Review articleReprint of “Concepts derived from the Challenge Hypothesis”☆
Introduction
The original “Challenge Hypothesis” (Wingfield et al., 1990) proffered new insights into the complexity of social interactions and hormone regulatory systems (e.g. Goymann et al., 2004, Goymann et al., 2007a, Goymann et al., 2007b; Moore, 2007; Oliveira, 2004). Some of these insights revisited long-standing issues in behavioral endocrinology and others inspired new hypotheses about ecological and evolutionary constraints of hormone-behavior interactions. These insights have metamorphosed in many ways over the decades allowing new explorations of the complexity of hormone-behavior interactions (Adkins-Regan, 2005) and attempts to explain it. These developments have also driven the emergence of related concepts that have influenced how we think about the organism in its environment, how social interactions change over the life cycle, and how the regulatory mechanisms may have developed independently in many species and populations of species (Wingfield, 2018).
In a related vein, two hypotheses have emerged as a potential framework. One is the evolutionary constraint hypothesis, according to which mechanisms of hormone-behavior interactions are well conserved across and within (e.g. individual variation) taxa, and there may be only restricted ways in which social interactions can be regulated by endocrine systems (Hau, 2007; Ketterson et al., 2009; Hau and Wingfield, 2011). The other is the evolutionary flexibility hypothesis, according to which there are potentially many ways by which control systems for social interactions can be adjusted despite a highly conserved endocrine system. Mechanisms may vary not only across species but also within populations and even individuals (Hau, 2007; Ketterson et al., 2009; Hau and Wingfield, 2011; Wingfield, 2018) and often include the actions of non-steroidal hormones such as peptides acting in paracrine fashion at the target cell level (e.g. Oyegbile and Marler, 2005; Adkins-Regan, 2005; Wingfield et al., 2005). Although social interactions and hormone secretions regulating them have been investigated for many decades (see Adkins-Regan, 2005), there is still a great need to integrate social and environmental factors (e.g. Goymann and Wingfield, 2004; Goymann et al., 2004; 2007; Rubenstein, 2007). Here we outline some developing concepts, from the original Challenge Hypothesis, that illuminate the complexities of hormone-behavior interactions, but at the same time allow clear hypotheses with testable predictions. Although the findings that originally led to these new concepts have been around for many decades, their importance for understanding how an individual interacts with a changing environment, both physical and social, has only recently been fully appreciated.
Section snippets
State levels A, B and C
According to the original Challenge Hypothesis, baseline levels of a hormone (e.g. testosterone) are sufficient for the development and maintenance of morphological, physiological and behavioral traits e.g. territoriality, see also Ball and Balthazart, 2007). Superimposed on baseline patterns of hormone secretion into blood are facultative responses to dynamic behavioral interactions that can modulate hormone secretion further (e.g. glucocorticoids, Sapolsky et al., 2000). These changes in
Costs of testosterone
Why are elevations of hormone levels to level C so brief? Wingfield et al., (1990) proposed that prolonged periods of level C secretion bears costs. For example, high circulating testosterone might be deleterious as are chronic high levels of glucocorticoids (Wingfield et al., 2001; Wingfield and Soma, 2002). Numerous experimental studies on the deleterious effects of high testosterone, both in the field and the laboratory, were published in the next years (e.g. reviewed in Ketterson et al.,
Refining androgen responsiveness
Originally, the Challenge Hypothesis defined androgen responsiveness (or R) as a ratio among the different hormone levels A, B and C. Specifically, androgen responsiveness was (Wingfield et al., 1990). Responsiveness was assumed to represent the rise of testosterone mainly during social interactions among males. At that time few data regarding the change of testosterone during male-male interactions were available. It was thus assumed that seasonal peaks in
Neural steroid synthesis and territorial aggression
During autumn and early winter in the temperate zone, nearly all birds are in non-breeding condition, with regressed gonads and basal levels of circulating sex steroids. Often, non-breeding birds abandon territories and form flocks (e.g. Soma and Wingfield, 1999). However, in some species, individuals continue to aggressively defend territories during the non-breeding season. For example, a subspecies of song sparrow (Melospiza melodia morphna) is sedentary (Wingfield and Hahn, 1994). Males are
Measuring effects of aggressive interactions on brain steroid levels
As summarized above, social interactions can affect steroid production in specific areas of the brain. To assess how social challenges affect local steroid levels, a powerful tool is in vivo micro-dialysis (Remage-Healey et al., 2008), but sampling is often limited to one brain region at a time. Another approach is the Palkovits punch (Palkovits, 1973), which can be used to micro-dissect multiple brain regions from a single animal (Taves et al., 2011). Samples can weigh only 1–2 mg, and
Conclusions
Over the past few decades, investigations of hormone-behavior interrelationships in free-living animals provided new insights into what plasma levels of a hormone may mean (state levels) and how dynamic changes hint at further underlying actions and mechanisms not fully appreciated before. These include development of frameworks for understanding androgen responsiveness to different environmental cues and ultimately what neural and neuroendocrine adaptations may have evolved. New techniques
Acknowledgments
JCW is grateful for a series of grants from the National Science Foundation that span several decades. This continuity of funding was critical to develop new hypothesis and test them over the years. Wingfield is also grateful for the critical input of so many undergraduate students, graduate students, postdoctoral scholars and visiting faculty. The Challenge Hypothesis would not have flourished for so long without their creativity, criticism and boundless energy working in the field and the
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This article is a reprint of a previously published article. For citation purposes, please use the original publication details; Hormones and Behavior, Volume 115, September 2019, Article number 104550.