Mating behaviors in ovoviviparous black rockfish (Sebastes schlegelii): molecular function of prostaglandin E2 as both a hormone and pheromone

Abstract

Prostaglandins (PGs) are profound hormones in teleost sexual behavior, especially in mating. PGs act as pheromones that affect the olfactory sensory neurons of males, inducing the initiation of a series of mating behaviors. However, the molecular mechanism by which PGs trigger mating behavior in ovoviviparous teleosts is still unclear. In the present study, we employed the ovoviviparous black rockfish (Sebastes schlegelii), an economically important marine species whose reproductive production is limited by incomplete fertilization, as a model species. The results showed that when the dose of PGE₂ was higher than 10 nmol/L, a significant (P < 0.05) increase in mating behaviors was observed. Dual-fluorescence in situ hybridization indicated that PGE₂ could fire specific neurons in different brain regions and receptor cells in the olfactory sac. After combining with specific neurons in the central nervous system (CNS), a series of genes related to reproduction are activated. The intracerebroventricular administration of PGE₂ significantly increased lhb levels (P < 0.05) in both sexes. Moreover, steroidogenesis in gonads was also affected, inducing an increase (P < 0.05) in E₂ levels in males and T levels in females. PGE₂ levels were also increased significantly (P < 0.05) in both sexes. The present study revealed that PGE₂ can activate mating behavior in black rockfish in both hormone and pheromone pathways, leading to variations in sex steroid levels and activation of reproductive behaviors. Our results provide not only novel insight into the onset of mating behaviors in ovoviviparous teleosts but also solutions for the incomplete fertilization caused by natural mating in cage aquaculture.

Keywords

Black rockfish / Mating behavior / Ovoviviparity / Prostaglandin E2

References

[1] An HS, Park JY, Kim M-J, Lee EY, Kim KK. Isolation and characterization of microsatellite markers for the heavily exploited rockfish Sebastes schlegeli, and cross-species amplification in four related Sebastes spp. Conserv Genet, 2009, 10: 1969-1972,

[2] Appelt CW (1995) Female goldfish appear to release pheromonally-active-prostaglandins in urinary pulses. In: Proceedings of the fifth international symposium on the reproductive physiology of fish fishsymp95, Austin

[3] Bayley M, Nielsen JR, Baatrup E. Guppy sexual behavior as an effect biomarker of estrogen mimics. Ecotoxicol Environ Saf, 1999, 43: 68-73,

[4] Bjerselius R, Lundstedt-Enkel K, Olsén H, Mayer I, Dimberg K. Male goldfish reproductive behaviour and physiology are severely affected by exogenous exposure to 17 beta-estradiol. Aquat Toxicol, 2001, 53: 139-152,

[5] Björnsson BT, Einarsdóttir IE, Johansson M, Gong N. The impact of initial energy reserves on growth hormone resistance and plasma growth hormone-binding protein levels in rainbow trout under feeding and fasting conditions. Front Endocrinol, 2018, 9: 231,

[6] Blesson CS, Büttner E, Masironi B, Sahlin L. Prostaglandin receptors EP and FP are regulated by estradiol and progesterone in the uterus of ovariectomized rats. Reprod Biol Endocrinol, 2012, 10: 3,

[7] Carlson EJ, Georg GI, Hawkinson JE. Steroidal antagonists of progesterone- and prostaglandin E(1)-induced activation of the cation channel of sperm. Mol Pharmacol, 2022, 101: 56-67,

[8] Chung-Davidson Y-W, Huertas M, Li W. Breithaupt T, Thiel M. A review of research in fish pheromones. Chemical communication in crustaceans, 2011 New York Springer 467-482

[9] Clasadonte J, Sharif A, Baroncini M, Prevot V. Gliotransmission by prostaglandin E(2): a prerequisite for GnRH neuronal function?. Front Endocrinol, 2011, 2: 91,

[10] Cole KS, Stacey NE. Prostaglandin induction of spawning behavior in Cichlasoma bimaculatum (Pisces cichlidae). Horm Behav, 1984, 18: 235-248,

