Do individual females differ intrinsically in their propensity to engage in extra-pair copulations?

Abstract

Background: While many studies have investigated the occurrence of extra-pair paternity in wild populations of birds, we still know surprisingly little about whether individual females differ intrinsically in their principal readiness to copulate, and to what extent this readiness is affected by male attractiveness.

Methodology/findings: To address this question I used captive zebra finches (Taeniopygia guttata) as a model system. I first measured female readiness to copulate when courted by a male for the first time in life. Second, I conducted choice-chamber experiments to assess the mating preferences of individual females prior to pair formation. I then paired females socially with a non-desired mate and once they had formed a stable pair bond, I observed the inclination of these females to engage in extra-pair copulations with various males. Females showing a high readiness to copulate when courted by a male for the first time in life were much more likely to engage in extra-pair copulations later in life than others. Male attractiveness, as measured in choice tests, was a useful predictor of whether females engaged in extra-pair copulations with these males, but, surprisingly, the attractiveness of a female's social partner had no effect on her fidelity. However, it remained unclear what made some males more attractive than others. Contrary to a widespread but rarely tested hypothesis, females did not preferentially copulate with males having a redder beak or singing at a higher rate. Rather it seemed that song rate was a confounding factor in choice-chamber experiments: song attracted the female's attention but did not increase the male's attractiveness as a copulation partner.

Conclusions/significance: Intrinsic variation in female readiness to copulate as well as variation in the attractiveness of the extra-pair male but not the social partner decided the outcome of extra-pair encounters.

Figure 1. Individual consistency in female copulatory behaviour.

(a) Mean number ±SE of extra-pair copulations performed by 63 females in experiment 3, depending on whether females had copulated or not when encountering males for the first time in life (experiment 1). (b) Mean sexual responsiveness ±SE of 63 females shown towards the males they preferred the most and the least, respectively, during choice-chamber tests. Females were more responsive towards preferred males (most vs. least preferred out of four males in a choice chamber), but only during extra-pair mating trials (experiment 3), not when females met them for the first time (experiment 1; first encounters). Responsiveness is measured on a scale from -1 (strong rejection) to +1 (strong inclination to copulate).

Figure 2. Outcome of 554 extra-pair mating trials in relation to female preferences.

The x-axis shows the relative times that females had spent with the extra-pair male vs. their partner during choice-chamber tests conducted before pair formation and is calculated as x = time spent with extra-pair male/(time spent with extra-pair male+time spent with partner). The numbers of trials with and without extra-pair copulations (EPC) are indicated.

Figure 3. Average female responsiveness during extra-pair mating trials towards 86 males.

Explanatory variables are (a) average male attractiveness (averaged across eight females) in the choice chamber, and (b) average male song rate during extra-pair trials. Each data point represents a male. Female responsiveness is measured on a scale from −1 (strong rejection) to +1 (strong inclination to copulate). Attractiveness is measured as the proportion of active time that females spent next to one of the four males in a choice chamber (expected value = 0.25). Song rate is the square-root transformed number of seconds of directed song that males produced during 5-min trials. Lines are fitted regression lines, irrespective of significance.