been proposed. Here I review the hypotheses and the evidence in favour of
them. At the same time I provide a new categorisation based on the adaptiveness of the preferences and the
information content of the cues. A few comparative and empirical studies suggest that most multiple cues are
Fisherian attractiveness cues or uninformative cues that occur alongside a viability indicator and facilitate de-
tection, improve signal reception, or are remnants from past select ion pressures. However, much evidence exists
for multiple cues providing additional information and serving as multiple messages that either indicate general
mate quality or enable females that differ in mate preferences to choose the most suitable male. Less evidence
exists for multiple cues serving as back-up signals. The importance of receiver psychology, multiple sensory
environments and signal interaction in the evolution of multiple cues and preferences has received surprisingly
little attention but may be of crucial importance. Similarly, sexual conflict has been proposed to result in mal-
adaptive preferences for manipulative cues, and in neutral preferences for threshold cues, but no reliab le evidence
exists so far. An important factor in the evolution of multiple preferences is the cost of using additional cues. Most
theoretical work assumes that the cost of choice increases with the number of cues used, which restricts the
conditions under which preferences for multiple cues are expected to evolve. I suggest that in contrast to this
expectation, the use of multiple cues can reduce mate choice costs by decreasing the number of mates inspected
more closely or the time and energy spent inspecting a set of mates. This may be one explanation for why multiple
cues are more common than usually expected. Finally I discuss the consequences that the use of multiple cues
may have for the process of sexual selection, the maintenance of genet ic variation, and speciation.
Key words: amplifiers, mate choice costs, mate preferences, multicomponent signals, multiple ornaments, receiver
psychology, sexual selection, signal interaction, unreliable signals, viability indicators.
CONTENTS
I. Introduction ............................................ ......... ......... ...... .......... ......... ......... ...... ......... .......... ......... ...... ......... 576
(1) Definition of cues and signals ................................................... ......... ......... ...... .......... ......... ......... ...... 576
II. Why use multiple cues ? .................. ......... ......... ...... ......... .......... ......... ...... ......... ......... .......... ...... ......... ...... 577
(1) Multiple messages .............................. ......... ......... ...... .......... ......... ......... ...... ......... .......... ......... ...... ...... 577
(a) Estimation of overall quality ......................................... ...... ......... ......... ......... ....... ......... ......... ...... 577
(b) Variation in mate preferences ...................................... ......... ......... ...... ......... .......... ......... ...... ...... 579
(2) Back-up signals .......................... ......... ......... ...... ......... .......... ......... ...... ......... ......... .......... ...... ......... ...... 580
(3) Species recognition ............................. ...... ......... ......... .......... ...... ......... ......... ......... ....... ......... ......... ...... 581
(4) Unreliable and Fisherian cues ............................................... ......... ...... ......... .......... ......... ...... ......... ... 581
(5) Receiver psychology ................. ......... ......... ...... ......... .......... ......... ...... ......... ......... .......... ...... ......... ...... 582
(6) Multiple sensory environments ...................................................... ......... ...... .......... ......... ......... ...... ... 582
(7) Intersexual conflict and antagonistic coevolution ............ ...... ......... ......... ......... ....... ......... ......... ...... 583
III. Theoretical studies on the evolution of multiple cues ....................... ......... ...... .......... ......... ......... ...... ... 583
IV. What do multiple cues indicate ? ....................................................... ......... ......... ...... .......... ......... ......... ... 584
V. Interaction between cues ......................... ......... ......... ......... ....... ......... ......... ......... ...... .......... ......... ......... ... 585
Biol. Rev. (2003), 78, pp. 575–595. f Cambridge Philosophical Society 575
DOI: 10.1017/S1464793103006158 Printed in the United Kingdom
VI. Evolution of multiple preferences and cues ....................................... ......... ......... ...... .......... ......... ......... . 587
(1) When do females use mult iple cues ? .................................................. ......... ......... ....... ......... ......... .... 587
(2) Increased or decreased costs of choice ? .................................... ......... ......... ......... ....... ......... ......... .... 587
VII. Consequences of the use of multiple cues ................................. ......... ......... ......... ...... .......... ......... ......... . 588
(1) Strength of sexual selection and the maintenance of variation ..................................... ......... ....... 588
(2) Speciation and the evolution of alternative signalling tactics ..................................... ...... ......... .... 589
VIII. Conclusions and directions for future research .............................. ......... ......... ...... .......... ......... ......... .... 589
IX. Acknowledgements .................................. ......... ...... ......... .......... ......... ...... ......... ......... .......... ...... ......... ....... 590
X. References .................................................... ......... ...... ......... .......... ......... ...... ......... ......... .......... ......... ...... .... 590
I. INTRODUCTION
The possibility that mate choice is based on several
cues, instead of on one, has received increased atten-
tion in recent years. Sexual displays are often highly
complex, involving many different signal components.
