Theory on the evolutionary history of lamprey metamorphosis: role of reproductive and thyroid axes

Metamorphosis is a developmental strategy used by only a small number of ex tant fishes and little is known about its phylogenetic development during t he evolution history of this large group of vertebrates. The present report provides a putative evolutionary history of metamorphosis in the lamprey, an extant agnathan with direct descendancy from some of the oldest known ve rtebrates. The study reviews recent data on the role of the thyroid gland a nd its hormones in metamorphosis, summarizes some recent Views on the evolu tion of the endostyle/follicular thyroid in lampreys, and provides new data on the content of two gonadotropin-releasing hormones (GnRH-I and -III) in brain during goitrogen-stimulated, precocious metamorphosis. These new dat a support an earlier viewpoint of a relationship between thyroid and reprod uctive axes during metamorphosis. It is proposed that the earliest lampreys were paedomorphic larvae and they lived in a marine environment; as such, they resembled in many ways the larvae from which the ancient protochordate s, Larvacea, are derived. The iodide-concentrating efficiency of the endost yle was a critical factor in the evolution of metamorphosis and this gland was replaced by a follicular thyroid, for postmetamorphic animals needed to store iodine following their invasion of freshwater. Larval growth and pos tmetamorphic reproduction in freshwater became fixtures in the lamprey life cycle; a non-parasitic adult life-history type appeared later. The presenc e among extant lampreys of two different adult life-history types, and exam ples of the [ability of the timing of sexual maturation in some species, im ply that there has been a complex interplay between the thyroid and reprodu ctive axes during the evolution of metamorphosis in lampreys. This proposal is consistent with what we know of interplay of these axes in extant adult lampreys and with the long-held viewpoint that thyroid function and sexual maturation are an association with an ancient history. (C) 2001 Elsevier S cience Inc. All rights reserved.