[11] Colman JR, Baldwin D, Johnson LL, Scholz NL. Effects of the synthetic estrogen, 17alpha-ethinylestradiol, on aggression and courtship behavior in male zebrafish (Danio rerio). Aquat Toxicol, 2009, 91: 346-354,

[12] Criscuolo-Urbinati E, Kuradomi RY, Urbinati EC, Batlouni SR. The administration of exogenous prostaglandin may improve ovulation in pacu (Piaractus mesopotamicus). Theriogenology, 2012, 78: 2087-2094,

[13] Davis TL, Bott RC, Slough TL, Bruemmer JE, Niswender GD. Progesterone inhibits oxytocin- and prostaglandin F2alpha-stimulated increases in intracellular calcium concentrations in small and large ovine luteal cells. Biol Reprod, 2010, 82: 282-288,

[14] Du Toit E, Browne L, Irving-Rodgers H, Massa HM, Fozzard N, Jennings MP, Peak IR. Effect of GPR84 deletion on obesity and diabetes development in mice fed long chain or medium chain fatty acid rich diets. Eur J Nutr, 2018, 57: 1737-1746,

[15] Fujimori C, Ogiwara K, Hagiwara A, Takahashi T. New evidence for the involvement of prostaglandin receptor EP4b in ovulation of the medaka, Oryzias latipes. Mol Cell Endocrinol, 2012, 362: 76-84,

[16] Gao T, Ding K, Song N, Zhang X, Han Z. Comparative analysis of multiple paternity in different populations of viviparous black rockfish, Sebastes schlegelii, a fish with long-term female sperm storage. Mar Biodivers, 2018, 48: 2017-2024,

[17] Gonçalves D, Costa SS, Teles MC, Silva H, Inglês M, Oliveira RF. Oestradiol and prostaglandin F2α regulate sexual displays in females of a sex-role reversed fish. Proc Biol Sci, 2014, 281: 20133070

[18] Goodson JL. The vertebrate social behavior network: evolutionary themes and variations. Horm Behav, 2005, 48: 11-22,

[19] Haldorson L, Love M. Maturity and fecundity in the rockfishes, Sebastes spp., a review. Mar Fish Rev, 1991, 53: 25-31

[20] Hallgren SL, Linderoth M, Olsén KH. Inhibition of cytochrome p450 brain aromatase reduces two male specific sexual behaviours in the male Endler guppy (Poecilia reticulata). Gen Comp Endocrinol, 2006, 147: 323-328,

[21] Harms PG, Ojeda SR, McCann SM. Prostaglandin involvement in hypothalamic control of gonadotropin and prolactin release. Science, 1973, 181: 760-761,

[22] Hong WS, Chen SX, Zhang QY, Zheng WY. Sex organ extracts and artificial hormonal compounds as sex pheromones to attract broodfish and to induce spawning of Chinese black sleeper (Bostrichthys sinensis Lacépède). Aquac Res, 2006, 37: 529-534,

[23] Juntti SA, Hilliard AT, Kent KR, Kumar A, Nguyen A, Jimenez MA, Loveland JL, Mourrain P, Fernald RD. A neural basis for control of cichlid female reproductive behavior by prostaglandin F2α. Curr Biol, 2016, 26: 943-949,

[24] Kennedy JH, Korn N, Thurston RJ. Prostaglandin levels in seminal plasma and sperm extracts of the domestic turkey, and the effects of cyclooxygenase inhibitors on sperm mobility. Reprod Biol Endocrinol, 2003, 1: 74,

[25] Kobayashi M, Sorensen PW, Stacey NE. Hormonal and pheromonal control of spawning behavior in the goldfish. Fish Physiol Biochem, 2002, 26: 71-84,

[26] Larsen MG, Hansen KB, Henriksen PG, Baatrup E. Male zebrafish (Danio rerio) courtship behaviour resists the feminising effects of 17alpha-ethinyloestradiol–morphological sexual characteristics do not. Aquat Toxicol, 2008, 87: 234-244,

[27] Leslie JF, Vrijenhoek RC. Genetic analysis of natural populations of Poeciliopsis monacha: allozyme inheritance and pattern of mating. J Hered, 1977, 68: 301-306,

[28] Liley N. The effects of estrogens and other steroids on the sexual behavior of the female guppy, Poecilia reticulata. Gen Comp Endocrinol, 1972, 3: 542-552,

