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Evidence for a gonadotropin inhibitory hormone (GnIH) system in the vertebrate gonads

Abstract

Reproduction is a fundamental stage in the life history of vertebrates. It has high costs: increased susceptibility to disease and resource limitations; but a high reward: the ability to produce successful offspring to carry genes to future generations. In order to minimize costs and maximize reproductive success, many vertebrates birth or hatch young during the times of greatest resource abundance. Breeding must be initiated well in advance of this time to allow for sufficient time to incubate offspring.

Vertebrates use cues from their environment to predict when times of high resource abundance will occur. In temperate zones, day lengths are appreciably different in each season but have low variance on a given day from year to year. As many vertebrates utilize resources that have seasonal cycles of abundance and occur at relatively the same time each year, day length would be an appropriate cue to predict such events. Vertebrates who can detect day lengths and who use changes in day length to appropriately initiate reproductive processes are called photoperiodic seasonal breeders. However, organisms also experience unpredictable environmental events, such as storms, increased predation, food shortage or other environmental stress, that make reproduction unfavorable. Reproductive success requires that they detect and respond to these unpredictable cues as well.

Thus seasonally breeding vertebrates must integrate a primary predictive cue (photoperiod) and supplementary cues to time reproduction appropriately. A system which allows for global changes in physiology and fine points of modulation within the system would be advantageous for such a response.

The hypothalamo-pituitary-gonad (HPG) axis regulates the endocrine control of reproduction. The HPG axis is "switched on" by stimulatory photoperiods in photoperiodic vertebrates. That is, when the organism experiences a stimulatory day length, neurosecretory cells in the hypothalamus of the brain produce and secrete gonadotropin releasing hormone (GnRH) into the external layer of the median eminence. Here, GnRH travels through the hypothalamo-hypophysial portal system into the pituitary gland. Inside the pituitary gland, GnRH binds to its receptor on gonadotroph cells, stimulating the production and secretion of luteinizing hormone (LH) and follicle stimulating hormone (FSH). LH and FSH travel through the bloodstream to their respective receptors on the testes and ovaries. In the gonads, LH and FSH stimulate the production of sex steroids and the maturation of gametes. Sex steroids, in turn, also stimulate reproductive behaviors in the brain and further stimulate or inhibit the production of GnRH, LH and FSH.

The discovery of gonadotropin inhibitory hormone (GnIH), a second hypothalamic peptide involved in reproduction, indicated that the HPG axis was more finely regulated than previously known. Hypothalamic GnIH inhibits the HPG at two levels: it inhibits the production and secretion of LH and FSH in the pituitary gland and it inhibits the activity of GnRH neurons directly. Furthermore, GnIH secretion is responsive both to endocrine correlates of day length and of stress. These responses indicate GnIH is a candidate for a "fine point modulation" in this system.

Recently, GnIH and GnIHR transcripts were identified in avian gonads. Furthermore, an experiment using systemic administration of GnIH inhibited gonadal function. The work of this dissertation was to identify the functional significance of a GnIH system in the gonads. Experiments using seasonally breeding songbirds and mammals identify the inhibitory function of GnIH on gonadal sex steroid production in males and females and the responsiveness of this system to supplementary cues. Finally, gonadal GnIH is presented in context with the gonadal GnRH system, to foster further research into the implications of gonadal neuropeptide systems. Thus gonadal GnIH is part of a complex system of reproductive regulation in vertebrates.

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