Sex and boldness explain individual differences in spatial learning in a lizard

Abstract

Understanding individual differences in cognitive performance is a major challenge to animal behaviour and cognition studies. We used the Eastern water skink (Eulamprus quoyii) to examine associations between exploration, boldness and individual variability in spatial learning, a dimension of lizard cognition with important bearing on fitness. We show that males perform better than females in a biologically relevant spatial learning task. This is the first evidence for sex differences in learning in a reptile, and we argue that it is probably owing to sex-specific selective pressures that may be widespread in lizards. Across the sexes, we found a clear association between boldness after a simulated predatory attack and the probability of learning the spatial task. In contrast to previous studies, we found a nonlinear association between boldness and learning: both 'bold' and 'shy' behavioural types were more successful learners than intermediate males. Our results do not fit with recent predictions suggesting that individual differences in learning may be linked with behavioural types via high-low-risk/reward trade-offs. We suggest the possibility that differences in spatial cognitive performance may arise in lizards as a consequence of the distinct environmental variability and complexity experienced by individuals as a result of their sex and social tactics.

Keywords: alternative reproductive strategies; behavioural syndromes; cognition; lizards; social specialization; spatial learning.

Figure 1.

Learning curves for males (white circles in a,c; n = 31) versus females (black circles in a,c; n = 31); and learner (black circles in b,d; n = 21) versus non-learner lizards (white circles in b,d; n = 41). The dashed line in (b,c) marks the probability of entering into the correct refuge by chance given the experimental set-up. Note that instances in which lizards were already encountered in the ‘safe’ refuge at the time of the simulated attack (see Material and methods) were not considered for the analysis of latencies.

Figure 2.

Parameter estimates after natural model averaging of models with a cumulative model weight of 95% (see Material and methods).

Figure 3.

The predicted probability of learning a spatial task for (a) males and (b) females as a function of the latency to return to a basking refuge after a simulated predatory attack (LATB). Predicted probabilities are based on our top-supported model (Model 8; electronic supplementary material, table S1) using standardized input variables We used our standardized input LATB variable to predict probabilities and fit a smoothed cubic spline function to the data. Dashed lines above and below fitted lines are the 95% CIs (predicted (p) ± 1.96 × s.e. of fit and smoothed with a cubic spline).