[29] Liu Q, Wang X, Xiao Y, Zhao H, Xu S, Wang Y, Wu L, Zhou L, Du T, Lv X, Li J. Sequencing of the black rockfish chromosomal genome provides insight into sperm storage in the female ovary. DNA Res, 2019, 26: 453-464,

[30] Liu C, Yue S, Solarz J, Lee J, Li L. Improving the sexual activity and reproduction of female zebrafish with high testosterone levels. Sci Rep, 2021, 11: 3822,

[62] Luo Z, Dong J, Zhang Z, Xu X, Zhang X. Microsatellite-based parentage analysis of offspring conducted in different regions of the black rockfish (Sebastes schlegelii) ovary. JFSC, 2021, 28: 391-402 (In Chinese with English abstract)

[31] Lyu LK, Li JS, Wang XJ, Yao YJ, Li JF, Li Y, Wen HS, Qi X. Arg-vasotocin directly activates isotocin receptors and induces COX2 expression in ovoviviparous guppies. Front Endocrinol, 2021, 12,

[32] Lyu L, Wang R, Wen H, Li Y, Li J, Wang X, Yao Y, Li J, Qi X. Cyclooxygenases of ovoviviparous black rockfish (Sebastes schlegelii): cloning, tissue distribution and potential role in mating and parturition. Comp Biochem Physiol B Biochem Mol Biol, 2022, 257,

[33] Matsumoto Y, Yabuno A, Kiros S, Soyano K, Takegaki T. Changes in male courtship intensity and androgen levels during brood cycling in the blenniid fish Rhabdoblennius nitidus. J Ethol, 2012, 30: 387-394,

[34] Mori H, Nakagawa M, Soyano K, Koya Y. Annual reproductive cycle of black rockfish Sebastes schlegeli in captivity. Fish Sci, 2003, 69: 910-923,

[35] Munakata A, Kobayashi M. Endocrine control of sexual behavior in teleost fish. Gen Comp Endocrinol, 2010, 165: 456-468,

[36] Nash JP, Kime DE, Van der Ven LT, Wester PW, Brion F, Maack G, Stahlschmidt-Allner P, Tyler CR. Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environ Health Perspect, 2004, 112: 1725-1733,

[37] Peter RE, Billard R. Effects of third ventricle injection of prostaglandins on gonadotropin secretion in goldfish, Carassius auratus. Gen Comp Endocrinol, 1976, 30: 451-456,

[38] Piotrowska-Tomala KK, Jonczyk AW, Skarzynski DJ, Szóstek-Mioduchowska AZ. Luteinizing hormone and ovarian steroids affect in vitro prostaglandin production in the equine myometrium and endometrium. Theriogenology, 2020, 153: 1-8,

[39] Pradhan A, Olsson PE. Zebrafish sexual behavior: role of sex steroid hormones and prostaglandins. Behav Brain Funct, 2015, 11: 23,

[40] Saaristo M, Johnstone CP, Xu K, Allinson M, Wong BBM. The endocrine disruptor, 17α-ethinyl estradiol, alters male mate choice in a freshwater fish. Aquat Toxicol, 2019, 208: 118-125,

[41] Saaristo M, Craft JA, Tyagi S, Johnstone CP, Allinson M, Ibrahim KS, Wong BBM. Transcriptome-wide changes associated with the reproductive behaviour of male guppies exposed to 17α-ethinyl estradiol. Environ Pollut, 2021, 270,

[42] Saoshiro S, Kawaguchi Y, Hayakawa Y, Kobayashi M. Sexual bipotentiality of behavior in male and female goldfish. Gen Comp Endocrinol, 2013, 181: 265-270,

[43] Saper CB, Romanovsky AA, Scammell TE. Neural circuitry engaged by prostaglandins during the sickness syndrome. Nat Neurosci, 2012, 15: 1088-1095,

[44] Schulz RW, de França LR, Lareyre JJ, Le Gac F, Chiarini-Garcia H, Nobrega RH, Miura T. Spermatogenesis in fish. Gen Comp Endocrinol, 2010, 165: 390-411,

