Winner and loser effects are modulated by hormonal states

Abstract

Introduction: Many animals use information acquired from recent experiences to modify their responses to new situations. Animals' decisions in contests also depend on their previous experience: after recent victories individuals tend to behave more aggressively and after defeats more submissively. Although these winner and/or loser effects have been reported for animals of different taxa, they have only recently been shown to be flexible traits, which can be influenced by extrinsic factors. In a mangrove killifish (Kryptolebias marmoratus), for instance, individuals which lost an earlier contest were more likely than others to alter contest decisions after a recent win/loss. This result suggests that individuals perceiving themselves to have worse fighting abilities are more inclined to adjust contest strategy based on new information. If this is the case, an individual's propensity to modify behaviour after a win/loss might also be modulated by intrinsic mechanisms related to its ability to fight. Stress and sex steroid hormones are often associated with an individual's contest behaviour and performance, so, in this study, we tested the hypothesis that an individual's propensity to change behaviour after wins or losses also depends on its hormonal state.

Results: Our results show that an individual's propensity to adjust contest decisions after wins and losses does depend on its hormonal state: individuals with lower levels of cortisol (F), testosterone (T) and 11-ketotestosterone (KT) are more receptive than others to the influence of recent contest experiences, especially losing experiences, and the influences last longer. Furthermore, although winning and losing experiences resulted in significant changes in behaviour, they did not bring about a significant change in the levels of F, T, KT or oestradiol (E2).

Conclusions: This study shows that an individual's receptivity to the influence of recent wins and losses is modulated by its internal state, as well as by extrinsic factors. Individuals with hormonal profiles corresponding to lower aggressiveness and a reduced likelihood of winning were more likely to alter contest decisions after a recent win/loss. The results also suggest that F, T, KT and E2 are not the primary physiological mechanisms mediating winner-loser effects in this fish.

Figure 1

Pre-contest T levels for the focal individuals assigned to different contest experience × time-decay treatments. Means (± SE) are least squares means adjusted for pre-experience T level and strain type. Within each of the time-decay treatments, none of the pair-wise differences between different experience treatments reached significance (Tukey multiple comparisons, all P > 0.05).

Figure 2

The likelihood of behaving aggressively for the focal individuals assigned to different decay-time treatments. Bars labelled with different letters differ significantly in the likelihood (P < 0.05, likelihood ratio χ² test).

Figure 3

The influence of winning/losing experience on aggressiveness for individuals with lower/higher hormone levels. The decay of the effect of experience on the probability of behaving aggressively for focal individuals with lower (< median) and higher (≥ median) levels of (A) pre-contest F, (B) pre-contest T and (C) pre-contest KT. Pearson’s χ² tests were used to determine the significance of overall experience effects for each time-decay treatment/hormone-level group. For treatments with significant overall experience effects, Fisher’s exact tests (2-tailed) were then used to test the significance of loser and winner effects separately by comparing the probabilities for the EL and the EW fish, respectively, to that for the EN fish (shown on tops of EL and EW bars, respectively). The sample size for each bar is presented on the bottom of the bar. ns P > 0.05; * P ≤ 0.05; ** P ≤ 0.01; *** P ≤ 0.001.

Figure 4

Influence of winning/losing experience on winning probability for individuals with lower/higher hormone levels. The decay of the effect of experience on the probability of winning for focal individuals with lower (< median) and higher (≥ median) levels of (A) pre-contest T and (B) pre-contest KT. This analysis was not carried out for individuals with lower and higher levels of pre-contest F as F had no significant influence on winning probability (Table  2). Pearson’s χ² tests were used to determine the significance of overall experience effects for each time-decay treatment/hormone-level group. For the treatments with significant overall experience effects, Fisher’s exact tests (2-tailed) were then used to test the significance of loser and winner effects separately by comparing the probabilities for the EL and the EW fish, respectively, to that for the EN fish (shown on tops of EL and EW bars, respectively). The sample size for each bar is presented on the bottom of the bar. ns P > 0.05; * P ≤ 0.05; ** P ≤ 0.01.

Figure 5

Pre-contest and post-contest hormone levels for focal individuals that won and that lost size-matched contests. Levels of (A) F, (B) T, (C) KT, and (D) E2 (ln transformed, mean ± SE) of the focal individuals that won (clear bars; N = 113) and lost (shaded bars; N = 142) the size-matched contests.

Figure 6

The influence of post-contest attacks on post-contest F levels. Post-contest F levels (ln transformed) for the focal individuals that won (clear squares) and lost (filled squares) to their size-matched opponents, where winners delivered different numbers of post-retreat attacks to the losers. The broken line shows the relationship between the focal individuals’ post-contest F levels and the number of attacks they delivered to their defeated opponents (for the focal individuals that won), and the solid line shows the relationship between the focal individuals’ post-contest F levels and the number of attacks they received from their victorious opponents (for the focal individuals that lost).