Economics of mate choice at leks: do female waxmoths pay costs for indirect genetic benefits?

Behavioral Ecology doi:10.1093/beheco/arq028 Advance Access publication 22 March 2010 Economics of mate choice at leks: do female waxmoths pay costs for indirect genetic benefits? Sylvain Alem and Michael D. Greenfield Institut de recherche sur la biologie de l’insecte, Centre National de la Recherche Scientifique Unité Mixte de Recherche 6035, Université Francxois Rabelais de Tours, Parc de Grandmont, 37200 Tours, France Sexual selection theory predicts low costs of choice when females choose among males for genetic (indirect) benefits, as occurs at leks. However, few empirical studies have investigated the actual costs incurred during the process of pair formation, and we generally do not know whether and to what extent females incur energetic expenditure, exposure to predation, or simple allocation of time by virtue of their choosiness. Do females that choose mates at larger aggregations of males necessarily pay these costs? Moreover, what costs are they willing to pay to obtain potential benefits? We addressed these questions in an acoustic pyralid moth, Achroia grisella, in which males aggregate and attract females with an advertisement song. Female choice is based on acoustic characters of displaying males, and only genetic benefits appear to be available. We measured the movement and time that females spent in mate sampling when presented with varying numbers of males in a laboratory arena. We found that female choice for specific males was retained as male number increased, although their sampling effort increased: female trajectories lengthened and reversed direction more often. The repeatability of female choice at larger leks and the basic precision of female phonotaxis indicated that the lengthened trajectories reflected sampling and choosiness as opposed to confusion. We propose that the cost of such choosiness in natural populations may be an increased exposure to predation and that females pay this cost because of the opportunity to mate with a specific male with certain song characteristics. Key words: acoustic communication, mating signals, orientation, pair formation, sexual selection. [Behav Ecol 21:615–625 (2010)] he costs and benefits that accrue to individuals engaged in courtship and mating represent an integral part of the sexual selection process (Andersson 1994). Although these economic factors can be expected to operate in the activities of both sexes, they were first considered and have been more thoroughly studied in the male. Following this scheme, modeling of the indirect (genetic) benefits mechanism of mate choice has generally considered that as a male’s signaling increases in extravagance, his elevated costs incurred in energy expenditure or exposure to the risk of predation are offset by increased attractiveness to females (Kotiaho 2001; Stuart-Fox et al. 2003; Danchin and Cézilly 2005; e.g., Reinhold et al. 1998). Analyses of female activities, however, focused initially on the various direct and indirect benefits that might be received by virtue of mating with a given male or with a given number of males, while ignoring potential costs or assuming that they are negligible. More recently, though, various modelers have proposed that females might sustain certain costs of choice when they receive direct benefits (Kirkpatrick 1985, 1996; Heywood 1989; Grafen 1990; Kirkpatrick and Ryan 1991; Kirkpatrick and Barton 1997; Cameron et al. 2003), and even in the case of indirect benefits provided that the costs are small (Iwasa et al. 1991; Pomiankowski et al.1991; Houle and Kondrashov 2002; Kokko et al. 2006). Similarly, a parallel series of empirical studies have begun to address the costs that females actually encounter in the process of pair formation (Parker 1978; Jennions and Petrie 1997; for studies T Address correspondence to S. Alem. E-mail: sylvain.alem@etu .univ-tours.fr. Received 14 September 2009; revised 9 February 2010; accepted 12 February 2010.
The Author 2010. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: that have measured such costs, see Wickman and Jansson 1997; Byers et al. 2005; Booksmythe et al. 2008). Nonetheless, basic questions remain because we still have relatively little information on which aspects of the entire pair-forming process are costly for a female and whether choosy females might receive certain added benefits that offset those costs. Empirical studies are particularly critical in species with no evidence for direct benefits, as theory predicts that mate choice under these circumstances should be relatively cost free, but some observations suggest otherwise. It has generally been recognized that aggregations of lekking males are ideal settings for studying female choice for indirect benefits (Höglund and Alatalo 1995). These same aggregations may also serve as most appropriate settings for investigating the costs associated with pair formation via female choice. We consider that the activity of choosing to mate with a particular male displaying at a lek may be partitioned into 2 processes, mate preference and ‘‘choosiness’’ (see Jennions and Petrie 1997; Kokko et al. 2006). We retain the distinction between these 2 processes because each may function independently within the context of pair formation. For example, 2 females may have the same ‘‘preference functions’’ (see Ritchie 1996) along the male phenotypic gradient, but one may have a high level of choosiness wherein she spends considerable time and effort in evaluating available males before pairing, whereas another being less choosy might pair more quickly, and possibly with a male displaying inferior courtship. In other words, the second makes a more cursory examination and in effect either adjusts her acceptance threshold to a lower value or has a higher probability of mating with an inferior male due to limited sampling (see Janetos 1980). We assume that the costs of female choice are largely subsumed within choosiness rather than preference unless there are costs associated with mating with specific categories of Behavioral Ecology 616 males (e.g., Head et al. 2005). In the context of leks, a female which visits or otherwise perceives a fixed proportion of displaying males and effects a given evaluation of each male will pay a greater cost when encountering leks of increasing male number (see Janetos 1980). Alternatively, she could avoid these elevated costs by visiting or perceiving a smaller proportion or reducing the evaluation of each male when encountering larger leks (Kotiaho and Puurtinen 2007). Thus, we might experimentally manipulate lek size, effectively changing the cost of choosiness, and then examine the effect on female sampling behavior and mate choice. Because costs associated with mate sampling are potential constraints on the optimal mate choice (Gibson and Bachmann 1992), we can observe whether females (...truncated)