Abstract

Most sex differences in phenotype are controlled by gonadal hormones, but recent work on laboratory strain mice that present discordant chromosomal and gonadal sex showed that sex chromosome complement can have a direct influence on the establishment of sex-specific behaviours, independently from gonads. In this study, we analyse the behaviour of a rodent with naturally occurring sex reversal: the African pygmy mouse Mus minutoides, in which all males are XY, while females are of three types: XX, XX* or X*Y (the asterisk represents an unknown X-linked mutation preventing masculinisation of X*Y embryos). X*Y females show typical female anatomy and, interestingly, have greater breeding performances. We investigate the link between sex chromosome complement, behaviour and reproductive success in females by analysing several behavioural features that could potentially influence their fitness: female attractiveness, aggressiveness and anxiety. Despite sex chromosome complement was not found to impact male mate preferences, it does influence some aspects of both aggressiveness and anxiety: X*Y females are more aggressive than the XX and XX*, and show lower anxiogenic response to novelty, like males. We discuss how these behavioural differences might impact the breeding performances of females, and how the sex chromosome complement could shape the differences observed.

Highlights

  • The influence of sex chromosomes on behaviour has been tested mostly on laboratory strain mice in which sex chromosome complement was genetically manipulated, but never in a species in which an unusual mode of sex determination was shaped by natural selection

  • We analyse several behavioural traits in the African pygmy mouse in order to answer two questions: does sex chromosome complement affect behaviour independently from gonadal sex in a species with naturally occurring sex reversal and could behavioural differences account for the greater reproductive output of X*Y females

  • This study addresses the influence of sex chromosome complement on female behaviour and attractiveness to males in a mammal with an unusual sex determination system (SDS): Mus minutoides

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Summary

Introduction

The influence of sex chromosomes on behaviour has been tested mostly on laboratory strain mice in which sex chromosome complement was genetically manipulated, but never in a species in which an unusual mode of sex determination was shaped by natural selection. Japanese spiny rat Tokudaia osimensis[18] and the mole vole Ellobius lutescens[19] Species with such unusual SDS are relevant to further investigate the link between sex chromosome complement and behaviour. The three types of females cannot be told apart phenotypically, they have a similar body mass and ano-genital distance, and all harbour typical ovarian structure[23], which suggest similar levels of circulating hormones Their reproductive performances differ: unexpectedly, X*Y females produce significantly more offspring than the XX and XX* females despite the meiotic issues expected in heterogametic oocytes and the loss of unviable YY embryos. We analyse several behavioural traits in the African pygmy mouse (female attractiveness, aggressiveness and anxiety in both sexes) in order to answer two questions: does sex chromosome complement affect behaviour independently from gonadal sex in a species with naturally occurring sex reversal and could behavioural differences account for the greater reproductive output of X*Y females

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