Contextual modulation of androgen effects on agonistic interactions

Pradhan, Devaleena S.; Kl, Connor; Pritchett, Elizabeth M.; Grober, Matthew S.

doi:10.1016/j.yhbeh.2013.11.006

Cited by 18 publications

(33 citation statements)

References 54 publications

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“…; Pradhan et al . ), and therefore higher 11‐kt in nesting males relative to other morphs is consistent with their behavioural repertoire. However, satellite males also exhibit high levels of aggression towards sneakers despite their low levels of circulating 11‐kt.…”

Section: Discussionsupporting

confidence: 62%

Neuroendocrine profiles associated with discrete behavioural variation in Symphodus ocellatus, a species with male alternative reproductive tactics

et al. 2016

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The molecular mechanisms underlying phenotypic plasticity are not well understood. Identifying mechanisms underlying alternative reproductive tactics (ARTs) in species for which the behavioural and fitness consequences of this variation are well characterized provides an opportunity to integrate evolutionary and mechanistic understanding of the maintenance of variation within populations. In the ocellated wrasse Symphodus ocellatus, the behavioural phenotypes of three distinct male morphs (sneakers, satellites and nesting males), which arise from a single genome, have been thoroughly characterized. To determine the neuroendocrine and genomic mechanisms associated with discrete phenotypic variation and ARTs in S. ocellatus in their natural environment, we constructed a whole-brain de novo transcriptome and compared global patterns of gene expression between sexes and male morphs. Next, we quantified circulating cortisol and 11-ketotestosterone (11-kt), mediators of male reproductive behaviours, as well as stress and gonadal steroid hormone receptor expression in the preoptic area, ventral subpallial division of the telencephalon and dorsolateral telencephalon, critical brain regions for social and reproductive behaviours. We found higher levels of 11-kt in nesting males and higher levels of cortisol in sneaker males relative to other male morphs and females. We also identified distinct patterns of brain region-specific hormone receptor expression between males such that most hormone receptors are more highly expressed in satellites and nesting males relative to sneakers and females. Our results establish the neuroendocrine and molecular mechanisms that underlie ARTs in the wild and provide a foundation for experimentally testing hypotheses about the relationship between neuromolecular processes and reproductive success.

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Section: Discussionsupporting

confidence: 62%

Neuroendocrine profiles associated with discrete behavioural variation in Symphodus ocellatus, a species with male alternative reproductive tactics

et al. 2016

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“…Each pair was provided with a PVC tube (7.62 cm in length, 3 cm in diameter) that served as the nest. After 5 days, each male was implanted IP with either beeswax (Natural Cosmetics) only (vehicle, n ¼ 5) or beeswax þ CBX (n ¼ 4) using previously described procedures [33]. Implants were prepared by heat sterilizing beeswax and moulding into small pellets under a microscope.…”

Section: Materials and Methods (A) General Methodsmentioning

confidence: 99%

A mechanism for rapid neurosteroidal regulation of parenting behaviour

et al. 2014

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While systemic steroid hormones are known to regulate reproductive behaviour, the actual mechanisms of steroidal regulation remain largely unknown. Steroidogenic enzyme activity can rapidly modulate social behaviour by influencing neurosteroid production. In fish, the enzyme 11b-hydroxysteroid dehydrogenase (11b-HSD) synthesizes 11-ketotestosterone (KT, a potent teleost androgen) and deactivates cortisol (the primary teleost glucocorticoid), and both of these steroid hormones can regulate behaviour. Here, we investigated the role of neurosteroidogenesis in regulating parenting in a haremic bidirectionally hermaphroditic fish, Lythrypnus dalli, where males provide all requisite parental care. Using an in vitro assay, we found that an 11b-HSD inhibitor, carbenoxolone (CBX), reduced brain and testicular KT synthesis by 90% or more. We modulated neurosteroid levels in parenting males via intracerebroventricular injection of CBX. Within only 20 min, CBX transiently eliminated parenting behaviour, but not other social behaviour, suggesting an enzymatic mechanism for rapid neurosteroidal regulation of parenting. Consistent with our proposed mechanism, elevating KT levels rescued parenting when paired with CBX, while cortisol alone did not affect parenting. Females paired with the experimental males opportunistically consumed unattended eggs, which reduced male reproductive success by 15%, but some females also exhibited parenting behaviour and these females had elevated brain KT. Brain KT levels appear to regulate the expression of parenting behaviour as a result of changes in neural 11b-HSD activity.

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“…dalli genitalia have two internal chambers composed of mesenchymal and epithelial tissue that are arranged in a manner consistent with the external genitalia of most vertebrates. Third, although primary sexual differentiation and adult sex change are regulated by social factors in L. dalli (Rodgers et al 2007;Solomon-Lane et al 2016), administration of the potent fish androgen, 11-ketotestosterone (KT) induces rapid reorganization and masculinization of GP morphology in adult females (Carisle et al 2000;Pradhan et al 2014). Paradoxically, KT concentrations are not sexually dimorphic in this species, so the maintenance of male genitalia is not dependent on "male typical" androgen levels.…”

Section: Introductionmentioning

confidence: 99%

Ancestral androgenic differentiation pathways are repurposed during the evolution of adult sexual plasticity

Schuppe

Solomon‐Lane

Pradhan

et al. 2016

Evolution and Development

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Although early exposure to androgens is necessary to permanently organize male phenotype in many vertebrates, animals that exhibit adult sexual plasticity require mechanisms that prevent early fixation of genital morphology and allow for genital morphogenesis during adult transformation. In Lythrypnus dalli, a teleost fish that exhibits bi-directional sex change, adults display dimorphic genitalia morphology despite the absence of sex differences in the potent fish androgen 11-ketotestosterone. Based on conserved patterns of vertebrate development, two steroid-based mechanisms may regulate the early development and adult maintenance of dimorphic genitalia; local androgen receptor (AR) and steroidogenic enzyme expression. Consistent with the ancestral pattern of AR expression during the multipotential phase of differentiation, juvenile differentiation into either sex involved high mesenchymal AR expression. In adults, AR expression was high throughout the male genitalia, but low or absent in females. Consistent with the hypothesis that adult sexual plasticity repurposes pathways from primary differentiation, we show that adults with transitioning genitalia also exhibited higher AR expression relative to females. Local androgen biosynthesis may also participate in genitalia transformation, as transitioning adults had greater 11β-HSD-like immunoreactivity in the epithelial layer of the dorsal lumen compared to both sexes. By administering an AR antagonist to adult males, we show AR is necessary to maintain male-typical morphology. In a species that is resistant to early sexual canalization, early androgenic differentiation mechanisms are consistent with other vertebrates and the tissue-specific regulation of AR expression appears to be repurposed in adulthood to allow for transitions between sexual phenotypes.

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Contextual modulation of androgen effects on agonistic interactions

Cited by 18 publications

References 54 publications

Neuroendocrine profiles associated with discrete behavioural variation in Symphodus ocellatus, a species with male alternative reproductive tactics

Neuroendocrine profiles associated with discrete behavioural variation in Symphodus ocellatus, a species with male alternative reproductive tactics

A mechanism for rapid neurosteroidal regulation of parenting behaviour

Ancestral androgenic differentiation pathways are repurposed during the evolution of adult sexual plasticity

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