Intersex, Hermaphroditism, and Gonadal Plasticity in Vertebrates: Evolution of the Müllerian Duct and Amh/Amhr2 Signaling

Adolfi, Mateus Contar; Nakajima, Rafael T.; Nóbrega, Rafael Henrique; Schartl, Manfred

doi:10.1146/annurev-animal-020518-114955

Cited by 69 publications

(68 citation statements)

References 102 publications

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“…www.nature.com/scientificreports www.nature.com/scientificreports/ However, sequential hermaphroditism is an evolutionary unstable state as it reverts quickly back to gonochorism, suggesting that both types of sequential hermaphroditism are costlier to sustain than gonochorism. These results may explain why, despite hermaphroditism being anatomically and physiologically possible in fish in contrast to other vertebrates 75 , gonochorism predominates among fishes 64 . Female has been often considered the 'default sex' in fishes because, even in some gonochoristic species, all individuals, exhibit ovarian differentiation at the early stages of development, a process that is subsequently halted in the individuals that become males 63,76 .…”

Section: Discussionmentioning

confidence: 93%

A phylogenetic comparative analysis on the evolution of sequential hermaphroditism in seabreams (Teleostei: Sparidae)

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Benvenuto

Capellini

et al. 2020

Sci Rep

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systems, particularly for both types of sequential hermaphroditism, given that it contains many gonochoristic, protogynous and protandrous species, with differences in sexual systems even between species belonging to the same genus. The main theoretical framework to explain the evolutionary advantage of sequential hermaphroditism based on sex allocation theory is the size-advantage model (SAM) 9,19-21. The SAM proposes that individuals should switch sex when the second sex achieves a greater fitness at a larger body size than the first sex, thus increasing lifetime fitness 22. When larger males have higher reproductive success than smaller males and similar sized females, fish should reproduce initially as female and change later to male (protogyny) 19,23,24. Conversely, protandry is expected when large females have greater fitness than smaller females and similar sized males 19,20. Empirical studies support this model in several fish families, explaining quantitatively the size or age at which an individual should change sex, as well as the overall population sex ratio 25,26. Typically, male-biased sex ratios are observed in populations of protandrous species, while female-biased sex ratios are observed in populations of protogynous species, especially in haremic groups 19,26,27. Mating systems (the number and social dominance of mates involved) and spawning mode (i.e., group spawning, where several males spawn with one or several females, or pair-mating, where a single male spawns with a single female), determine the fitness that a fish of a given size can achieve as a female or as a male 23,28. Fish mating systems range from monogamy or pair-mating, to harem polygyny (one dominant male controls access to multiple females 29), lek-type polygyny (temporary harems 25), and large polygamous or promiscuous aggregations (where group spawning occurs 30). Sperm competition is particularly intense in large aggregations with multiple males 31,32 while it is absent in monogamy and pair-mating, and low in polygynous mating systems. Sperm competition and spawning modes have been used to infer mating systems 33-35 , which are relevant when testing the predictions of SAM since they can generate sex-specific differences in reproductive expectations 23,24,36,37. Thus, the first study that tested the predictions of SAM incorporating the mating system in a phylogenetic context focused on the evolution of protogynous groupers according to pair spawning mode 35. Indeed, protandry should be favored when sperm competition is low (mating occurs between members of monogamous or random pairs 19,22-24), and mate monopolization by large males should occur in protogynous species 23. Even though sperm competition was not included in the original formulation of the model 9,19 , it was subsequently mentioned as absent in protogyny 21,23,24,38 , limited in protandry (considered typical of random pairing and small groups) 22,23 and high in gonochorism (when mating occurs in large groups) 21,23,35,39. The influence of sperm competition on sex c...

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Section: Discussionmentioning

confidence: 93%

A phylogenetic comparative analysis on the evolution of sequential hermaphroditism in seabreams (Teleostei: Sparidae)

Pla

Benvenuto

Capellini

et al. 2020

Sci Rep

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“…Most studies on teleost Amh regulation come from zebrafish, where FSH was found to down-regulate amh expression in adult testis (19,23,24). While models for these regulatory networks have been proposed, the target genes of Amh are still mostly unknown (25,26).…”

