We have developed a powerful experimental system for testing genetic models of sexual selection using the yeast S. cerevisiae. We have used this system to demonstrate, for the first time, the central process underlying sexual selection theory: the spread of a strong signalling allele through a population of weak signallers. We found that an allele encoding a strong sexual signal rapidly increased in frequency under high sexual selection but not under low sexual selection. As we were able to demonstrate the absence of significant viability or fecundity selection on variation at the signalling locus, the increase in frequency of the strong signalling allele is attributable solely to mate choice.
It is noteworthy that evolution did not proceed identically in all six replicates of each treatment. Under high sexual selection, the strong signalling allele initially increased in frequency in all replicates, but in just one replicate it then fell rapidly. Under low sexual selection, the frequency of the strong signalling allele remained close to the initial frequency throughout the experiment, except in one replicate population where it rose slowly. This replicate-to-replicate variation is caused by the stochastic factors that can affect evolution. The rapid decline in frequency of the strong signalling allele observed in replicate high E was probably caused by selection of a novel beneficial mutation, probably linked to the weak signalling allele. If the fitness effects of this mutation were large enough to overwhelm the sexually selected advantage associated with the strong signalling allele, it would drive the spread of the weak signalling allele through the population, producing the observed dynamics. We found no difference in vegetative haploid fitness between a sample of weak and strong signallers from high E, suggesting that the mutation affected some other component of fitness (data not shown). In the laboratory, just as in nature, evolution does not necessarily follow a predictable or repeatable trajectory.
So great are the difficulties associated with the experimental evolution of sexual displays, that we are aware of only one previous study to attempt it. In an ambitious experiment, Snook et al. (2005)
followed changes in the components of the courtship song of male Drosophila pseudoobscura
at different intensities of sexual selection. One song component known to influence male mating success, interpulse interval, showed significant changes from baseline in both the high and low sexual selection treatments. However, interpretation of these results is hampered by an incomplete understanding of the genetic basis of courtship song and preference for it, a paucity of genetic tools and the difficulties in controlling other evolutionary forces at work during the experiment.
In this experiment, we have tested the simplest possible sexual selection scenario. We introduced variation in the strength of the sexual signal (in the form of just two alleles), but not in mate preference. Our measurements show that mate preference did not change during the course of the experiment. This could be simply because no spontaneous mutations affecting the strength of mate preference arose. Alternatively, any such mutations were not selected because they conferred too small an advantage for us to detect, or because any advantage was countered by the high cost of choice (see Pagel 1993
Why do yeasts prefer to mate with stronger signallers? The preference for stronger pheromone sources might simply be a mechanism of locating the nearest mating partner, a system termed passive attraction (Pagel 1993
). An alternative is that stronger signallers are preferred because they provide some benefit, direct or indirect, to individuals that choose them. If the pheromone is costly to produce, it may act as a reliable indicator of the producer's genetic or phenotypic quality or condition, because high-quality individuals can afford a stronger signal (Pagel 1993
). The strong and weak signallers had equal fitness in our experimental conditions, so there was no detectable cost of stronger signalling, but natural conditions may be completely different. Work to test the two explanations for the existence of the preference for stronger signallers is ongoing (C. Smith, D. W. Rogers, S. J. Tazzyman, A. Pomiankowski & D. Greig 2008, unpublished data), but for the purposes of the experiment presented here, it does not matter why the preference exists, only that it does.
Our system can be used to test specific models of sexual selection. Introducing variance in mate choice in our experimental system should be relatively straightforward. The α-pheromone receptor, STE2
, is extremely well characterized, and mutations that alter specific amino acids can change its sensitivity and specificity to α-pheromone (Sen et al. 1997
). By adding a mutant STE2
allele that confers either stronger or weaker preference for strong signallers to the design used herein, it would be possible to test simple two-locus two-allele models of the Fisher process (e.g. Kirkpatrick 1982
). The cost of this preference could be manipulated by tightly linking the stronger preference allele to a marker conferring reduced viability. Any number of simple variations are possible, allowing the empirical testing of most existing models of sexual selection in haploids.
The study of sexual selection using traditional model organisms has perhaps been most limited by the extraordinary difficulty of measuring fitness. This is particularly true when addressing the issue of the costs of sexual signals and preferences for them. Consequently, although being able to measure and manipulate costs lies at the heart of discriminating between models of sexual selection and testing the conditions under which they work, there is very little direct empirical evidence that sexual signals and preferences impose actual costs on fitness (Kotiaho 2001
). Measurement of total fitness in microbes by direct competition between genotypes is simple and powerful (Lenski et al. 1991
). Because yeast can reproduce both sexually and asexually, sexual and non-sexual elements of fitness can be isolated. Yeast asexual fitness is very similar to Maynard Smith's (1987)
concept of viability or ‘all components of fitness other than mating success’, which has subsequently been termed ‘condition’. The ability to accurately measure condition provides a powerful mechanism for testing genetic models related to the handicap principle and the exciting possibility of an experimental resolution to the lek paradox (Pomiankowski & Møller 1995
; Rowe & Houle 1996
The most compelling advantages of the use of microbes for experimental evolution come from their short generation time and large population sizes, which allows selection to act on spontaneous mutations, rather than simply sorting pre-existing alleles (e.g. Lenski & Travisano 1994
). Even in the relatively short-duration experiment described here, spontaneous mutation appeared to cause replicate-to-replicate variation, and any mutations affecting signal or preference strength will be subject to selection in our experimental system. Changes in attractiveness and mate choice can be simply monitored using tester strains and the underlying genetic basis for sexual selection can be elucidated using the powerful genomic methods available for yeast (Segrè et al. 2006
). Observing the real-time evolution of novel sexually selected traits, and preferences for them, is the ultimate test for sexual selection theory.