TRENDS IN COMPARATIVE ENDOCRINOLOGY AND NEUROBIOLOGY
Hormonal and Environmental Control of Puberty in Perciform Fish The Case of Sea Bass M. Carrillo, S. Zanuy, A. Felip, M. J. Bayarri, G. Mol´es, and A. Gomez ´ Consejo Superior de Investigaciones Cientificas, Instituto de Acuicultura de Torre de la Sal, Torre de la Sal, Spain A specific chronology for puberty and changes at the brain–pituitary–gonad axis for sea bass are reviewed. Recent findings demonstrate that the Kisspeptin system, gonadotropin releasing hormones, follicle stimulating hormone, 11-ketotestosterone, and leptin are potential candidates for the onset of puberty of this fish species, stressing the importance of the daily and annual rhythms of some of these hormones. Environmental control of puberty is also reviewed, specifically the manipulations of constant photoperiods for altering or even suppressing the onset of puberty in sea bass. Recently, a possible narrow sensitive period for suppressing gonadogenesis in sea bass has been identified. Key words: puberty; precocity; hormonal regulation; photoperiod control; sea bass
Introduction When and how puberty can be controlled in fish is of particular interest for understanding some basic mechanisms underlying this process and for its application in aquaculture to advance or delay puberty in cultivated species. Puberty occurs some time after sexual differentiation and is characterized by the capacity of fish to reproduce for the first time in its life; spermatocytes or oocytes are produced at the onset of this process, which further culminates with the first spermiation and ovulation in males and females, respectively.1 Anticipated puberty (precocity) is a common feature in some male fish; it generally occurs 1 year earlier than in those fish where puberty is attained normally. A series of reproductive hormones, i.e., gonadotropin releasing hormone (GnRH), follicle stimulating hormone (FSH), luteinizing horAddress for correspondence: M. Carrillo, CSIC-Instituto de Acuicultura de Torre de la Sal, Ribera de Cabanes, 12595, Torre de la Sal, Spain. Voice: 34-964319500; fax: 34-964319509. [email protected]
mone (LH), and 11-ketotestosterone (11-KT), increase during the year preceding puberty, despite fish exhibiting very poorly developed gonads; this occurs at the time when gonadal development and maturation occurs in adult fish. However, hormonal levels are currently lower in precocious fish than those exhibited by pubertal or broodfish,2–5 which suggests that the limiting factor for the onset of puberty may occur at the gonad level, i.e., gonadotropin (GTH) receptors or steroideogenic enzymes. In mammals, GTH secretion is controlled by changes in pulsatile release of GnRH increasing at puberty in a diurnal fashion, which is prompted by changes in trans-synaptic and glial inputs to the GnRH neuronal network.6 This suggests that the onset of puberty depends on the contribution of a gene network of a hierarchical nature.7 Notwithstanding, the fundamental mechanism underlying the onset of puberty has not yet been elucidated in any vertebrate, and the information becomes remarkably scarce in fish particularly when comparing with the achievements attained in mammals.1,8–11 Besides, these
Trends in Comparative Endocrinology and Neurobiology: Ann. N.Y. Acad. Sci. 1163: 49–59 (2009). C 2009 New York Academy of Sciences. doi: 10.1111/j.1749-6632.2008.03645.x
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Figure 1. Schematic representation of the chronology of puberty in sea bass and terms used. In this species the female fish differentiates earlier than the male fish, but the male fish attains puberty 1 year earlier than the female fish. In a certain percentage of individuals, an early activation (tentative) of the brain– pituitary–gonad axis occurs one year before puberty is attained, giving rise to the precocious fish (early puberty). These fish are able to produce gametes, although in a small amount and having low quality.