[45] Sorensen PW, Hara TJ, Stacey NE, Goetz FW. F prostaglandins function as potent olfactory stimulants that comprise the postovulatory female sex pheromone in goldfish. Biol Reprod, 1988, 39: 1039-1050,

[46] Stacey NE. Hormonal regulation of female reproductive behavior in fish. Am Zool, 1981, 21: 305-316,

[47] Stacey NE, Sorensen PW (2011) Hormonally derivedsex pheromones in fish. In: Rocha MJ, Arukwe A, Kapoor BG (eds) Fish reproduction. Science Publishers, Enfield, pp 169–1924

[48] Stacey N, Chojnacki A, Narayanan A, Cole T, Murphy C. Hormonally derived sex pheromones in fish: exogenous cues and signals from gonad to brain. Can J Physiol Pharmacol, 2003, 81: 329-341,

[49] Takahashi T, Hagiwara A, Ogiwara K. Prostaglandins in teleost ovulation: a review of the roles with a view to comparison with prostaglandins in mammalian ovulation. Mol Cell Endocrinol, 2018, 461: 236-247,

[50] Tang H, Liu Y, Li J, Li G, Chen Y, Yin Y, Guo Y, Cheng CH, Liu X, Lin H. LH signaling induced ptgs2a expression is required for ovulation in zebrafish. Mol Cell Endocrinol, 2017, 447: 125-133,

[51] Volkoff H, Peter RE. Actions of two forms of gonadotropin releasing hormone and a GnRH antagonist on spawning behavior of the goldfish Carassius auratus. Gen Comp Endocrinol, 1999, 116: 347-355,

[52] Wang X, Wen H, Li Y, Lyu L, Song M, Zhang Y, Li J, Yao Y, Li J, Qi X. Characterization of CYP11A1 and its potential role in sex asynchronous gonadal development of viviparous black rockfish Sebastes schlegelii (Sebastidae). Gen Comp Endocrinol, 2021, 302,

[53] Wingfield JC, Hegner RE, Dufty AM Jr, Ball GF. The "challenge hypothesis": theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat, 1990, 136: 829-846,

[54] Wong RY, Ramsey ME, Cummings ME. Localizing brain regions associated with female mate preference behavior in a swordtail. PLoS ONE, 2012, 7,

[55] Yabuki Y, Koide T, Miyasaka N, Wakisaka N, Masuda M, Ohkura M, Nakai J, Tsuge K, Tsuchiya S, Sugimoto Y, Yoshihara Y. Olfactory receptor for prostaglandin F2α mediates male fish courtship behavior. Nat Neurosci, 2016, 19: 897-904,

[56] Yambe H, Munakata A, Kitamura S, Aida K, Fusetani N. Methyltestosterone induces male sensitivity to both primer and releaser pheromones in the urine of ovulated female masu salmon. Fish Physiol Biochem, 2003, 28: 279-280,

[57] Yao Y, Wen H, Lyu L, Wang X, Li J, Xie S, Zuo C, Yan S, Wang Z, Qi X. Gnih/gnihr regulates the expression of genes related to mating behavior in ovoviviparous black rockfish (Sebastes schlegelii). Acta Hydrobiol Sin, 2023, 47: 1-16 in Chinese with English abstract

[58] Yoshida K. Pedigree tracing of a hatchery-reared stock used for aquaculture and stock enhancement based on DNA markers. Fish Genet Breed Sci, 2001, 30: 27-35

[59] Young K, Morrison H. Quantifying microglia morphology from photomicrographs of immunohistochemistry prepared tissue using ImageJ. J vis Exp, 2018, 136: 57648

[60] Zhang YT, Hong WS, Qiu HT, Wang Q, Chen SX. Androgen induces olfactory expression of prostaglandin E2 receptor Ep1 in the burrow-living fish Bostrychus sinensis. J Steroid Biochem Mol Biol, 2019, 188: 156-165,

[61] Zhao H, Wang X, Du T, Gao G, Wu L, Xu S, Xiao Y, Wang Y, Liu Q, Li J. Sperm maturation, migration, and localization before and after copulation in black rockfish (Sebastes schlegelii). Theriogenology, 2021, 166: 83-89,