For example, in bird species males are often both
brightly ornamented and perform an elaborate song,
whereas many fish species combine bright colours with
conspicuous courtship displays. In addition, males of
several species offer some resource to the female, such
as a territory or a nest, which may be used as a cue in
female mate choice. The picture is further complicated
when the complexity of mate choice behaviour is con-
sidered. Recent studies show that females may em-
phasise different cues in different contexts, they may
vary in the attention they pay to different cues or in the
number of cues that they evaluate, and that interaction
between cues may obscure preferences for single cues
( Jennions & Petrie, 1997; Møller et al., 1998; Kodric-
Brown & Nicoletto, 2001b).
To explain how mating preferences arise and select
for sexual signals in the opposite sex, three main mech-
anisms have been proposed: (1) direct fitness benefits of
choice, such as improved parental care that enhances
offspring survival (Hoelzer, 1989); (2) indirect genetic
benefits in the form of the inheritance of genes for vi-
ability (Zahavi, 1975) and attractiveness [the runaway
process of Fisher (1930)]; and (3) exploitation of pre-
existing sensory biases in the receiver (Ryan & Rand,
1993a; Endler & Basolo, 1998). These mechanisms may
work either alone or in combination in the evolution of
sexual signals. Preferences for multiple signals may arise
through a single preference selecting for multiple sig-
nals or, alternatively, through multiple preferences each
coevolving with a signal (Brooks & Couldridge, 1999).
Recently, a new model was proposed by Holland &
Rice(1998),theantagonisticchase-awayselection,which
proposes that resistance instead of preference can sel-
ect for exaggerated display traits and generate mating
biases. The model is, however, an extension of earlier
models, as both fitness benefits and sensory exploitation
are invoked (Rosenthal & Servedio, 1999; Getty, 1999;
Rice & Holland, 1999), and as resistance can be de-
scribed as cryptic preference (Kokko et al., 2003).
But why should females, and sometimes males, use
multiple cues instead of one cue? Different hypotheses
have been put forward, some of which have received
empirical support, but their generality remains un-
known. Here I review the latest progress in the study of
the use of multiple cues in mate choice and consider
the plausibility and generality of the proposed hypoth-
eses. In addition, I discuss the consequences that the
use of multiple cues may have for the process of sexual
selection and the maintenance of genetic variation, and
the role that multiple cues may play in speciation. The
aim is to provide a picture of the present state of the
field, to clarify confusing topics, to categorise the pres-
ented hypotheses, and to point out areas where more
studies are needed. To avoid repetition, I have omitted
several interesting studies with similar conclusions
and instead given more details for a few exemplifying
studies.
(1) Definition of cues and signals
Cues are traits that are assessed during mate choice
and influence the mating decision. They can be pheno-
typic traits (morphological, acoustic, olfactory, tactile
or behavioural traits) or resources defended or pro-
duced by the signaller, such as a nest or a territory. The
traits can arise in another context than communication
and be maintained due to other selection pressures
than selection for communication. For example, body
constitution and running speed may be under survival
selection but simultaneously be used as indicators of
fitness. However, often the traits have been modified
for communication, or serve a function in communi-
cation only, such as colourful ornaments or courtship
behaviours that are detrimental to survival but increase
attractiveness to the opposite sex.
Cues that have at least partly been modified by
natural selection for the purpose of communication are
termed signals and, thus, form a special type of cue.
576 Ulrika Candolin
Signals can consist of one cue or, alternatively, of sev-
eral cues (components) that are evaluated together as
one signal, such as displays combining visual and acous-
tic components. Signals that are made up of several
components are called multicomponent signals, or
multimodal signals if the components occur in several
sensory modalities. Signals are under different selective
pressures to other traits, due to the dual interaction
between signallers and receivers. Properties of the re-
ceiver exert selective pressures on signal design by
favouring signallers who elicit favourable responses. At
the same time signal design exerts reciprocal selective
pressures on receiver behaviour by favouring receivers
who can accurately deduce the nature and intentions
of signallers ( Johnstone, 1997).
II. WHY USE MULTIPLE CUES?
The use of multiple cues in mate choice may: (1) be
adaptive and increase fitness by reducing mate choice
errors or costs of choice; (2) have no influence on fit-
ness but include preferences that are remnants from
past selection or have arisen in another context and are
exploited by the signaller; or (3) be maladaptive and
decrease fitness, as the signaller manipulates mating
resistance of the receiver by taking advantage of pre-
existing sensory biases (Table 1). Fitness benefits can be
gained either directly, through effects on fecundity,
survival and future reproductive opportunities, or in-
directly through the inheritance of genes that increase
offspring viability or attractiveness.
