Evolutionary genetics of personality in the Trinidadian guppy I: maternal and additive genetic effects across ontogeny

Abstract

Among-individual variation in behaviour is a widespread phenomenon, with several frameworks developed to explain its existence. Maternal effects, which can have significant influence over evolutionary processes, are an understudied source of behavioural variation. Maternal effects are not necessarily static, however, since their importance can change over offspring ontogeny, typically declining with age relative to additive genetic effects. Here, using a quantitative genetics approach, we test the prediction that maternal effects will influence age-specific risk-taking behaviour in Trinidadian guppies, Poecilia reticulata. Individuals were subject to a single open-field trial as juveniles and up to four repeat trials as adults, with five traits indicative of risk-taking behaviour measured in each trial. We then partitioned phenotypic variance into additive genetic (V_A) and maternal identity (V_M) components, in addition to testing brood size and maternal weight as specific sources of maternal effects. We found that V_M had significant influence over juvenile traits, with very low V_A estimates. Whereas, in adults, all traits were significantly heritable, with little support for V_M. We also found a strong influence of maternal traits on juvenile behaviours as predicted, with significant, albeit smaller, effects found in adults. Maternal weight was heritable and itself subject to maternal effects. Thus, maternal weight is a likely source of maternal genetic effects that are expected to alter response to selection on personality in this system. More generally, our study highlights that while maternal effects can be an important source of personality variation, this varies over ontogeny of offspring.

Fig. 1

Predicted relationships between Maternal weight and offspring behaviour for each OFT. Predictions are shown for juvenile (blue) and adult (red) offspring from small (n = 5), mean (n = 17.21) and large (n = 25) brood sizes. Shaded areas indicate ± 1 SE around the predicted behavioural phenotype. Maternal weight is shown in SD units, while behaviours are observed units except for Freezings (for which counts have been square root-transformed)