Context-dependent effects of testosterone treatment to males on pair maintenance behaviour in zebra finches

Abstract

International audienceMonogamous pair bonds can be transient or long-lasting, which varies across species. The neuroendocrine mechanisms regulating pair maintenance behaviours are largely unknown, yet fundamental to our understanding of monogamy. Furthermore, the expression and regulation of pair maintenance behaviour is likely to be greatly influenced by social and environmental contexts. Our previous research suggested that androgens might regulate long-term pair maintenance behaviour in the monogamous zebra finch, Taeniopygia guttata. Here, we tested the hypothesis that testosterone treatment to males affects long-term pair maintenance behaviour in zebra finches. Established pairs were randomly assigned to one of two groups: control (N = 8) or testosterone (N = 7). Males were given either an empty or a testosterone-filled Silastic implant. Physical and acoustic affiliative behaviours and plasma testosterone levels were examined at three time points: pre-implantation, 30 days post-implant and 60 days post-implant. Importantly, we examined affiliative behaviours under two contexts: in the home cage (baseline) and following a brief chase (post stressor). Male testosterone treatment had no effects on behaviour during the baseline period, but significantly affected behaviours during the post stressor period. Specifically, testosterone-treated males spent less time in close proximity to their partner and sang more. To our knowledge, this is the first report of a context-dependent effect in the neuroendocrine regulation of pair maintenance behaviour, as well as the first report of an inhibitory effect of testosterone on zebra finch pairing behaviours. These results raise interesting questions about the function of affiliative behaviours in established pair bonds

What’s in a Moment: What Can Be Learned About Pair Bonding From Studying Moment-To-Moment Behavioral Synchrony Between Partners?

“…This focus is particularly relevant for animal behavior research, where the terms behavioral synchrony and coordination are less pervasive than in human research. For example, spatial proximity or coordinated activities, which are commonly used dependent variables ( Prior et al, 2014 , 2016 , 2018 ; Prior and Soma, 2015 ), are not referred to in the literature as measures of synchrony, despite that they would be classified as synchrony by the above definitions. Considered generally, spatial proximity itself is a hallmark of pair bonding and social bonding in birds and other species ( Black and Hulme, 1996 ; Frigerio et al, 2001 ; Emery Thompson, 2019 ; Szipl et al, 2019 ); but such research lines are not included here.…”

“…One potential strategy that may allow us to disentangle behavioral synchrony (during brief interactions), parental coordination, and hormonal synchrony is to expose pairs to perturbations, disrupting levels of coordination between partners. In general behavioral disruptions are valuable in eliciting pair-directed behavior ( Prior et al, 2014 , 2016 ), and disrupting parental coordination has been effectively used to clarify the behavioral mechanisms underlying parental coordination ( Boucaud et al, 2016a , b , 2017 ).…”

“…By this reasoning, it may be assumed that strongly bonded pairs display more affiliative behaviors across domains. However, various disruptions (e.g., brief stressors, pharmacological and hormonal manipulations) often affect one type of affiliative behavior and not another (Prior et al, 2014), or affect different types of behaviors in opposing ways (Prior et al, 2016(Prior et al, , 2018. Such experiments raise the question of how different behavioral components contribute to the formation and maintenance of pair bonds as well as how to assess the consequences of such perturbations on pair bonds.…”

“…Overall, it has been particularly challenging to identify changes in affiliative behavior following the formation of a pair bond ( Williams et al, 1992 ; Carter, 1998 ; Resendez et al, 2016 ; Scribner et al, 2019 ). Current research on pair-bond maintenance often requires interrogation of relatively subtle behavioral dynamics ( Prior et al, 2016 , 2019 ; Scribner et al, 2019 ).…”

The singing question: re‐conceptualizing birdsong

“…Despite this strong association, in temperate birds, between song and breeding, neither are exclusive to the spring. Furthermore, although there is evidence in many species that testosterone can increase the probability and intensity of singing (Schlinger & Brenowitz, 2002; Alward, Balthazart & Ball, 2013), this can be context specific (Prior et al ., 2016). Thus, it is important not to adopt an overly deterministic view as testosterone is not required for song in all contexts (e.g.…”