The costs of female choice in a lekking bird

We investigated the costs of active female choice in sage grouse, Centrocercus urophasianus, a lekking species in which females make repeated, lengthy visits to leks to assess males before mating. Several potential costs were measured by monitoring changes in hens’ ranging behavior, time budgets, and encounter rates with predators when they visited leks. Two costs were identified: hens moved farther per day and encountered golden eagles, Aquila chrysaetos, more frequently when visiting leks. However, extra travel due to visiting leks increased predicted daily energetic expenditure by only about 1%, and the risk of predation by golden eagles over a typical series of lek visits (compared to a single short visit for mating) was estimated to reduce annual survival by < 0.1%. Two other potential costs were not supported: visiting leks did not depress foraging time or conflict with nest defense. These results indicate that any costs of mate choice are slight and imply that even very small benefits could be sufficient to maintain female choice. We present calculations which suggest that increased offspring viability due to choosing fitter males could balance predation costs even if the heritability of fitness is low and if females identify fitter males with only moderate accuracy. Despite recent emphasis on the direct benefits of mate choice, we conclude that either indirect or direct benefits could provide a plausible solution to the lek paradox. The prevalence of active mate choice in species with nonresource-based systems, such as leks, is often regarded as an evolutionary paradox. Active sampling of prospective mates appears to be a costly process. Mate choice is therefore unlikely to be maintained by selection unless it provides compensating benefits. One view is that these benefits are obtained indirectly through increased sexual attractiveness of sons, the Fisher process, or increased viability of offspring of both sexes, the good genes hypothesis (Maynard Smith, 1991). These hypotheses have the merit of generality, but they face the difficulty that indirect genetic benefits are likely to be small. Therefore, such mechanisms could maintain choice only if sampling costs were correspondingly slight. Another view, emphasized in some recent reviews (Kirkpatrick and Ryan, 1991; Reynolds and Gross, 1990), is that mate choice G I B S O N A N D B A C H M A N , B E H A V I O R A L E C O L O G Y 3 (1 9 9 2 ) 2 provides direct benefits deriving, for example, from reduced social interference (Trail, 1985), disease transmission (Borgia and Collis, 1990), or increased fertility (Avery, 1984). Such benefits might be large and thus maintain choice in the face of substantial sampling costs. However, the existence of these direct benefits is an open question. Measurements of the cost of mate choice offer a possible resolution of this issue. Because indirect genetic benefits are likely to be small, a demonstration that females who choose males incur large costs would favor the direct selection hypothesis, whereas sufficiently small costs would be consistent with either indirect or direct benefits. It has also been suggested that even small costs would prevent the maintenance of choice by the Fisher process (Kirkpatrick, 1987; Lande, 1981; Pomiankowski, 1988). However, more recent work has shown that the Fisher process is compatible with costly choice provided that there is a mutational bias on the attractive male trait (Pomiankowski et al., 1991). To date there have been few empirical studies of the costs of mate choice (Alatalo et al., 1988; Engelhard et al., 1988; Slagsvold et al., 1988) and, to our knowledge, none in lekking species. In this paper, we attempt to fill this gap by analyzing the costs of female choice in a lekking bird, the sage grouse, Centrocercus urophasianus. Two observations suggest that female choice could be costly in lekking species. First, females often visit leks repeatedly and spend time with several different males before mating (Gibson and Bradbury, 1986; Pruett-Jones and Pruett-Jones, 1990; Trail and Adams, 1989). Such behavior would be costly if movement to leks increases energetic expenditure on travel, exposes females to increased predation risks, or takes time from other activities beyond that necessary for mating. Second, in some species females adopt secondary tactics of mate assessment, such as fidelity to former mating sites (Gibson et al., 1991; Lill, 1974) or copying the choices of others (Gibson et al., 1991; Höglund et al., 1990), which could reduce the time spent on mate assessment and thus reduce any associated costs. However, these observations alone do not justify the conclusion that choice is costly, because it is possible that visiting leks has little effect on risk of predation or on daily time and energy budgets. It is also possible that secondary tactics of mate assessment are driven by benefits other than cost reduction. Direct measurements of costs are needed to resolve these issues. Most female sage grouse visit leks on 2 or 3 mornings each spring and mate once on the last visit, obtaining enough sperm to fertilize a clutch of 6–10 eggs. Each visit lasts from a few minutes to more than 2 h and typically includes visits to the territories of several males. Because mating can be completed in a single brief visit, both repeated visits to leks and the time invested in sampling per visit are clearly in excess of what is needed to mate. There are at least three ways in which this additional sampling might be costly. First, visits to a lek could increase energetic expenditure on travel above typical daily levels. Large excess expenditure might represent an important cost for hens whose energetic requirements are already elevated by the need to accumulate reserves for laying and incubation. Second, time at leks might expose hens to higher risks of predation, particularly from golden eagles (Aquila chrysaetos), which regularly attack leks (Bradbury et al., 1989a; Hartzler, 1972; Lumsden, 1968; Scott, 1942; Wiley, 1973). Finally, time spent at leks might reduce opportunities to forage or defend nesting territories (Gibson et al., 1991). In this paper we assess the likelihood and magnitude of each of these hypothesized costs by measuring how visiting leks affects female ranging behavior, encounter rates with G I B S O N A N D B A C H M A N , B E H A V I O R A L E C O L O G Y 3 (1 9 9 2 ) 3 golden eagles, time budgets, and proximity to nests. We then consider whether measured costs would be sufficient to override indirect sexual selection on female choice.