Sexually dimorphic role of oxytocin in medaka mate choice

Yokoi, Sana; Naruse, Kiyoshi; Kamei, Yasuhiro; Ansai, Satoshi; Kinoshita, Masato; Mito, Mari; Iwasaki, Shigeo; Inoue, Shuntaro; Okuyama, Toru; Nakagawa, Shinichi; Young, Larry J.; Takeuchi, Hideaki

doi:10.1073/pnas.1921446117

Cited by 46 publications

(32 citation statements)

References 34 publications

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“…For example, oxt expression in the telencephalon and hypothalamus was not different between WT and scg2a −/− ;-scg2b −/− males and females. Importantly, using oxt and oxtr1 mutations in medaka, Yokoi et al (51) demonstrated that oxt function is required for mate choice based on familiarity recognition. They concluded that oxt is important for female recognition of familiar males.…”

Section: Discussionmentioning

confidence: 99%

Targeted mutation of secretogranin-2 disrupts sexual behavior and reproduction in zebrafish

Mitchell

Zhang

et al. 2020

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

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The luteinizing hormone surge is essential for fertility as it triggers ovulation in females and sperm release in males. We previously reported that secretoneurin-a, a neuropeptide derived from the processing of secretogranin-2a (Scg2a), stimulates luteinizing hormone release, suggesting a role in reproduction. Here we provide evidence that mutation of thescg2aandscg2bgenes using TALENs in zebrafish reduces sexual behavior, ovulation, oviposition, and fertility. Large-scale spawning within-line crossings (n= 82 to 101) were conducted. Wild-type (WT) males paired with WT females successfully spawned in 62% of the breeding trials. Spawning success was reduced to 37% (P= 0.006), 44% (P= 0.0169), and 6% (P< 0.0001) forscg2a−/−,scg2b−/−, andscg2a−/−;scg2b−/−mutants, respectively. Comprehensive video analysis indicates thatscg2a−/−;scg2b−/−mutation reduces all male courtship behaviors. Spawning success was 47% in saline-injected WT controls compared to 11% in saline-injectedscg2a−/−;scg2b−/−double mutants. For these mutants, spawning success increased 3-fold following a single intraperitoneal (i.p.) injection of synthetic secretoneurin-a (P= 0.0403) and increased 3.5-fold with injection of human chorionic gonadotropin (hCG). Embryonic survival at 24 h remained on average lower inscg2a−/−;scg2b−/−fish compared to WT injected with secretoneurin-a (P< 0.001). Significant reductions in the expression of gonadotropin-releasing hormone 3 in the hypothalamus, and luteinizing hormone beta and glycoprotein alpha subunits in the pituitary provide evidence for disrupted hypothalamo-pituitary function inscg2aandscg2bmutant fish. Our results indicate that secretogranin-2 is required for optimal reproductive function and support the hypothesis that secretoneurin is a reproductive hormone.

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Section: Discussionmentioning

confidence: 99%

Targeted mutation of secretogranin-2 disrupts sexual behavior and reproduction in zebrafish

Mitchell

Zhang

et al. 2020

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

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“…The ability to recognize another individual is crucial for social interaction [28], emerges very early in development [29,30], is conserved across species [28], and is linked to the oxytocin (OXY) system [31,32]. Humans, like other primates, recognize other individuals mostly by their face [33][34][35], which has evolved to signal individual identity [36].…”

Section: Introductionmentioning

confidence: 99%

Face individual identity recognition: a potential endophenotype in autism

et al. 2020

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Background Face individual identity recognition skill is heritable and independent of intellectual ability. Difficulties in face individual identity recognition are present in autistic individuals and their family members and are possibly linked to oxytocin polymorphisms in families with an autistic child. While it is reported that developmental prosopagnosia (i.e., impaired face identity recognition) occurs in 2–3% of the general population, no prosopagnosia prevalence estimate is available for autism. Furthermore, an autism within-group approach has not been reported towards characterizing impaired face memory and to investigate its possible links to social and communication difficulties. Methods The present study estimated the prevalence of prosopagnosia in 80 autistic adults with no intellectual disability, investigated its cognitive characteristics and links to autism symptoms’ severity, personality traits, and mental state understanding from the eye region by using standardized tests and questionnaires. Results More than one third of autistic participants showed prosopagnosia. Their face memory skill was not associated with their symptom’s severity, empathy, alexithymia, or general intelligence. Face identity recognition was instead linked to mental state recognition from the eye region only in autistic individuals who had prosopagnosia, and this relationship did not depend on participants’ basic face perception skills. Importantly, we found that autistic participants were not aware of their face memory skills. Limitations We did not test an epidemiological sample, and additional work is necessary to establish whether these results generalize to the entire autism spectrum. Conclusions Impaired face individual identity recognition meets the criteria to be a potential endophenotype in autism. In the future, testing for face memory could be used to stratify autistic individuals into genetically meaningful subgroups and be translatable to autism animal models.

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“…Regarding sexual behavior, in studies where the regulation of sex hormones was altered, changes in sexual behavior were primarily related to courtship, such as the frequencies of following, dancing, and latency from the first courtship (Hiraki-Kajiyama et al, 2019;Oshima et al, 2003). Additionally, when brain regulators were altered, such as arginine-vasotocin (Yokoi et al, 2015), oxytocin ligand (oxt) (Yokoi et al, 2020) and TN-GnRH3 (Okuyama et al, 2014), changes in courtship display and sexual motivation, latency to mating and number of courtships displays, and latency to mating, were observed, respectively. None of these courtship actions changed in the male ndrg1b mutants, leading us to consider whether the specific mating actions of quivering and convulsions are exclusively related to the lower number of spermatogonia and spermatozoa in males.…”

Section: Discussionmentioning

confidence: 99%

Cystic proliferation of germline stem cells is necessary to reproductive success and normal mating behavior in medaka

Padilla

Castañeda-Cortés

Rosa

et al. 2021

eLife

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The production of an adequate number of gametes is necessary for normal reproduction, for which the regulation of proliferation from early gonadal development to adulthood is key in both sexes. Cystic proliferation of germline stem cells is an especially important step prior to the beginning of meiosis; however, the molecular regulators of this proliferation remain elusive in vertebrates. Here, we report that ndrg1b is an important regulator of cystic proliferation in medaka. We generated mutants of ndrg1b that led to a disruption of germ cells cystic proliferation. This loss of cystic proliferation was observed from embryogenic to adult stages, impacting the success of gamete production and reproductive parameters such as spawning and fertilization. Interestingly, the depletion of cystic proliferation also impacted male sexual behavior, with a decrease of mating vigor. These data illustrate why it is also necessary to consider gamete production capacity in order to analyze reproductive behavior.

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Sexually dimorphic role of oxytocin in medaka mate choice

Cited by 46 publications

References 34 publications

Targeted mutation of secretogranin-2 disrupts sexual behavior and reproduction in zebrafish

Targeted mutation of secretogranin-2 disrupts sexual behavior and reproduction in zebrafish

Face individual identity recognition: a potential endophenotype in autism

Cystic proliferation of germline stem cells is necessary to reproductive success and normal mating behavior in medaka

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