The challenge hypothesis revisited: Focus on reproductive experience and neural mechanisms

Abstract

Our review focuses on findings from mammals as part of a Special Issue "30th Anniversary of the Challenge Hypothesis". Here we put forth an integration of the mechanisms through which testosterone controls territorial behavior and consider how reproductive experience may alter these mechanisms. The emphasis is placed on the function of socially induced increases in testosterone (T) pulses, which occur in response to social interactions, as elegantly developed by Wingfield and colleagues. We focus on findings from the monogamous California mouse, as data from this species shows that reproductive status is a key factor influencing social interactions, site fidelity, and vigilance for offspring defense. Specifically, we examine differences in T pulses in sexually naïve versus sexually experienced pair bonded males. Testosterone pulses influence processes such as social decision making, the winner-challenge effect, and location preferences through rewarding effects of T. We also consider how social and predatory vigilance contribute to T pulses and how these interactions contribute to a territory centered around maximizing reproduction. Possible underlying mechanisms for these effects include the nucleus accumbens (rewarding effects of testosterone), hippocampus (spatial memories for territories), and the bed nucleus of the stria terminalis (social vigilance). The development of the challenge effect has provided an ideal framework for understanding the complex network of behavioral, environmental, physiological and neural mechanisms that ultimately relates to competition and territoriality across taxa. The opportunity to merge research on the challenge effect using both laboratory and field research to understand social behavior is unparalleled.

Testosterone induces a conditioned place preference to the nest of a monogamous mouse under field conditions

“…Fusani 2008; Goymann et al 2015; Ketterson et al 1992; Marler and Moore 1989) and, among other possibilities, may allow males to avoid the high costs of sustained T levels. T-pulse release in response to social interactions can occur in a variety of species, including humans (Gleason et al 2009; Fuxjager et al 2017; review by Marler and Trainor 2020) and our results are consistent with laboratory observations in mice, rats, and hamsters showing that T-pulses have reinforcing/rewarding effects as described in the introduction (Alexander et al 1994; Arnedo et al 2000; Wood 2004; Zhao and Marler 2014; 2016). It is of interest to note that the androgen-induced CPPs can by blocked by dopamine antagonists, further reinforcing the concept of reinforcing/reward functions (Gleason et al 2009; Marler et al 2005; Packard et al 1998).…”

“…Our research significantly extends our understanding of the functions of such T-pulses with relevance to the large variety of species that express these T pulses. Research on California mice has provided evidence for a variety of functions of T-pulses in male California mice (review by Marler and Trainor 2020), but this is among the first study to extend this to a complex field environment (also see Timonin et al 2018). Our research further extends evidence that T manipulations alter vocal communication, in a biparental and monogamous species through both direct and indirect mechanisms.…”

The postnatal testosterone rebound in first‐time fathers and the quality and quantity of paternal care

“…Similar nuance with regard to the role of T on paternal behavior comes from the California mouse-one of very few mammals where paternal care is observed. In these males, higher levels of T are associated with increased levels of care (see Marler & Trainor, 2019 for a review on context and T). While this may be mediated in a manner that differs from human males (i.e., estrogen receptors; Trainor & Marler, 2002), this is one more example that viewing T and paternal care as unidimensional is inaccurate.…”

Supergenes on Steroids

“…This rise in testosterone has been hypothesized to heighten vigilance in anticipation of a sustained challenge [17]; however, the function of challenge-induced testosterone secretion in birds remains unclear [18]. In mice, challenge-induced testosterone pulses have been shown to alter social decision-making, social vigilance, and the probability of winning future encounters [19]. These transient increases are rewarding and reinforcing, suggesting that a challenge-induced increase in testosterone may increase the probability of subsequent aggression because responding to the challenge was reinforcing.…”