Male-typical courtship, spawning behavior, and olfactory sensitivity are induced to different extents by androgens in the goldfish suggesting they are controlled by different neuroendocrine mechanisms

Ghosal, Ratna; Sorensen, Peter W.

doi:10.1016/j.ygcen.2016.04.028

Cited by 31 publications

(18 citation statements)

References 46 publications

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“…mature males have higher sensitivity to (a) component(s) in female urine than females themselves. Thus, the process of sexual maturation may influence the expression of olfactory receptor genes in the olfactory epithelium in the sole, as has been shown in the eel (Churcher et al, 2015), and in cyprinids, olfactory sensitivity is increased by androgens (Belanger et al, 2010;Cardwell et al, 1995;Ghosal and Sorensen, 2016). It is likely, therefore, that during sexual maturation, increased circulating sex steroids evoke a differential expression of pheromone receptors in the olfactory epithelium.…”

Section: Discussionmentioning

confidence: 88%

Olfactory sensitivity of the marine flatfishSolea senegalensisto conspecific body fluids

Fatsini

Carazo

Chauvigné

et al. 2017

Journal of Experimental Biology

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Chemical communication is better understood in freshwater fish than marine fish. The Senegalese sole (Solea senegalensis) is a marine flatfish wherein one of the problems in aquaculture is the poor reproductive performance of hatchery-bred males. Is chemical communication involved in the reproduction of this species? Urine, intestinal fluid and mucus samples were taken from adult fish (wildcaught and hatchery-bred) over the spawning season (March-May), and assessed for olfactory potency using the electro-olfactogram (EOG). The effect of stimulation of the olfactory system with adult female urine on circulating luteinizing hormone (LH) levels was also tested in males. Intestinal fluid and urine were potent olfactory stimuli for both juvenile and adult conspecifics, evoking large-amplitude, concentration-dependent EOG responses, with thresholds of detection at approximately 1:10 6 . However, the amplitude of the response to urine depended on the sex and state of maturity of both the donor and the receiver. Most olfactory activity could be extracted by C18 solid-phase cartridges. Urine from mature females evoked a slight, but significant, increase in circulating LH levels in mature males 30 min after exposure. Furthermore, the olfactory potency of urine differed between wild-caught and hatchery-bred fish; however, contrary to expectations, urine from wild-caught females was less potent than that from hatchery-bred females. Taken together, these results strongly suggest that faeces-and urine-released odorants are involved in reproduction in the Senegalese sole, and establish a basis for further investigation into pheromonal communication in marine teleosts.

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Section: Discussionmentioning

confidence: 88%

Olfactory sensitivity of the marine flatfishSolea senegalensisto conspecific body fluids

Fatsini

Carazo

Chauvigné

et al. 2017

Journal of Experimental Biology

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“…Notably, PGF 2α -implants mimic natural circulating levels of PGF 2α , eliciting normal pheromone release for days and making this technique very useful as well as biologically relevant [12]. Electrophysiological experiments have also shown that the olfactory systems of both the Goldfish and Common Carp and a variety of other fishes detect PGF 2α and its metabolites, 15K-PGF 2α and dh15K-PGF 2α , at low concentrations [13,15] in a sexually dimorphic manner that is inducible by androgen treatment [16][17][18]. Studies of the PGF spawning pheromone show that Goldfish and Common Carp discern each other's odors and that a variety of PGFs as well as other metabolites are responsible while specific ratios of PGFs may not be especially important [11].…”

Section: Introductionmentioning

confidence: 99%

“…The present study asked the question of whether the Silver Carp might also use PGFs as a sex pheromone to attract and discern conspecifics. Because this species naturally matures at a large size (about 60 cm) and is very difficult to study in the field, we conducted a proof-of-concept laboratory study with small (juvenile) fish using the same techniques that we have developed to artificially masculinize and study reproductive behaviors in the Goldfish as well as some other cyprinids [17,18]. We asked five questions.…”

Section: Introductionmentioning

confidence: 99%

A Blend of F Prostaglandins Functions as an Attractive Sex Pheromone in Silver Carp

Sorensen

Rue

Leese

et al. 2019

Fishes

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A series of laboratory experiments tested the hypothesis that the Silver Carp (Hypophthalmichthys molitrix), an invasive river carp from China, employs a prostaglandin F2α-derived sex pheromone that is attractive and species-specific. Using electro-olfactogram recording (EOG), we found that the olfactory system of this species is acutely sensitive to three F-series prostaglandins (PGFs) at picomolar concentrations and that this sensitivity is enhanced when juveniles are masculinized using androgens, consistent with expectations of a sex pheromone. Individual PGFs had behavioral activity but it was low, suggesting a mixture might be important. To pursue this possibility, we implanted carps with osmotic pumps containing prostaglandin F2α (PGF2α), a treatment previously shown to elicit release of a PGF-based spawning pheromone in the Common Carp. We found that PGF2α-implanted Silver Carp released a species-specific odor that contained a blend of PGF2α and two of its metabolites, which masculinized individuals detected and were attracted to with high sensitivity. Finally, we found that a mixture of these PGFs was attractive to masculinized Silver Carp, while a different mixture released by Bighead Carp was not. We conclude that Silver Carp likely use a species-specific PGF2α-derived sex pheromone that is probably released at spawning and might be useful in its control. Confirmatory studies that explore pheromone function in naturally mature Silver Carp using natural odors in the field should now be conducted to further confirm our proof-of-concept study.

