Sex Steroid Regulation of Male- and Female-Typical Mating Behaviors in Teleost Fish

Okubo, Kataaki; Nishiike, Yuji; Fleming, Thomas; Kikuchi, Yukiko; Hiraki-Kajiyama, Towako

doi:10.1007/978-981-19-5359-0_7

Cited by 7 publications

(15 citation statements)

References 133 publications

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“…Taken together with the observation that castration in males severely reduced VT expression in the pNVT, it seems that the sexually dimorphic pattern of VT expression in medaka can be reversed between the sexes in response to changes in the adult androgen milieu. It is known that the sexual phenotypes of teleosts (behavioral or otherwise), unlike those of terrestrial vertebrates, are highly labile across the lifespan and can be reversed between the sexes, even as adults (Okubo et al ., 2019; 2022); the present study now shows that manipulation of the adult androgen milieu effectively reverses sex-typical aggressive behavior. The reversibility of sexually dimorphic VT expression may reflect this fact.…”

Section: Discussionsupporting

confidence: 65%

“…First, in the rodent extended amygdala, a large fraction of testosterone is converted locally to E2 and then acts through the ESR (Aspesi and Choleris, 2022), whereas in the medaka tuberal hypothalamus, KT, an androgen that cannot be converted to E2, acts directly through the AR. Because the effects of androgens on male behavior rely primarily on an AR-mediated pathway in many vertebrate species (Okubo et al ., 2022), our findings in medaka may be broadly applicable to other species. The second difference concerns whether treating adult females with sex steroids induces VT expression above basal levels.…”

Section: Discussionmentioning

confidence: 99%

“…However, the transcriptional targets of ESR1 that mediate aggressive behavior remain elusive, and the specific role of sex steroids in the regulation of aggression is unclear. Furthermore, and importantly, it is unlikely that the findings in rodents apply to other vertebrates including primates and teleost fish, where androgens act directly on behaviorally relevant neural circuits via the androgen receptor (AR) without conversion to estrogens (Okubo et al ., 2019; 2022).…”

Section: Introductionmentioning

confidence: 99%

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Male-specific vasotocin expression in the medaka tuberal hypothalamus: androgen dependence and probable role in aggression

Kawabata-Sakata,

Kanda,

Okubo

2023

Preprint

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Terrestrial vertebrates have a population of androgen-dependent vasotocin (VT)-expressing neurons in the extended amygdala that are more abundant in males and mediate male-typical social behaviors, including aggression. Teleosts lack these neurons but instead have novel male-specific VT-expressing neurons in the tuberal hypothalamus. Here we found in medaka thatvtexpression in these neurons is dependent on post-pubertal gonadal androgens and that androgens can act on these neurons to directly stimulatevttranscription via the androgen receptor subtype Ara. Furthermore, administration of exogenous VT induced aggression in females and alterations in the androgen milieu led to correlated changes in the levels of tuberal hypothalamicvtexpression and aggression in both sexes. However, genetic ablation ofvtfailed to prevent androgen-induced aggression in females. Collectively, our results demonstrate a marked androgen dependence of male-specificvtexpression in the teleost tuberal hypothalamus, although its relevance to male-typical aggression needs to be further validated.

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Section: Discussionsupporting

confidence: 65%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Male-specific vasotocin expression in the medaka tuberal hypothalamus: androgen dependence and probable role in aggression

Kawabata-Sakata,

Kanda,

Okubo

2023

Preprint

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“…In this study, we found that male medaka deficient for cyp19a1b exhibit severely impaired male-typical mating and aggression. This observation was unexpected because the fish had markedly elevated brain levels of 11KT, the primary driver of male-typical behaviors in teleosts (9, 11). These behavioral deficits were rescued by estrogen administration, indicating that reduced levels of neuroestrogens are the primary cause of the observed phenotypes: in other words, neuroestrogens are pivotal for male-typical behaviors in teleosts.…”

Section: Discussionmentioning

confidence: 99%

Neuroestrogens facilitate male-typical behaviors by potentiating androgen receptor signaling in medaka

Nishiike,

Maki,

Miyazoe

et al. 2024

Preprint

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In rodents, estrogens aromatized from androgens in the brain, also known as neuroestrogens, are essential for the development of male-typical behaviors. In many other vertebrates including humans and teleost fish, however, androgens facilitate these behaviors directly via the androgen receptor without aromatization into estrogens. Here we report that male medaka fish lacking Cyp19a1b (a subtype of aromatase predominantly expressed in the brain) exhibit severely impaired male-typical mating and aggression, despite elevated brain androgen levels. These phenotypes can be rescued by estrogen administration, indicating that neuroestrogens are pivotal for male-typical behaviors even in non-rodents. Our results further suggest that neuroestrogens facilitate male-typical behaviors by potentiating androgen action in the brain via the direct stimulation of androgen receptor transcription, thereby revealing a previously unappreciated mechanism of action of neuroestrogens. We additionally show that female fish lacking Cyp19a1b are less receptive to male courtship and conversely court other females, highlighting the significance of neuroestrogens in establishing sex-typical behaviors in both sexes.

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“…Female teleosts, when treated with 11KT as adults, display male-typical aggressive and mating behavior while retaining their ovaries (18)(19)(20)(21)33). We considered that, if the above conclusions apply to females as well as males, the male-typical aggressive and mating behaviors observed in 11KT-treated females are likely to be elicited through Ara and Arb, respectively.…”

Section: Adult Androgen/ar Signaling Elicits Male-typical Behavioral ...mentioning

confidence: 99%

The decision of male medaka to mate or fight depends on two complementary androgen signaling pathways

Nishiike,

Okubo

2024

Preprint

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Adult male animals typically court and attempt to mate with females, while attacking other males. Emerging evidence from mice indicates that neurons expressing the estrogen receptor ESR1 in behaviorally relevant brain regions play a central role in mediating these mutually exclusive behavioral responses to conspecifics. However, the findings in mice are unlikely to apply to most other vertebrates, where androgens, rather than estrogens, have been implicated in male behaviors. Here we report that male medaka (Oryzias latipes) lacking one of the two androgen receptor subtypes (Ara) are less aggressive toward other males and instead actively court them, while those lacking the other subtype (Arb) are less motivated to mate with females and conversely attack them. These findings indicate that, in male medaka, the Ara- and Arb-mediated androgen signaling pathways facilitate appropriate behavioral responses, while simultaneously suppressing inappropriate responses, to males and females, respectively. Notably, males lacking either receptor retain the ability to discriminate the sex of conspecifics, suggesting a defect in the subsequent decision-making process to mate or fight. We further show that Ara and Arb are expressed in intermingled but largely distinct populations of neurons, and stimulate the expression of different behaviorally relevant genes including galanin and vasotocin, respectively. Collectively, our results demonstrate that male teleosts make adaptive decisions to mate or fight as a result of the activation of one of two complementary androgen signaling pathways, depending on the sex of the conspecific that they encounter.

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Sex Steroid Regulation of Male- and Female-Typical Mating Behaviors in Teleost Fish

Cited by 7 publications

References 133 publications

Male-specific vasotocin expression in the medaka tuberal hypothalamus: androgen dependence and probable role in aggression

Male-specific vasotocin expression in the medaka tuberal hypothalamus: androgen dependence and probable role in aggression

Neuroestrogens facilitate male-typical behaviors by potentiating androgen receptor signaling in medaka

The decision of male medaka to mate or fight depends on two complementary androgen signaling pathways

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