Abstract

There is a growing awareness of the influence of mitochondrial genetic variation on life-history phenotypes, particularly via epistatic interactions with nuclear genes. Owing to their direct effect on traits such as metabolic and growth rates, mitonuclear interactions may also affect variation in behavioural types or personalities (i.e. behavioural variation that is consistent within individuals, but differs among individuals). However, this possibility is largely unexplored. We used mitonuclear introgression lines, where three mitochondrial genomes were introgressed into three nuclear genetic backgrounds, to disentangle genetic effects on behavioural variation in a seed beetle. We found within-individual consistency in a suite of activity-related behaviours, providing evidence for variation in personality. Composite measures of overall activity of individuals in behavioural assays were influenced by both nuclear genetic variation and by the interaction between nuclear and mitochondrial genomes. More importantly, the degree of expression of behavioural and life-history phenotypes was correlated and mitonuclear genetic variation affected expression of these concerted phenotypes. These results show that mitonuclear genetic variation affects both behavioural and life-history traits, and they provide novel insights into the maintenance of genetic variation in behaviour and personality.

Highlights

  • A fundamental challenge in biology is to understand phenotypic and genetic variation, and the links between them [1]

  • We demonstrate that mitonuclear interactions affect personality, and that behaviour and life-history traits are correlated across genotypes, as predicted by pace-of-life syndrome (POLS)

  • By using experimentally constructed mitonuclear introgression lines, we show that mitonuclear interactions affect phenotypes along an axis of covariation between life-history traits and behaviour in seed beetles

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Summary

Introduction

A fundamental challenge in biology is to understand phenotypic and genetic variation, and the links between them [1]. The genetic architecture of metabolic rate is not well understood [26 –28] and the maintenance of variation in POLS remains unclear Those studies that have demonstrated a relationship between personality, metabolic rate and life-history traits suggest that genes with major pleiotropic effects may be involved [3,20]. We employ the seed beetle Callosobruchus maculatus In this system, previous work has demonstrated genetic covariance between suits of life-history traits, including lifespan, body size and metabolic rate To investigate variation in behavioural responses, single beetles (n 1⁄4 932) were observed in a novel arena test for 10 min in the afternoon (13.00– 18.00 local time) of the day after they had emerged (i.e. when 1 day old). This model included mtDNA, nDNA, sex and their two-way interactions as fixed-effect factors and generation as a random-effect factor

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