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“…Interestingly, however, this is not the case in teleost fish. 56In teleosts, experimental manipulations that alter the sex steroid milieu lead to the reversal of sex-typical 57 mating behaviors, even in adulthood (Munakata and Kobayashi, 2010; Paul-Prasanth et al, 2013; 58 Göppert et al, 2016;Ghosal and Sorensen, 2016). Furthermore, a large number of teleost species 59 spontaneously undergo phenotypic sex reversal, involving both behavioral and anatomical changes, in 60 response to social and physiological stimuli (Liu et al, 2017; Capel, 2017).…”

mentioning

confidence: 99%

Neuropeptide B mediates female sexual receptivity in medaka fish, acting in a female-specific but reversible manner

Hiraki-Kajiyama

Yamashita

Yokoyama

et al. 2019

Preprint

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26Male and female animals display innate sex-specific mating behaviors. Among vertebrates, teleosts are 27 unique in that altering the adult sex steroid milieu can reverse sex-typical mating behaviors, suggesting 28 sexual lability of their brains. In the teleost medaka, neuropeptide B (NPB) is expressed female-29 specifically in the brain nuclei implicated in mating behavior. Here, we demonstrate that NPB is a direct 30 mediator of estrogen action on female mating behavior, acting in a female-specific but reversible manner. 31Analysis of regulatory mechanisms revealed that the female-specific expression of NPB is dependent 32 on direct transcriptional activation by estrogen via an estrogen-responsive element and is reversed in 33 response to changes in the adult sex steroid milieu. Behavioral studies of NPB knockouts revealed that 34 female-specific NBP mediates female receptivity to male courtship. The female-specific NPB signaling 35 identified herein is presumably a critical element of the neural circuitry underlying sexual dimorphism 36 and lability of mating behaviors in teleosts. 37 Introduction 38 39 From invertebrates to humans, males and females of a given species exhibit profound differences 40 in mating behavior; in general, males perform elaborate courtship displays to attract females for mating, 41 and females evaluate male courtship displays to decide whether to mate. Such differences in mating 42 behavior between males and females result from sexually dimorphic development and activation of the 43 underlying neural circuits (Yang and Shah, 2016). In vertebrates, sex-typical mating behaviors and the 44 underlying neural circuits are highly dependent on the sex steroid hormone milieu, which is unique to 45 each sex (McCarthy and Arnold, 2011; McCarthy et al., 2017). Males have higher circulating levels of 46 androgen derived from the testis, whereas females have a cyclic pattern of estrogen and progestin arising 47 from the ovary. Sex steroids largely exert their effects by binding to intracellular receptors, which 48 subsequently interact with sex steroid-responsive elements in the genome to modulate the transcription 49 of target genes. Recent work, particularly in rodents and songbirds, has identified sex steroid-responsive 50 neural circuits that underlie the divergent mating behaviors of males versus females, as well as the genes 51 downstream of sex steroids that mediate these behaviors. However, the identity of the sex-specific direct 52 transcriptional targets of sex steroids that mediate sex-typical mating behaviors remains elusive (Yang 53 and Shah, 2014). 54Differences between the sexes in mating behavior are evidently robust and irreversible in many 55 vertebrate taxa, including mammals and birds. Interestingly, however, this is not the case in teleost fish. 56In teleosts, experimental manipulations that alter the sex steroid milieu lead to the reversal of sex-typical 57 mating behaviors, even in adulthood (Munakata and Kobayashi, 2010; Paul-Prasanth et al., 2013; 58 Göppert et al....

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Male-typical courtship, spawning behavior, and olfactory sensitivity are induced to different extents by androgens in the goldfish suggesting they are controlled by different neuroendocrine mechanisms

Cited by 31 publications

References 46 publications

Olfactory sensitivity of the marine flatfishSolea senegalensisto conspecific body fluids

Olfactory sensitivity of the marine flatfishSolea senegalensisto conspecific body fluids

A Blend of F Prostaglandins Functions as an Attractive Sex Pheromone in Silver Carp

Neuropeptide B mediates female sexual receptivity in medaka fish, acting in a female-specific but reversible manner

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