Medial amygdala ERα expression influences monogamous behaviour of male prairie voles in the field.

Connor T Lambert,Bruce S Cushing,Nancy G Solomon,James B Lichter,Adam N Perry,Brian Keane,Samuel A Castillo

doi:10.1098/rspb.2021.0318

Abstract

Formation of long-term pair-bonds is a complex process, involving multiple neural circuits and is context- and experience-dependent. While laboratory studies using prairie voles have identified the involvement of several neural mechanisms, efforts to translate these findings into predictable field outcomes have been inconsistent at best. Here we test the hypothesis that inhibition of oestrogen receptor alpha (ERα) in the medial amygdala of male prairie voles would significantly increase the expression of social monogamy in the field. Prairie vole populations of equal sex ratio were established in outdoor enclosures with males bred for high levels of ERα expression and low levels of prosocial behaviour associated with social monogamy. Medial amygdala ERα expression was knocked down in half the males per population. Knockdown males displayed a greater degree of social monogamy in five of the eight behavioural indices assessed. This study demonstrates the robust nature of ERα in playing a critical role in the expression of male social monogamy in a field setting.

Highlights

Even though social monogamy in mammals is relatively rare, estimates ranging from 5% to 15% [1,2], it has been a highly studied phenomenon
Social monogamy is classified by a suite of prosocial behaviours, which includes the formation of long-term male–female pairs bonds and bi-parental care of offspring, rather than mating exclusivity
While laboratory studies have been invaluable in elucidating neural mechanisms and circuits involved in regulating social monogamy and prosocial behaviour, the critical step is to examine if these highly controlled experimental results translate into predictable outcomes under the greater complexity of natural conditions

Summary

Introduction

Even though social monogamy in mammals is relatively rare, estimates ranging from 5% to 15% [1,2], it has been a highly studied phenomenon. While laboratory studies have been invaluable in elucidating neural mechanisms and circuits involved in regulating social monogamy and prosocial behaviour, the critical step is to examine if these highly controlled experimental results translate into predictable outcomes under the greater complexity of natural conditions. One study by Keane et al [33] did find a relationship between the number of females with which a male sires offspring and avpr1a microsatellite length, but it was the opposite of the predicted relationship with males with longer microsatellites breeding with more females, while others found no relationships between avpr1a genotype and any aspect of the mating system [27,29,30,34] The results of these studies clearly indicate that other factors are playing a critical role in behaviours linked to monogamy [26,35,36]. Additional tables containing model results are available in the electronic supplementary material

Discussion

Findings

Methods