Review article
Reprint of “Concepts derived from the Challenge Hypothesis”

https://doi.org/10.1016/j.yhbeh.2020.104802Get rights and content

Highlights

  • The Challenge Hypothesis 30th anniversary

  • Hormone action occurs at three levels, routine day-to-day regulation levels A and B, and facultative, highest, level C.

  • These state levels may have different regulatory pathways.

  • Testosterone release can be regulated by gonadotropin-releasing hormone (GnRH) and gonadotropin-inhibiting hormone (GnIH).

  • Different social and environmental inputs appear to have unique regulatory pathways.

  • Spectrophotometry has revolutionized assay methods enabling measurement of hormone levels in specific brain areas.

Abstract

The Challenge Hypothesis was developed to explain why and how regulatory mechanisms underlying patterns of testosterone secretion vary so much across species and populations as well as among and within individuals. The hypothesis has been tested many times over the past 30 years in all vertebrate groups as well as some invertebrates. Some experimental tests supported the hypothesis but many did not. However, the emerging concepts and methods extend and widen the Challenge Hypothesis to potentially all endocrine systems, and not only control of secretion, but also transport mechanisms and how target cells are able to adjust their responsiveness to circulating levels of hormones independently of other tissues. The latter concept may be particularly important in explaining how tissues respond differently to the same hormone concentration. Responsiveness of the hypothalamo-pituitary-gonad (HPG) axis to environmental and social cues regulating reproductive functions may all be driven by gonadotropin-releasing hormone (GnRH) or gonadotropin-inhibiting hormone (GnIH), but the question remains as to how different contexts and social interactions result in stimulation of GnRH or GnIH release. These concepts, although suspected for many decades, continue to be explored as integral components of environmental endocrinology and underlie fundamental mechanisms by which animals, including ourselves, cope with a changing environment. Emerging mass spectrometry techniques will have a tremendous impact enabling measurement of multiple steroids in specific brain regions. Such data will provide greater spatial resolution for studying how social challenges impact multiple steroids within the brain. Potentially the Challenge Hypothesis will continue to stimulate new ways to explore hormone-behavior interactions and generate future hypotheses.

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 R=levelClevelAlevelBlevelA (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

References (100)

  • S.A. Heimovics et al.

    Non-invasive administration of 17β-estradiol rapidly increases aggressive behavior in non breeding, but not breeding, male song sparrows

    Horm. Behav.

    (2015)
  • S.A. Heimovics et al.

    Rapid effects of 17β-estradiol on aggressive behavior in songbirds: environmental and genetic influences

    Horm. Behav.

    (2018)
  • M.M. Landys et al.

    Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes

    Gen. Comp. Endocrinol.

    (2006)
  • M.M. Landys et al.

    Impact of season and social challenge on testosterone and corticosterone levels in a year-round territorial bird

    Horm. Behav.

    (2010)
  • B.S. McEwen et al.

    The concept of allostasis in biology and biomedicine

    Horm. Behav.

    (2003)
  • P.E. Micevych et al.

    Estradiol membrane-initiated signaling in the brain mediates reproduction

    Trends Neurosci.

    (2017)
  • I.T. Moore

    Advancing the challenge hypothesis

    Horm. Behav.

    (2007)
  • A.E. Newman et al.

    Aggressive interactions differentially modulate local and systemic levels of corticosterone and DHEA in a wild songbird

    Horm. Behav.

    (2011)
  • R.F. Oliveira

    Social modulation of androgens in vertebrates: mechanisms and function

    Adv. Study Behav.

    (2004)
  • T.O. Oyegbile et al.

    Winning fights elevates testosterone levels in California mice and enhances future ability to win fights

    Horm. Behav.

    (2005)
  • M. Palkovits

    Isolated removal of hypothalamic or other brain nuclei of the rat

    Brain Res.

    (1973)
  • D.S. Pradhan et al.

    Aggressive interactions rapidly increase androgen synthesis in the brain during the non-breeding season

    Horm. Behav.

    (2010)
  • N.H. Prior et al.

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

    Anim. Behav.

    (2016)
  • L.M. Romero et al.

