Origin and Evolution of the Neuroendocrine Control of Reproduction in Vertebrates, With Special Focus on Genome and Gene Duplications

Abstract

In humans, as in the other mammals, the neuroendocrine control of reproduction is ensured by the brain-pituitary gonadotropic axis. Multiple internal and environmental cues are integrated via brain neuronal networks, ultimately leading to the modulation of the activity of gonadotropin-releasing hormone (GnRH) neurons. The decapeptide GnRH is released into the hypothalamic-hypophysial portal blood system and stimulates the production of pituitary glycoprotein hormones, the two gonadotropins luteinizing hormone and follicle-stimulating hormone. A novel actor, the neuropeptide kisspeptin, acting upstream of GnRH, has attracted increasing attention in recent years. Other neuropeptides, such as gonadotropin-inhibiting hormone/RF-amide related peptide, and other members of the RF-amide peptide superfamily, as well as various nonpeptidic neuromediators such as dopamine and serotonin also provide a large panel of stimulatory or inhibitory regulators. This paper addresses the origin and evolution of the vertebrate gonadotropic axis. Brain-pituitary neuroendocrine axes are typical of vertebrates, the pituitary gland, mediator and amplifier of brain control on peripheral organs, being a vertebrate innovation. The paper reviews, from molecular and functional perspectives, the evolution across vertebrate radiation of some key actors of the vertebrate neuroendocrine control of reproduction and traces back their origin along the vertebrate lineage and in other metazoa before the emergence of vertebrates. A focus is given on how gene duplications, resulting from either local events or from whole genome duplication events, and followed by paralogous gene loss or conservation, might have shaped the evolutionary scenarios of current families of key actors of the gonadotropic axis.

Fish reproductive biology – Reflecting on five decades of fundamental and translational research

“…In the 1977 Paimpont 1st ISRPF meeting, a very productive collaboration between Dick Peter, Larry Crim and Henk Goos provided the first evidence for the existence of a gonadotropin release inhibitory factor (GRIF) in the brain of goldfish (Peter and Crim, 1979;Peter et al, 1978). Many follow-up studies led by Dick Peter, his past graduate students John Chang and Hamid Habibi, as well as Olivier Kah, Sylvie Dufour and others, have identified GRIF as dopamine, which was later confirmed in all studied cyprinid fish and a handful of other fish species (reviewed by Dufour et al, 2020). As presented by Dick Peter, Hao-Ren Lin and Glen Van Der Kraak at the 3rd ISRPF in 1987, in broodstock of such fish, LH release, FOM, ovulation and spawning can only be induced by the administration of both GnRHa and dopamine antagonists (Peter et al, 1988).…”

“…From then on, led by young (and now young in spirit) stars like Penny Swanson, Sylvie Dufour, Abigail Elizur and Berta Sivan, several groups purified and characterized fish FSH and LH and cloned their genes, a process that was rapidly applied to multiple fish species once PCR amplification technology was implemented (Elizur et al, 1996), negating the need for the collection of thousands of pituitaries for the synthesis and screening of the traditional cDNA libraries. This progress, together with the production of recombinant LH and FSH hormones, paved the way for studying the GtHs' respective functions, evolution, annual and daily patterns, receptors, structure-function, mechanisms of action, and regulation of their synthesis and secretion at the hormonal and molecular levels (Dufour et al, 2020;Guzmán et al, 2014;Levavi-Sivan et al, 2010;Rocha et al, 2009;Swanson et al, 2003;Dickey and Swanson, 2000;Swanson et al, 1991). In vivo and in vitro studies demonstrated the importance of FSH in the control of earlier stages of gametogenesis, spermatogenesis in males, and oogenesis in females.…”

“…The OB/TN GnRH3 has been implicated in transducing external cues, such as olfaction and social information (pheromones) to reproductive processes (Ueda et al, 2016;Munoz-Cueto 2020). Additionally, the multiplicity of GnRHs across fish and vertebrate species has raised many interesting evolutionary questions that were addressed by several excellent reviews (Okubo and Nagahama, 2008;Kah et al, 2007;Roch et al, 2011Roch et al, , 2014Lovejoy et al, 2018;Choi 2018;Umatani and Oka, 2019;Dufour et al, 2020;Kah, 2020;Munoz-Cueto et al, 2001;Trudeau and Somoza, 2020).…”

Cell Communications among Microorganisms, Plants, and Animals: Origin, Evolution and Interplays

“…For example, in cnidarians (medusae, corals), there is no endocrine gland, but the diffuse neurons secrete neuromediators and molecules that are chemicaly related to vertebrate hormones such as steroids, melatonin or GnRH [153]. During the Evolution, the endocrine system has gained in complexity in all invertebrates but even more in vertebrates due to the dual duplication of entire genome at the root of vertebrates' radiation, and to the emergence of the pituitary as an integrator of an important part of endocrine functions [154][155][156].…”

Cell Communications among Microorganisms, Plants, and Animals: Origin, Evolution and Interplays

“…For example, in cnidarians (medusae, corals), there is no endocrine gland, but the diffuse neurons secrete neuromediators and molecules that are chemically related to vertebrate hormones such as steroids, melatonin, or GnRH[148]. During the Evolution, the endocrine system has gained in complexity in all invertebrates but even more in vertebrates due to the dual duplication of the entire genome at the root of vertebrates' radiation, and to the emergence of the pituitary as an integrator of an essential part of endocrine functions[149][150][151].Preprints (www.preprints.org) | NOT PEER-REVIEWED | Posted: 25 September 2020 doi:10.20944/preprints202008.0379.v2…”