John H. Youson

2 First Metamorphosis

Publisher Summary This chapter describes the different aspects of metamorphosis and fish ontogeny. The term “metamorphosis,” when considered in the broadest sense in the animal kingdom, refers to any abrupt change in the form or structure of an organism during postembryonic development. A first metamorphosis occurs in all species having a larva period and is the phase that terminates this period and that leads into a juvenile period. Bony fishes with a classical first metamorphosis during their ontogeny are Anguilliformes, Elopiformes, Notacanthiformes, and Pleuronectiformes. First metamorphosis is also present in Petromyzontiformes, but not in Class Chondrichthyes or in Myxiniformes. A second metamorphosis may occur in many fish species when juveniles undergo sexual maturation to definitive adults, but it is not a true metamorphosis. The time of first metamorphosis varies among the orders of fishes, but is usually related more to body length than to age. Growth rate within a population may also be an important determinant. In species with a protracted and nontrophic metamorphic phase, physiological preparation is essential to the completion of metamorphosis.

Neuropeptide Y-related peptides from the pancreas of a teleostean (Eel), Holostean (bowfin) and elasmobranch (skate) fish

Homologous peptides belonging to the pancreatic polypeptide (PP) family were isolated from the pancreas of a teleostean fish, the American eel (Anguilla rostrata), an holostean fish, the bowfin (Amia calva) and an elasmobranch fish, the skate (Raja rhina), and their primary structures were determined. The peptides show stronger homology to neuropeptide Y, particularly in their COOH-terminal regions, than to peptide YY or pancreatic polypeptide and contain an alpha-amidated COOH-terminal tyrosine residue. The skate peptide Tyr-Pro-Pro-Lys-Pro-Glu-Asn-Pro-Gly-Asp10-Asp-Ala-Ala-Pro-Glu-Glu- Leu-Ala-Lys- Tyr20-Tyr-Ser-Ala-Leu-Arg-His-Tyr-Ile-Asn-Leu30-Ile-Thr-Arg- Gln-Arg-Tyr-NH2 represents the first member of the PP family to be isolated from a cartilaginous fish. The primary structure of the pancreatic PP family peptide has been more strongly conserved among the phylogenetically more ancient holostean and elasmobranch fishes than among the teleosts. A comparison of the primary structures of all PP family peptides supports the hypothesis and evolution has acted to conserve features of tertiiary structure in the molecules (e.g., the polyproline- and alpha-helices) rather than individual amino acid residues.

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 extant fishes and little is known about its phylogenetic development during the 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 vertebrates. The study reviews recent data on the role of the thyroid gland and its hormones in metamorphosis, summarizes some recent views on the evolution 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 data support an earlier viewpoint of a relationship between thyroid and reproductive 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 protochordates, Larvacea, are derived. The iodide-concentrating efficiency of the endostyle 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 postmetamorphic reproduction in freshwater became fixtures in the lamprey life cycle; a non-parasitic adult life-history type appeared later. The presence among extant lampreys of two different adult life-history types, and examples of the lability of the timing of sexual maturation in some species, imply that there has been a complex interplay between the thyroid and reproductive 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.

The Biology of Metamorphosis in Sea Lampreys: Endocrine, Environmental, and Physiological Cues and Events, and Their Potential Application to Lamprey Control

The present study describes 20 years of research driven by the view that new control methods may be a product of an extensive examination of the cues and events of sea lamprey (Petromyzon marinus) metamorphosis. A rise in water temperature (and not its magnitude) from its winter minimum is a requirement for spontaneous metamorphosis in sea lampreys. Neither density, starvation, nor photoperiod have been proved in laboratory studies to influence metamorphosis. Thyroid hormones (TH) in the serum reach a peak level just prior to metamorphosis and decline sharply at the initial stage of this phase. Precocious metamorphosis can be induced in sea lampreys and other lamprey species by most goitrogens; the induction is accompanied by a decline in serum levels of TH. Lipogenesis and lipolysis are key events in sea lamprey metamorphosis and they involve a complex interaction between TH, insulin, and somatostatin. Many larval molecules are deleted, altered, or replaced by adult forms during metamorphosis in sea lampreys and some of these do not show a similar developmental profile in a nonparasitic species (Lampetra appendix). Albumin is one of the molecules that changes from a larval to an adult form during sea lamprey metamorphosis but is not replaced by an adult albumin in L. appendix. The functional significance of this interspecific variation needs to be examined, for it may be relevant to adult feeding behavior. Future studies that compare the development of nonparasitic and parasitic adult life histories, however, should be performed on paired (statellite) species. The redistribution of nonhaem iron at this time emphasizes the unique feature of tissue iron-loading that exists in larval lampreys. Features of sea lamprey metamorphosis are discussed in a context of their potential relevance to the control program.

