Sexual selection and the differential effect of polyandry

Abstract

In principle, widespread polyandry (female promiscuity) creates potential for sexual selection in males both before and after copulation. However, the way polyandry affects pre- and postcopulatory episodes of sexual selection remains little understood. Resolving this fundamental question has been difficult because it requires extensive information on mating behavior as well as paternity for the whole male population. Here we show that in replicate seminatural groups of red junglefowl, Gallus gallus, polyandry eroded variance in male mating success, which simultaneously weakened the overall intensity of sexual selection but increased the relative strength of postcopulatory episodes. We further illustrate the differential effect of polyandry on pre- and postcopulatory sexual selection by considering the case of male social status, a key determinant of male reproductive success in this species. In low-polyandry groups, however, status was strongly sexually selected before copulation because dominants mated with more females. In high-polyandry groups, sexual selection for status was weakened and largely restricted after copulation because dominants defended paternity by mating repeatedly with the same female. These results reveal polyandry as a potent and dynamic modulator of sexual selection episodes.

Fig. 1.

Differential effect of polyandry on male sexual selection. (A) Opportunity for pre- (I_M) and postcopulatory (I_P) sexual selection in relation to average group polyandry. I_M significantly decreased with polyandry (slope = −1.16 ± 0.26, t = −4.40, R² = 0.60, df = 11, P = 0.001) but not I_P (slope = −0.53 ± 0.39, t = −1.32, R² = 0.06, df = 10, P = 0.218). A qualitatively similar pattern was obtained using alternative measures of I_M and I_P (38): I_M (t = −4.40, R² = 0.60, df = 11, P = 0.001); I_P (t = −0.14, R² = −0.09, df = 11, P = 0.892). (B) Multivariate gradients of pre- (β_M) and postcopulatory (β_P) sexual selection in relation to average group polyandry. β_M significantly decreased with polyandry (slope = −1.32 ± 0.56, t = −2.42, R² = 0.31, df = 10, P = 0.036), but this trend was much weaker for β_P (slope = −0.66 ± 0.35, t = −1.90, R² = −0.25, df = 7, P = 0.099). A qualitatively similar pattern was obtained using univariate measures of β_M and β_P based on ref. : β_M (t = −6.30, R² = 0.78, df = 10, P < 0.001); β_P (t = −3.16, R² = 0.45, df = 10, P = 0.010). (C) The opportunity for total sexual selection (I_T) significantly decreased with group polyandry (−1.35 ± 0.26, t = −5.19, R² = 0.68, df = 11, P < 0.001). (D) In more polyandrous groups, the proportion of the variance in total male reproductive success explained by male mating success tended to decline (solid line, t = −2.06, df = 11, P = 0.064), and simultaneously the proportion of male reproductive success explained by paternity share increased (shaded line, t = 1.50, df = 10, P = 0.019). Data points represent individual replicate groups.

Fig. 2.

Sexual selection on male social status. (A) Gradients of pre- (β_SM) and postcopulatory (β_SP) sexual selection on social status in relation to average group polyandry. β_SM decreased with polyandry (slope = −0.55 ± 0.14, t = −4.05, R² = 0.56, df = 11, P = 0.002), but this trend was nonsignificant for β_SP (slope = −0.48 ± 0.26, t = −1.88, R² = 0.19, df = 10, P = 0.090). (B) The total sexual selection gradient on social status (β_ST) decreased with polyandry (−0.64 ± 0.18, t = −3.64, R² = 0.50, df = 11, P = 0.004). Data points represent individual replicate groups. (C) The rate of male remating with the same female was strongly status dependent (F = 11.11, df = 2, P < 0.001). (D) Postcopulatory sexual selection gradient on remating with the same female(s) increased significantly with the postcopulatory sexual selection gradient on social status [i.e., β_SP (slope = 0.88 ± 0.11, t = 7.90, R² = 0.85, df = 10, P < 0.001)]. Data points represent individual replicate groups.