Abstract

Female intrasexual competition can be intense in cooperatively breeding species, with some dominant breeders (matriarchs) limiting reproduction in subordinates via aggression, eviction or infanticide. In males, such tendencies bidirectionally link to testosterone, but in females, there has been little systematic investigation of androgen-mediated behaviour within and across generations. In 22 clans of wild meerkats (Suricata suricatta), we show that matriarchs 1) express peak androgen concentrations during late gestation, 2) when displaying peak feeding competition, dominance behaviour, and evictions, and 3) relative to subordinates, produce offspring that are more aggressive in early development. Late-gestation antiandrogen treatment of matriarchs 4) specifically reduces dominance behaviour, is associated with infrequent evictions, decreases social centrality within the clan, 5) increases aggression in cohabiting subordinate dams, and 6) reduces offspring aggression. These effects implicate androgen-mediated aggression in the operation of female sexual selection, and intergenerational transmission of masculinised phenotypes in the evolution of meerkat cooperative breeding.

Highlights

  • Female intrasexual competition can be intense in cooperatively breeding species, with some dominant breeders limiting reproduction in subordinates via aggression, eviction or infanticide

  • Consistent with prediction 1a, androgen concentrations in dominant females during and post pregnancy exceeded those in subordinate females (generalised linear mixed model (GLMM): androstenedione χ21,31 = 50.49, P < 0.001; testosterone χ21,32 = 6.39, P = 0.011; linear mixed model (LMM): faecal androgen metabolites χ21,7 = 7.60, P = 0.006; Fig. 1a–c and Supplementary Table 1)

  • Unconventionally focused on wild females, our androgenmediated behavioural findings adhere to traditional theory on sexual differentiation[29], whilst recognising the added potential for genetic and epigenetic factors[27]

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Summary

Introduction

Female intrasexual competition can be intense in cooperatively breeding species, with some dominant breeders (matriarchs) limiting reproduction in subordinates via aggression, eviction or infanticide. In males, such tendencies bidirectionally link to testosterone, but in females, there has been little systematic investigation of androgen-mediated behaviour within and across generations. Late-gestation antiandrogen treatment of matriarchs 4) reduces dominance behaviour, is associated with infrequent evictions, decreases social centrality within the clan, 5) increases aggression in cohabiting subordinate dams, and 6) reduces offspring aggression These effects implicate androgen-mediated aggression in the operation of female sexual selection, and intergenerational transmission of masculinised phenotypes in the evolution of meerkat cooperative breeding. We combine normative and experimental data to ascertain female meerkat phenotypes and test for both activational and organisational effects on behaviour that could reveal a heritable/epigenetic, androgenic mechanism of female reproductive competition

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