The changing biological roles of melatonin during evolution: from an antioxidant to signals of darkness, sexual selection and fitness

Abstract

Melatonin is a molecule present in a multitude of taxa and may be ubiquitous in organisms. It has been found in bacteria, unicellular eukaryotes, macroalgae, fungi, plants and animals. A primary biological function of melatonin in primitive unicellular organisms is in antioxidant defence to protect against toxic free radical damage. During evolution, melatonin has been adopted by multicellular organisms to perform many other biological functions. These functions likely include the chemical expression of darkness in vertebrates, environmental tolerance in fungi and plants, sexual signaling in birds and fish, seasonal reproductive regulation in photoperiodic mammals, and immunomodulation and anti-inflammatory activity in all vertebrates tested. Moreover, its waning production during aging may indicate senescence in terms of a bio-clock in many organisms. Conversely, high melatonin levels can serve as a signal of vitality and health. The multiple biological functions of melatonin can partially be attributed to its unconventional metabolism which is comprised of multi-enzymatic, pseudo-enzymatic and non-enzymatic pathways. As a result, several bioactive metabolites of melatonin are formed during its metabolism and some of the presumed biological functions of melatonin reported to date may, in fact, be mediated by these metabolites. The changing biological roles of melatonin seem to have evolved from its primary function as an antioxidant.

Melatonin: a possible link between the presence of artificial light at night and reductions in biological fitness

“…B 370: 20140122 a number of invertebrates, including Drosophila [56], crickets [57] and Daphnia [58]. The observed differences in the timing and location of peak melatonin concentrations in the invertebrates is perhaps not surprising given the relative breadth of taxonomic diversity compared with vertebrates, but nonetheless it raises some interesting questions regarding the ubiquitous nature of the hormone and reinforces the belief that functionally it is more than simply a signal of darkness [33].…”

“…First isolated from the bovine pineal gland [34], the indolamine melatonin has subsequently been identified in all higher taxonomic groups [33,35]. Its structure is thought to be highly conserved across taxa [33,35,36] and in animals its biosynthesis from tryptophan via serotonin (see figure 1) is believed to be comparable for vertebrates and invertebrates [35].…”

“…In vertebrates, circulating concentrations of pinealderived melatonin vary throughout a 24 h cycle, typically reaching their highest concentrations during periods of natural darkness and their lowest concentrations during daylight hours [31][32][33]. Seasonal shifts in circulating melatonin concentrations are also evident, with lower concentrations observed in winter compared with those in summer [42].…”

“…Melatonin is one of the key drivers of biological rhythm whose principal function is to relay information about changes in day-length [31,32]. Perhaps less well known, but of potentially considerable physiological importance, is the critical role melatonin plays as an antioxidant (for a recent review, see [33]). The major problem faced by species living in regions with artificial night lighting is that, in the presence of LAN, the potential for melatonin to act as either an antioxidant or a regulator of biological rhythm may be compromised because endogenous melatonin concentrations are reduced.…”

“…Its structure is thought to be highly conserved across taxa [33,35,36] and in animals its biosynthesis from tryptophan via serotonin (see figure 1) is believed to be comparable for vertebrates and invertebrates [35]. The primary site of endogenous melatonin synthesis in vertebrates is the pineal gland, but its presence has been documented in many other organs and tissues, including the retina, intestine, salivary gland, Hardian gland and leucocytes [33,37]. In invertebrates, endogenous melatonin is typically synthesized in the cerebral ganglia but it is similarly found in other tissues and organs, including the eyes and reproductive tissues [35,[38][39][40][41].…”