Evaluating testosterone as a phenotypic integrator: From tissues to individuals to species

Lipshutz, Sara E.; George, Emad; Bentz, Alexandra B.; Rosvall, Kimberly A.

doi:10.1016/j.mce.2019.110531

Cited by 55 publications

(41 citation statements)

References 107 publications

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“…However, the pattern does occur in some cases, such as in association with aggression in spotted antbirds [25] and Siberian hamsters [33,55]. The observed variation across species in these relationships is consistent with recent evidence that the endocrine system, and particularly tissue sensitivity to hormones as mediated by receptor abundance, is evolutionarily labile [80,81]. Empirical studies that evaluate a potential protective effect of seasonal downregulation of receptors have been far fewer, though patterns consistent with such a role have emerged in association with the parental stage [76].…”

Section: Discussionsupporting

confidence: 85%

Seasonal regulation of behaviour: what role do hormone receptors play?

Watts

2020

Proc. R. Soc. B.

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Many animals differentially express behaviours across the annual cycle as life stages are coordinated with seasonal environmental conditions. Understanding of the mechanistic basis of such seasonal changes in behaviour has traditionally focused on the role of changes in circulating hormone levels. However, it is increasingly apparent that other endocrine regulation mechanisms such as changes in local hormone synthesis and receptor abundance also play a role. Here I review what is known about seasonal changes in steroid hormone receptor abundance in relation to seasonal behaviour in vertebrates. I find that there is widespread, though not ubiquitous, seasonal variation in the expression of steroid hormone receptors in the brain, with such variation being best documented in association with courtship, mating and aggression. The most common pattern of seasonal variation is for there to be upregulation of sex steroid receptors with the expression of courtship and mating behaviours, when circulating hormone levels are also high. Less well-documented are cases in which seasonal increases in receptor expression could compensate for low circulating hormone levels or seasonal downregulation that could serve a protective function. I conclude by identifying important directions for future research.

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Section: Discussionsupporting

confidence: 85%

Seasonal regulation of behaviour: what role do hormone receptors play?

Watts

2020

Proc. R. Soc. B.

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“…Circulating T is only one component of the androgen signaling system, and regulatory mechanisms of competitive traits in both sexes could also depend on T-responsiveness in neural and peripheral tissues, including tissue-specific variation in T production, metabolite conversion, and androgen or estrogen receptors (Ball and Balthazart, 2019;Fuxjager and Schuppe, 2018;Schmidt et al, 2008;Soma, 2006;Staub and De Beer, 1997). Such tissue-specific variability may regulate phenotypic traits independently of circulating sex steroids (Bentz et al, 2019;Horton et al, 2014;Lipshutz et al, 2019a;Rosvall et al, 2012), but there is some evidence that tissue-specific versus systemic regulation of sex steroid mediated traits may be more prevalent for groups in which T levels are depressed (Demas et al, 2007;Rosvall, 2013b). Sex differences in androgenic signaling in the brain have been found in several sex-role reversed species; female black coucals and barred button quails had higher mRNA expression of androgen receptors (AR) in neural regions implicated in the control of aggressive and sexual behavior (Voigt, 2016;Voigt and Goymann, 2007).…”

Section: Discussionmentioning

confidence: 99%

“…This cross-stage shift in T production has been well demonstrated in males (Hirschenhauser and Oliveira, 2006), and is potentially more dramatic in females (DeVries et al, 2012;George and Rosvall, 2018;Jawor et al, 2007). Cross-stage shifts may also alter correlations between T and sexually selected traits, such that these traits are strongly integrated with T during competition for mates, but more independent from T during periods of parental care (Ketterson et al, 2009;Lipshutz et al, 2019a). An open question is how reproductive roles impose sex-specific selection pressures on the phenotypic covariation between T and competitive traits, especially if these traits are under stronger selection in a particular breeding stage and/or for a particular sex (Hämäläinen, 2018).…”

Section: Introductionmentioning

confidence: 91%

Testosterone secretion varies in a sex- and stage-specific manner: insights on the regulation of competitive traits from a sex-role reversed species

