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The Use of Multiple Cues in Mate Choice View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Helsingin yliopiston digitaalinen arkisto Biol. Rev. (2003), 78, pp. 575–595. f Cambridge Philosophical Society 575 DOI: 10.1017/S1464793103006158 Printed in the United Kingdom 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 selection 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 reliable 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 genetic 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 ........................................................................................................................... 585 576 Ulrika Candolin VI. Evolution of multiple preferences and cues ............................................................................................ 587 (1) When do females use multiple 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 are invoked (Rosenthal & Servedio, 1999; Getty, 1999; Rice & Holland, 1999), and as resistance can be de- The possibility that mate choice is based on several scribed as cryptic preference (Kokko et al., 2003). cues, instead of on one, has received increased atten- But why should females, and sometimes males, use tion in recent years. Sexual displays are often highly multiple cues instead of one cue? Different hypotheses complex, involving many different signal components. have been put forward, some of which have received For example, in bird species males are often both empirical support, but their generality remains un- brightly ornamented and perform an elaborate song, known. Here I review the latest progress in the study of whereas many fish species combine bright colours with the use of multiple cues in mate choice and consider conspicuous courtship displays. In addition, males of the plausibility and generality of the proposed hypoth- several species offer some resource to the female, such eses. In addition, I discuss the consequences that the as a territory or a nest, which may be used as a cue in use of multiple cues may have for the process of sexual female mate choice. The picture is further complicated selection and the maintenance of genetic variation, and when the complexity of mate choice behaviour is con- the role that multiple cues may play in speciation. The sidered. Recent studies show that females may em- aim is to provide a picture of the present state of the phasise different cues in different contexts, they may field, to clarify confusing topics, to categorise the pres- vary in the attention they pay to different cues or in the ented hypotheses, and to point out areas where more number of cues that they evaluate, and that interaction studies are needed. To avoid repetition, I have omitted between cues may obscure preferences for single cues several interesting studies with similar conclusions ( Jennions & Petrie, 1997; Møller et al., 1998; Kodric- and instead given more details for a few exemplifying Brown & Nicoletto, 2001b). studies. To explain how mating preferences arise and select for sexual signals in the opposite sex, three main mech- (1) Definition of cues and signals anisms have been proposed: (1) direct fitness benefits of choice, such as improved parental care that enhances Cues are traits that are assessed during mate choice offspring survival (Hoelzer, 1989); (2) indirect genetic and influence the mating decision. They can be pheno- benefits in the form of the inheritance of genes for vi- typic traits (morphological, acoustic, olfactory, tactile ability (Zahavi, 1975) and attractiveness [the runaway or behavioural traits) or resources defended or pro- process of Fisher (1930)]; and (3) exploitation of pre- duced by the signaller, such as a nest or a territory. The existing sensory biases in the receiver (Ryan & Rand, traits can arise in another context than communication 1993a; Endler & Basolo, 1998). These mechanisms may and be maintained due to other selection pressures work either alone or in combination in the evolution of than selection for communication. For
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