Cues can be further grouped into two groups de-
pending on their information content: (a) informative
and (b) uninformative cues (Table 1). Informative cues
provide information about mate quality, the species
or the resources offered. This can reduce mate choice
errors or the cost at which the information is gained by
reducing time or energy expenditure or mortality risk.
Uninformative cues are unreliable indicators of mate
quality but can belong to any of the three groups de-
tailed above: they can increase receiver fitness by fa-
cilitating detection or signal assessment, have no effect
on fitness, or decrease receiver fitness if the signaller
manipulates mating resistance of the receiver. Cues
whose use are harmful to the receiver do, in fact, in-
dicate a harmful mate, but the receiver is not able to
receive this information as the cues exploit pre-existing
sensory biases. The cues are therefore uninformative of
mate quality to the receiver.
Hypotheses relating to the group of adaptive pre-
ferences for informative cues include the multiple mess-
ages hypothesis, the backup hypothesis (or redundant
signal hypothesis) (Møller & Pomiankowski, 1993;
Johnstone, 1997), the species recognition hypothesis
(Pfennig, 1998), and the hypothesis of Fisherian cues
that reflect indirect genetic benefits (Pomiankowski &
Iwasa, 1993). Hypotheses relating to the group of
adaptive preferences for uninformative cues, include
the receiver psychology hypothesis (Rowe, 1999) and
the hypothesis of unreliable cues that exploit pre-
existing sensory biases of the receiver but still are
beneficial to the receiver (Ryan & Rand, 1993a). The
hypotheses of multiple sensory environments can
belong to either group, as some cues may facilitate
detection or signal transmission whereas others reflect
mate quality.
Non-adaptive preferences for uninformative cues
that have no effect on receiver fitness can be explained
by the hypotheses of unreliable and threshold cues
(Møller & Pomiankowski, 1993; Holland & Rice,
1998). Maladaptive preferences that have a detrimen-
tal effect on receiver fitness can be explained by inter-
sexual conflict (Holland & Rice, 1998). In the following
sections I will review the different hypotheses and evi-
dence for and against them to give an overview of the
current state of the field.
(1) Multiple messages
According to the multiple messages hypothesis, differ-
ent signals give information about different mate qual-
ities (Møller & Pomiankowski, 1993; Johnstone, 1997).
The signals may then be evaluated together to indicate
the general quality of the mate, or alternatively, differ-
ent receivers may pay attention to different signals and,
thus, to different aspects of mate quality, according to
their own condition or genetic make-up (Wedekind,
1992).
(a) Estimation of overall quality
To gain information on the overall quality of a poten-
tial mate an individual may pay attention to several
traits that reflect different qualities. In support of this,
several studies have found different ornaments to re-
flect different aspects of mate quality. For example,
ornamental colours that are made up of different
pigments often reflect different qualities; carotenoid
pigments usually reflect physical condition (Hill &
Montgomerie, 1994; Linville & Breitwisch, 1997;
Olson & Owens, 1998; McGraw & Hill, 2000), es-
pecially disease condition (reviewed by Møller et al.,
2000), whereas melanin-based colours mostly reflect
social status (reviewed in Senar, 1999; but see Fitze &
Richner, 2002). An example of this is the ornamen-
tation of the American goldfinch (Carduelis tristis) where
The use of multiple cues in mate choice 577
Table 1. Categorisation of the hypotheses put forward to explain the use of multiple cues in mate choice
Adaptiveness of
preferences Form of cues Proposed hypotheses Purpose of different cues
Proximate benefit
gained by the receiver
Adaptive, increase
fitness through less
errors or lower costs
of mate choice
Informative cues Multiple messages Indicator traits that reflect
different qualities
– Sensitive to different
environmental or
– Evaluated together the traits
reflect overall quality
intrinsic factors – Individuals can emphasise the cue
– Develop at different times that is most relevant for them
Back-up cues Indicator traits that reflect
the same quality
Increased accuracy of assessment
Species recognition Different cues for species
recognition and mate assessment
Avoidance of costly matings with
other species
Fisherian cues Indicate heritable attractiveness Offspring inherit the attractive trait
Uninformative cues Unreliable cues Exploitation of sensory
biases in the receiver
Facilitates detection of the signaller
Receiver psychology Additional cues enhance
detectability, discriminability
or memorability of the signal
Facilitates mate assessment
Informative or
uninformative cues
Multiple sensory
environments
Indicator or unreliable
cues that are used :
– At different distances
– At different stages of the
courtship ritual
– In different signal
transmission habitats
Facilitates mate assessment or
increases the amount of
information gained
Non-adaptive, no
effect on fitness
Uninformative cues Unreliable cues,
threshold cues
– Exploitation of sensory
biases in the receiver
– Remnants from past selection
Maladaptive,
reduce fitness
Uninformative,
manipulating cues
Intersexual conflict Manipulation of mating
resistance by exploitation
of pre-existing sensory biases
578 Ulrika Candolin