mechanisms are likely to differ among the different species of teleost, which is the largest taxon among the vertebrates. In this work, we review the state of the art of puberty in sea bass and also discuss future directions for research in this matter. Importance of the Species The European sea bass (Dicentrarchus labrax L.) is a highly valuable species for aquaculture, representing 40% of the annual marine fish production of the Mediterranean aquaculture industry.12 However, some problems, linked to the reproductive biology of this species, limit its production. Puberty occurs at 3 years in female fish whereas it is attained at 2 years in male fish.13 Under intensive culture conditions 20– 30% of males mature precociously in the first year of life and generally precocious fish being
larger than nonprecocious ones.14 However, in the second annual cycle, precocious male fish weigh up to 18% less and are 5% less in fork length than nonprecocious fish.15 Overall, male fish exhibit 20–40% less body weight at harvest time than female fish (around 18–22 months of age); this is likely induced by the earlier onset of puberty, which drives energy toward gonadogenesis and breeding behavior instead of somatic growth.13 In addition, most aquaculture institutions and Mediterranean fish farms may show extremely high percentages sex ratios skewed to males (70–90%).13 We have also observed early puberty in female fish, and this will likely have important effects on aquaculture production of large adult fish (royal and imperial sea bass), although more detailed studies are needed to confirm all these aspects. Control of puberty in sea bass is becoming an important issue for practical reasons and also to understand the basic mechanisms that control the start
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of reproduction in nonmammalian vertebrates. Figure 1 summarizes the chronology of puberty in sea bass and illustrate the concept of puberty and other related terms in relation to the stages of gonadal maturation including the first three consecutive years of life of this specie. The Role of the Brain–Pituitary–Gonad Axis during Puberty The vertebrate reproduction process is regulated by a hormonal cascade throughout the brain–pituitary–gonad axis, which is activated at the onset of puberty. In mammals, the commencement of puberty is characterized by a pulsatile secretion of GnRH that prompts the synthesis and secretion (also pulsatile) of gonadotropins (GTHs): LH and FSH. These in turn stimulate the gonads, inducing gametogenesis and steroid production until full maturation and functionality at puberty.16 Despite the importance of the activation of the GnRH system, which seems to be the key element for the onset of puberty,11 no data on pulsatile secretion of GnRH are available in teleosts, mainly because in these fish GnRH neurons innervate the pituitary directly. Kiss1/Kiss1R The identification of the role of kisspeptins (Kiss1s) a family of a RFamide peptides encoded by the Kiss1 gene and their putative receptor G-protein-coupled receptor Kiss1 receptor (Kiss1R; previously designated Gprotein-coupled receptor 54, GPR54) in the neuroendocrine regulation of reproduction in mammals have revolutionized the understanding of the mechanisms responsible for the control of the reproductive axis. Presently, the KiSS-1/GPR54 system is considered as the gatekeeper of GnRH allowing integration of central and peripheral signals, playing the GnRH a central role in the control of the reproductive function, including the ability to di-
rectly activate the GnRH neurons to secrete GnRH and to enhance the GTH release by the pituitary gland in several species of vertebrates. The hypothalamic Kiss1 system is considered a key element for relaying both positive and negative feedback inputs of sex steroids to GnRH neurons. Finally, a pivotal role of the Kiss1 system in timing puberty onset in mammals has been demonstrated.17 In fish, the potential role of kisspeptins in the control of reproduction remains largely unexplored. Only recently, the putative Kiss1 sequences in five teleost genomes, i.e., zebrafish, fugu, tetraodon, medaka, and sea lamprey, and the anatomical distribution of Kiss1 mRNA-expressing neurones in the brain of medaka have been identified.18,19 Cloning of Kiss1R in fathead minnow, tilapia, grey mullet, and cobia has been achieved,20–23 showing a high degree of conservation of the amino acid sequences and supporting that the Kiss1/Kiss1R system is a feature that all vertebrates conserved during evolution. These studies have also proved that GnRH cells are direct targets of kisspeptins, which induce GnRH release at puberty throughout interactions with their cognate receptor Kiss1R, as occurs in mammals. An increase of Kiss1R expression levels in the brain of tilapia at the onset of puberty, which later on decreases by exposure to continuous light, has also been reported.24 These results suggest that the transcriptional mechanisms regulating Kiss1R expression could be influenced by light, opening the possibility that the Kiss1/Kiss1R system might mediate the photoperiodic control of reproduction in teleosts, as has been proposed for mammals.25 Sequencing analysis of two complete complementary (c)DNA sequences obtained from a sea bass brain cDNA library indicated that two Kiss1-like genes exist in this species. Both genes show a marked expression in the brain and gonadal tissues of pubertal sea bass, although expression in other tissues is also observed.26 Functional activity of the two Kiss1-like genes has been examined in several in vivo experiments based on the effect of their administration on GTH secretion in