    The reactive scope model – a new model integrating homeostasis, allostasis, and stress

    Horm. Behav.

    (2009)
  • B.A. Schlinger et al.

    3β-HSD activates DHEA in the songbird brain

    Neurochem. Int.

    (2008)
  • K.L. Schmidt et al.

    Neurosteroids, immunosteroids, and the balkanization of endocrinology

    Gen. Comp. Endocrinol.

    (2008)
  • K.K. Soma et al.

    Dehydroepiandrosterone in songbird plasma: seasonal regulation and relationship to territorial aggression

    Gen. Comp. Endocrinol.

    (2001)
  • K.K. Soma et al.

    Combined aromatase inhibitor and antiandrogen treatment decreases territorial aggression in a wild songbird during the nonbreeding season

    Gen. Comp. Endocrinol.

    (1999)
  • K.K. Soma et al.

    Dehydroepiandrosterone (DHEA) increases territorial song and the size of an associated brain region in a male songbird

    Horm. Behav.

    (2002)
  • K.K. Soma et al.

    Novel mechanisms for neuroendocrine regulation of aggression

    Front. Neuroendocrinol.

    (2008)
  • K.K. Soma et al.

    DHEA effects on brain and behavior: insights from comparative studies of aggression

    J. Ster. Biochem. Mol. Biol.

    (2015)
  • M.D. Taves et al.

    Lymphoid organs of neonatal and adult mice preferentially produce active glucocorticoids from metabolites, not precursors

    Brain, Behav. Immun.

    (2016)
  • J.C. Wingfield

    Control of territorial aggression in a changing environment

    Psychoneuroendocrinology

    (1994)
  • J.C. Wingfield

    A continuing saga: the role of testosterone in aggression

    Horm. Behav.

    (2005)
  • J.C. Wingfield

    Communicative behaviors, hormone-behavior interactions, and reproduction in vertebrates

  • J.C. Wingfield et al.

    Testosterone and territorial behaviour in sedentary and migratory sparrows

    Anim. Behav.

    (1994)
  • J.C. Wingfield et al.

    Testosterone, territoriality, and social interactions in neotropical birds

  • E. Adkins-Regan

    Hormones and Animal Social Behavior

    (2005)
  • G.F. Ball et al.

    Individual variation and the endocrine regulation of behavior and physiology in birds: a cellular/molecular perspective

    Phil. Trans. R. Soc. B

    (2007)
  • P.J. Bentley

    Comparative Vertebrate Endocrinology

    (1998)
  • D.F. Cobice et al.

    Mass spectrometry imaging for dissecting steroid intracrinology within target tissues

    Anal. Chem.

    (2013)
  • D.F. Cobice et al.

    Future technology insight: mass spectrometry imaging as a tool in drug research and development

    Brit. J. Pharmacol.

    (2015)
  • J. Cohen

    Statistical Power Analysis for the Behavioral Sciences

    (1988)
  • C. Corpechot et al.

    Characterization and measurement of dehydroepiandrosterone sulfate in rat brain

    Proc. Natl. Acad. Sci. U. S. A.

    (1981)
  • G. Cumming et al.

    A primer on the understanding, use, and calculation of confidence intervals that are based on central and non-central distributions

    Educ. Psychol. Meas.

    (2001)
  • W.R. Dawson et al.

    Metabolic aspects of shivering thermogenesis in passerines during winter

    Ornis Scand.

    (1992)
  • S.M. DeVries et al.

    Non-breeding gonadal testosterone production of male and female northern cardinals (Cardinalis cardinalis) following GnRH challenge

    Gen. Comp. Endocrinol.

    (2011)
  • M.M. Elekonich et al.

    Seasonality and hormonal control of territorial aggression in female song sparrows (Passeriformes: Emberizidae: Melospiza melodia)

    Ethology

    (2000)
  • H.B. Fokidis et al.

    Neuropeptide Y and orexin immunoreactivity in the sparrow brain coincide with seasonal changes in energy balance and steroids

    J. Comp. Neurol.

    (2019)
  • W. Goymann et al.

    Testosterone in tropical birds: effects of environmental and social factors

    Am. Nat.

    (2004)
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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.

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