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

Stephen John White,Alastair James Wilson

doi:10.1038/s41437-018-0082-1

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 (VA) and maternal identity (VM) components, in addition to testing brood size and maternal weight as specific sources of maternal effects. We found that VM had significant influence over juvenile traits, with very low VA estimates. Whereas, in adults, all traits were significantly heritable, with little support for VM. 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.

Highlights

Among-individual variation in behaviour, or personality, has been well documented in a large number of animal species
In a previous study of independent data, we found that tracklength and activity capture among-individual variation that might be better interpreted as stress-responsiveness, while pattern of variation in the remaining are more aligned with expectations under a simple ‘boldness’ paradigm (White et al 2016)
Very few studies outside of domestic animal breeding have looked into grand-maternal effects, owing to the difficulty in collecting multigenerational pedigree data and none to our knowledge have looked at personality in this regard. We found that both additive genetic and maternal effects are important determinants of risk-taking behaviour traits in guppies, the former are only evident in adult fish

Summary

Introduction

Among-individual variation in behaviour, or personality, has been well documented in a large number of animal species. No longer considered as noise around the mean, there have been multiple adaptive frameworks developed to try to explain the maintenance of personality variation. There is some empirical support for each of these, it is not clear that a single explanation will apply to all cases These adaptive explanations for personality variation implicitly assume a genetic basis to the variation.

Methods

Discussion

Conclusion