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prepubertal sea bass. Results have evidenced that both kisspeptins stimulated LH and FSH secretion, although Kiss2 shows a more noticeable response in the activation than that of Kiss1.26 Likewise, two Kiss1R genes have been characterized in sea bass, and their tissue expression analysis revealed that both are mainly expressed in brain, pituitary, testis, and ovary.27 The presence of the Kiss1/Kiss1R system in the brain of sea bass provides a solid base to perform further studies to demonstrate the claimed central role on the control of puberty and thus reproductive function as shown in other teleost species and mammals. GnRH System Evidence of participation of GnRH systems in puberty in sea bass was shown by Rodr´ıguez et al.4 who reported a high and a moderate sea bream (sb)GnRH and salmon (s)GnRH pituitary content, respectively, at the onset of puberty. Later, three different GnRH cDNAs were characterized in the brain of sea bass, using riboprobes corresponding to the GAP regions that generate three GnRH decapeptides: sbGnRH, sGnRH, and chicken II GnRH (cGnRH-II).28,29 These authors recognized sbGnRH and, on a minor scale, sGnRH as the main hypophysiotropic isoforms. In addition, five GnRH receptors have been cloned and characterized in sea bass and all of them were functional and presented a strong affinity for cGnRH-II. However, only one of these receptors (dlGnRHR-II.1A), strongly expressed in the pituitary GTH cells, showed affinity for sbGnRH and sGnRH.30 In prepubertal female red sea bream, continuous GnRH treatment resulted in precocious induction of female puberty. Moreover, this treatment stimulated a sustained LH release from the pituitary, as observed in other teleost species, and upregulated the expression of GnRHR receptor (GnRHR) and the three GTH subunit genes.31 Similarly, a long-term release of plasma LH in sea bass was obtained in male fish after treatment with GnRH analog (GnRHa) sustained-
release delivery systems.32 Nevertheless, injections of GnRHa did not increase FSHβ gene expression but stimulated LHβ and Glyco protein alpha (GPα) subunit mRNA in nonmature adult sea bass previously implanted with testosterone and estradiol (E 2 ).33 Similar results were observed in postpubertal resting female sea bream, suggesting the possibility that regulation of FSHβ gene expression by GnRH differs with species, season, or age.31 Finally, a peak of sbGnRH brain expression correlating with a peak of pituitary FSHβ gene expression was observed at sex differentiation, a period that precedes gametogenesis at early puberty during the first year of life of sea bass,34 suggesting the possibility that the activation of the brain GnRH system could trigger both the sex differentiation and the onset of puberty in sea bass. Gonadotropins Pulsatile pre-ovulatory LH secretion has been described in sea bream,35 and recently nocturnal rises of LH plasma levels, during the early puberty of sea bass, were reported by Bayarri et al.36 as signals for the oncoming spawning period. However, when a reproductive inhibitory photoperiod treatment (i.e., continuous light) was applied, the nocturnal LH peak was eliminated as well as the gonadal maturation processes37 (Fig. 2). These results suggest that the pulsatile secretion of LH could be important to trigger puberty in sea bass. Nocturnal elevations of plasma LH in sea bass are comparable to those observed in humans where pulsatile GTH secretion starting from a nonpulsatile base line progresses to a sleepentrained nocturnal increase in LH during early to mid puberty and is lost at the end of this period.38 It has been suggested that FSH could have a key role both in sex differentiation and at early stages of gonadal development in prepubertal sea bass.34 The recent purification and characterization of the biological actions of sea bass FSH39 provides further support that FSH could be acting at early stages
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Figure 2. Effects of continuous light (LL) on the inhibition of the nocturnal luteinizing hormone (LH) plasma peaks specifically during November (spermatogenesis) and February (full spermiation). Origin of data is from Ref. 36 and unpublished results. Abbreviations: spgA, spermatogonia A; spgB, spermatogonia B; spc1, spermatocytes 1; spz, spermatozoids.
of gametogenesis by promoting the synthesis of sexual steroids involved in spermatogonial proliferation in male fish40 and progression of vitellogenesis in female fish,41 as reported for other teleosts. Sexual Steroids It has been stated that testosterone downregulates FSH release from the pituitary gland and acts on the gonads as a stem cell renewal stimulating factor throughout its conversion to E 2 in male fish42,43 and oogonial proliferation in female fish.44 11-KT, the major androgen produced in the testicles of teleost fish, stimulates the Sertoli cells to produce growth factors and promotes spermatogonial proliferation leading to meiosis and later stages of spermatogenesis.45 It has also been suggested that 11KT could exert an effective regulation on the
positive-feedback mechanisms on sbGnRH expression levels in the brain of Pagrus major, providing an important role in the reproductive cycles of the male sea bream.1 These facts provide support that sexual steroids can be postulated for the regulation of the neuronal GnRH system in teleosts. Evidence has been put forward that 11-KT can be considered as a firm candidate for the regulation of the onset of puberty in teleosts.46,47 In prepubertal male sea bass, 11-KT is able to induce spermatogenesis; in fact, we have shown that exogenous administration of 11-KT (not testosterone) to continuous light-exposed fish (see below) allows the testis to recover active spermiogenesis capacity, inducing significant increases of pituitary LHβ gene expression and pituitary and plasma LH levels. This suggests that 11-KT plays a key role in the control of the first spermatogenesis and spermiogenesis in sea bass.48
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Figure 3. Close relationship between the average weight of the whole population of early maturing male sea bass and the further rates of precocity. Mean size of precocious male sea bass is approximately 144.2 ± 10.7 g. Asterisks represent significant differences between fish of the same population (P ≥ 0.05). Origin of data: (a),14 (b),67 and (c) (unpublished results).