Lipshutz

Rosvall

2019

Preprint

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Highlights• Hormones in role reversed species can reveal the influence of parental vs gonadal sex • In jacanas, females face stronger intra-sexual competition, and males care for offspring • We examine covariation between testosterone (T) and mating competition • Circulating T is similar in females and incubating males, but higher in copulating males • T levels co-vary with different competitive traits, depending on sex and breeding stage. AbstractTestosterone (T) mediates a variety of traits that function in competition for mates, including territorial aggression, ornaments, armaments, and gametogenesis. The link between T and mating competition has been studied mainly in males, but is less understood in females, who also face selection pressures to compete for mates. Sex-role reversed species, in which females are the more competitive sex, provide a unique perspective on the role of T in promoting competitive traits. We examined whether T co-varies with competitive traits in sexrole reversed Northern Jacanas (Jacana spinosa) during breeding, when females are fertile and males are either seeking copulations or conducting parental care. We collected data on baseline levels of T in circulation in both sexes, and measured a suite of behavioral and morphological traits putatively involved in mating competition. Contrary to nearly all prior work on sex-role reversal, we did not find a significant main effect of sex on T secretion. Instead, females and incubating males had similar levels of T secretion, which were lower than those observed in copulating males. Nevertheless, females had higher expression of a suite of competitive traits, and their T was higher than most tropical birds. In females, T positively correlated with wing spur size, but was uncorrelated with other competitive traits, including aggression. In males, T correlated with facial shield size and body mass, and among copulating males, T also predicted testes mass. These findings suggest that the mechanisms regulating competitive traits vary with reproductive role in ways that are unique from gonadal sex.

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“…Hormones are common mediators of phenotypic integration. For example, many hormones govern contemporaneous developmental changes during maturation [ 17 , 18 , 19 ]. Hormones may also induce integration via pleiotropic effects on phenotypically-plastic traits [ 19 , 20 , 21 , 22 ].…”

Section: Introductionmentioning

confidence: 99%

Physiological Stress Integrates Resistance to Rattlesnake Venom and the Onset of Risky Foraging in California Ground Squirrels

Holding

Putman

Kong

et al. 2020

Toxins

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Using venom for predation often leads to the evolution of resistance in prey. Understanding individual variation in venom resistance is key to unlocking basic mechanisms by which antagonistic coevolution can sustain variation in traits under selection. For prey, the opposing challenges of predator avoidance and resource acquisition often lead to correlated levels of risk and reward, which in turn can favor suites of integrated morphological, physiological and behavioral traits. We investigate the relationship between risk-sensitive behaviors, physiological resistance to rattlesnake venom, and stress in a population of California ground squirrels. For the same individuals, we quantified foraging decisions in the presence of snake predators, fecal corticosterone metabolites (a measure of “stress”), and blood serum inhibition of venom enzymatic activity (a measure of venom resistance). Individual responses to snakes were repeatable for three measures of risk-sensitive behavior, indicating that some individuals were consistently risk-averse whereas others were risk tolerant. Venom resistance was lower in squirrels with higher glucocorticoid levels and poorer body condition. Whereas resistance failed to predict proximity to and interactions with snake predators, individuals with higher glucocorticoid levels and in lower body condition waited the longest to feed when near a snake. We compared alternative structural equation models to evaluate alternative hypotheses for the relationships among stress, venom resistance, and behavior. We found support for stress as a shared physiological correlate that independently lowers venom resistance and leads to squirrels that wait longer to feed in the presence of a snake, whereas we did not find evidence that resistance directly facilitates latency to forage. Our findings suggest that stress may help less-resistant squirrels avoid a deadly snakebite, but also reduces feeding opportunities. The combined lethal and non-lethal effects of stressors in predator–prey interactions simultaneously impact multiple key traits in this system, making environmental stress a potential contributor to geographic variation in trait expression of toxic predators and resistant prey.

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Evaluating testosterone as a phenotypic integrator: From tissues to individuals to species

Cited by 55 publications

References 107 publications

Seasonal regulation of behaviour: what role do hormone receptors play?

Seasonal regulation of behaviour: what role do hormone receptors play?

Testosterone secretion varies in a sex- and stage-specific manner: insights on the regulation of competitive traits from a sex-role reversed species

Physiological Stress Integrates Resistance to Rattlesnake Venom and the Onset of Risky Foraging in California Ground Squirrels

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