Section: Introductionmentioning

confidence: 99%

An ex vivo Approach to Study Hormonal Control of Spermatogenesis in the Teleost Oreochromis niloticus

et al. 2020

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As the male reproductive organ, the main task of the testis is the production of fertile, haploid spermatozoa. This process, named spermatogenesis, starts with spermatogonial stem cells, which undergo a species-specific number of mitotic divisions until starting meiosis and further morphological maturation. The pituitary gonadotropins, luteinizing hormone, and follicle stimulating hormone, are indispensable for vertebrate spermatogenesis, but we are still far from fully understanding the complex regulatory networks involved in this process. Therefore, we developed an ex vivo testis cultivation system which allows evaluating the occurring changes in histology and gene expression. The experimental circulatory flow-through setup described in this work provides the possibility to study the function of the male tilapia gonads on a cellular and transcriptional level for at least 7 days. After 1 week of culture, tilapia testis slices kept their structure and all stages of spermatogenesis could be detected histologically. Without pituitary extract (tilPE) however, fibrotic structures appeared, whereas addition of tilPE preserved spermatogenic cysts and somatic interstitium completely. We could show that tilPE has a stimulatory effect on spermatogonia proliferation in our culture system. In the presence of tilPE or hCG, the gene expression of steroidogenesis related genes (cyp11b2 and stAR2) were notably increased. Other testicular genes like piwil1, amh, or dmrt1 were not expressed differentially in the presence or absence of gonadotropins or gonadotropin containing tilPE. We established a suitable system for studying tilapia spermatogenesis ex vivo with promise for future applications.

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“…On the other hand, cortisol significantly increased the transcript level of amh (anti-Müllerian hormone) after 7 days of culture. Amh, a member of transforming growth factor β, is expressed in Sertoli cells [77,80], and exerts an important role in spermatogonial proliferation and differentiation, as reported in zebrafish and other fish species [80]. Moreover, studies have shown that Amh inhibits spermatogonial proliferation and differentiation in zebrafish testis [66,77,81].…”

Section: Discussionmentioning

confidence: 87%

Cortisol Directly Stimulates Spermatogonial Differentiation, Meiosis, and Spermiogenesis in Zebrafish (Danio rerio) Testicular Explants

et al. 2020

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Cortisol is the major endocrine factor mediating the inhibitory effects of stress on vertebrate reproduction. It is well known that cortisol affects reproduction by interacting with the hypothalamic–pituitary–gonads axis, leading to downstream inhibitory and stimulatory effects on gonads. However, the mechanisms are not fully understood. In this study, we provide novel data demonstrating the stimulatory effects of cortisol on spermatogenesis using an ex vivo organ culture system. The results revealed that cortisol treatment did not modulate basal androgen production, but it influenced transcript levels of a selected number of genes involved in the zebrafish testicular function ar (androgen receptor), star (steroidogenic acute regulatory), cyp17a1 (17α-hydroxylase/17,20 lyase/17,20 desmolase), cyp11a2 (cytochrome P450, family 11, subfamily A, polypeptide 2), hsd11b2 (11-beta hydroxysteroid dehydrogenase), cyp2k22 (cytochrome P450, family 2, subfamily K, polypeptide 22), fkbp5 (FKBP prolyl isomerase 5), grα (glucocorticoid receptor alpha), and grβ (glucocorticoid receptor beta) in a short-term culture. We also showed that cortisol stimulates spermatogonial proliferation and differentiation in an androgen independent manner as well as promoting meiosis and spermiogenesis by increasing the number of spermatozoa in the testes. Moreover, we demonstrated that concomitant treatment with RU 486, a potent glucocorticoid receptor (Gr) antagonist, did not affect the cortisol effects on spermatogonial differentiation but blocked the induced effects on meiosis and spermiogenesis. Supporting the Gr-mediated effects, RU 486 nullified the cortisol-induced expression of sycp3l (synaptonemal complex protein 3), a marker for the meiotic prophase that encodes a component of the synaptonemal complex. This is consistent with in silico analysis that found 10 putative GREs (glucocorticoid response elements) upstream of the zebrafish sycp3l. Finally, we also showed that grα mRNA is expressed in Sertoli and Leydig cells, but also in several types of germ cells, including spermatogonia and spermatocytes. Altogether, this evidence indicates that cortisol exerts paracrine roles in the zebrafish testicular function and spermatogenesis, highlighting its effects on spermatogonial differentiation, meiosis, and spermiogenesis.

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Intersex, Hermaphroditism, and Gonadal Plasticity in Vertebrates: Evolution of the Müllerian Duct and Amh/Amhr2 Signaling

Cited by 69 publications

References 102 publications

A phylogenetic comparative analysis on the evolution of sequential hermaphroditism in seabreams (Teleostei: Sparidae)

A phylogenetic comparative analysis on the evolution of sequential hermaphroditism in seabreams (Teleostei: Sparidae)

An ex vivo Approach to Study Hormonal Control of Spermatogenesis in the Teleost Oreochromis niloticus

Cortisol Directly Stimulates Spermatogonial Differentiation, Meiosis, and Spermiogenesis in Zebrafish (Danio rerio) Testicular Explants

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