Leptin In vertebrates, puberty is attained when individuals reach a certain age/size and accumulate the necessary energy stores to guarantee a successful reproduction. To initiate puberty precise informative environmental signals are required to trigger this process. Fish exhibit marked seasonal biological functions, such as growth and reproduction, that occur at separate periods of the year. The period of high food intake, which generally parallels enhanced growth rates, is negatively correlated with gonadal growth; this happens also in sea bass.49 This inverse correlation between food intake and gonadal growth, common in teleosts, suggests that nutritional status could be involved in the modulation of the reproductive axis. It has been hypothesized that the first gonadal maturation, a high energetically demanding process, is only allowed in those virgin fish that attain a certain degree of somatic growth or
a threshold of energy reserves.50 Early maturing male sea bass have a significantly higher weight, size, and condition factor than nonprecocious ones.14 The rate of precocious male growth decreases according to the total weight or length attained at the time of first maturation, supporting this hypothesis (Fig. 3). The relationship between body weight and fertility that integrates body weight and food intake as puberty-initiating factors has been known for decades in mammals. However, only recently peripheral signals and neuroendocrine networks that integrate energy balance and reproduction have been identified.51 Cloning of leptin in 1994 was the major breakthrough for understanding the mechanisms underlying reproduction and metabolism. Leptin, secreted by white adipose tissue, is considered as a satiety factor in the regulation of body weight in mammals. Leptin also has a role in the control of reproduction by its action in the hypothalamus involving GnRH release, which in
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Figure 4. Screening of the critical period for inhibition of early puberty by LL exposure at selected periods between the summer and winter solstice, coinciding with photoperiodic reduction.
turn regulates pulsatile LH secretion, suggesting that leptin may play a permissive role in the onset of puberty in mammals.52 In teleost fish, leptin function has been largely ignored and its characterization is very recent, i.e., in puffer fish53,54 and in rainbow trout.55 Physiological evidence for the involvement of leptin in the regulation of reproductive function in teleosts comes from research that mammalian leptin (bovine) stimulates the release of luteinizing hormone56 and somatolactin57 in sea bass and that a high concentration of human leptin stimulates in vitro release of pituitary FSH and LH in female rainbow trout.58 In the ayu,59 a clear correlation between immunoreactive leptin (Ir-leptin) values, rising levels of E 2 , and an increase of prolactin secretion at maturity was found. The recent availability of recombinant leptin55,59 in some teleost species will help researchers understand the likely participation of this hormone in the control of puberty in fish. Environmental Control of Puberty Puberty, being a particular stage of the overall reproductive process of fish, could share the same mechanism of action and morphologi-
cal bases of the neuro-endocrine system, which participates in the transduction and translation of environmental signals in the adult fish. Similarly, the effects of environmental manipulation on altering spawning time in adults may also be effective in pubertal fish. The onset of puberty in rainbow trout is advanced by using compressed or constant long photoperiods.60,61 Similarly, compressed photoperiod advances the first sexual maturation in sea bass,62 whereas constant long days produce a delay.63 Continuous illumination (LL) is becoming an important tool for research and aquaculture industry operations of species, such as Atlantic salmon,64 sea bass,65 Senegalensis sole,66 and cod.67,68 These studies suggested that the key environmental signal for the recruitment of individuals that enter the sexual maturation cycle is the autumnal decrease of photoperiod. If this signal is masked by continuous light exposure, reproductive activity becomes completely inhibited, as evidenced in cod.67 The first evidence of the LL effects on gonadal maturation in sea bass was obtained by Begtashi et al.65 These authors reported that juvenile fish exposed to LL throughout a year show a drastic reduction in the rates that the male fish enter
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early puberty (0–3% treated fish versus 22% in controls). Recently, Felip et al.15 showed that shorter LL treatments, lasting 4 or 6 months during pregametogenesis and gametogenesis periods, respectively, resulted in similar rates of precocity to those fish maintained under LL all year. This study suggests that a “critical” period to LL exposure may be placed somewhere between both treatments. The study of the endocrine mechanisms underlying LL treatment in sea bass have revealed that plasma levels of 11-KT are very low or unbalanced and the three sea bass GTH subunit gene expression levels are either drastically reduced or differentially regulated, particularly FSH. These results suggest that the reduced or unbalanced production of this androgen, likely regulated by FSH, may be a limiting factor for germinal cell proliferation and entering into meiosis, consequently arresting the onset of early puberty. These studies paved the way for screening the period August–November with LL windows of short duration (2 months) to find a critical period that effectively blocks gametogenesis in sea bass69 (Fig. 4).
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Sea bass original data were obtained through European Union (EU) #Q5RS-2002– 01801 (PUBERTIMING), Ministery of Education and Science (MEC) (AGL2000-12470E, AGL200500796 and AGL200604672), and Generalitat Valenciana (GV) (ACOMP07262 and GV06/268) grants. Conflicts of Interest
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