Transformation of the endostyle of the anadromous sea lamprey, Petromyzon marinus L., during metamorphosis ☆: I. Light microscopy and autoradiography with 125I

Abstract Routine light microscopy and autoradiography with 125 I were used to examine the transformation in structure and iodine-binding capacity of the endostyle throughout (stages 1 to 4) metamorphosis in the anadromous sea lamprey, Petromyzon marinus L. The endostyle began to transform prior to the first external signs of metamorphosis (prometamorphosis) and was already replaced by thyroid follicles by the end of stage 2 of metamorphosis. Many of these follicles appeared to have formed as a result of proliferation of the epithelia (type II and V cells) at the angle of the original lumina of the endostyle. However, it is possible that all cell types of the ammocoete endostyle, with the exception of the type I cells, may be involved in the formation of at least some follicles. The colloid of the newly formed follicles was not stainable with periodic acid-Schiff, suggesting that the thyroglobulin which is synthesized or released by metamorphosing lamprey may have different chemical properties than thyroglobulin of the adult. Large numbers of pigmented granules within some of the remaining epithelial cells may reflect their involvement in the storage of thyroid hormone or in its release during metamorphosis. 125 I was bound within the transforming endostyle and its replacement throughout metamorphosis, but the localization of the radioiodine varied during the reconstruction. During prometamorphosis and early stage 1 the distribution of iodine resembled that of ammocoetes. In subsequent stages, at first not all follicles demonstrated the ability to bind iodine (end of stage 2), but there was a progressive increase in binding to the end of the metamorphic period. It is suggested that the binding of iodine in the newly formed follicles reflects the involvement of cells of the ammocoete endostyle. There also appears to be a variable differentiation of cells within the developing follicles.

Concentration of triiodothyronine in the sera of the sea lamprey, Petromyzon marinus, and the brook lamprey, Lampetra lamottenii, at various phases of the life cycle

Triiodothyronine (T3) was measured by double antibody radioimmunoassay in the sera of individuals of all stages of the life cycle in the sea lamprey, Petromyzon marinus, and in larval (ammocoetes) and metamorphosing individuals of the brook lamprey, Lampetra lamottenii. There was no significant difference in results from the two species. Although serum T3 concentration did not vary significantly in ammocoetes maintained at the same temperature throughout the year, concentrations in ammocoetes displayed an inverse response to fluctuations in water temperature. Ammocoetes maintained at temperatures of 7 to 10 degrees and 19 to 21 degrees exhibited significantly different circulating T3 levels of 2400 and 1550 ng dl-1, respectively. Therefore, it is expected that there may be some seasonal variation in the levels of the hormone in ammocoetes in their natural environment. A precipitous collapse of the serum levels of T3 was observed by an early stage of metamorphosis (100 ng dl-1) and no significant difference in levels was observed throughout the remaining period of this phase. Young parasitic adults and adult lampreys collected during their spawning migration (upstream migrants) exhibited circulating T3 concentrations of 40 and 30 ng dl-1, respectively. T3 levels in some upstream migrants were below the limit of detection (less than 5 ng dl-1). The metamorphic decline in serum T3 may simply mark the beginning of the lower T3 levels that characterizes the adult serum.

DISTRIBUTION OF LAMPREY GONADOTROPIN-RELEASING HORMONE-III (GNRH-III) IN BRAINS OF LARVAL LAMPREYS (PETROMYZON MARINUS)

Two immunoreactive forms of gonadotropinreleasing hormone (GnRH), lamprey GnRH-I and lamprey GnRH-III, were found in neurons in larval sea lampreys (Petromyzon marinus). Using antisera preferentially directed against either lamprey GnRH-I or-III, dense reaction product was seen in cell bodies in the rostral hypothalamus and preoptic area. Reaction product was also dense in fibers to and within the neurohypophysis, in addition to numerous fibers which projected caudally, beyond the neurohypophysis through the mesencephalon. The majority of immunoreactive GnRH was lamprey GnRH-III, and when lamprey GnRH-I was seen, it was in cells that appeared to contain both forms of GnRH. A small number of cells found in the caudal hypothalamus contained only immunoreactive lamprey GnRH-III, and these may constitute a functional subgroup within the population of GnRH neurons. In animals undergoing metamorphosis there was a large increase in reaction product in all GnRH-containing cells and fibers. A striking change within the distribution of GnRH cells was localized to a distinct group of GnRH-immunoreactive cells (GnRH-I and-III) in the ventral anterior hypothalamic area. These cells were minimally detectable in larvae, but during metamorphosis became densely filled with immunoreactive product in perikarya and distal processes. The results are consistent with the hypothesis that lamprey GnRH-III is an important form of GnRH during the maturation of GnRH cells and fibers, and further indicates that these cells have attained their normal positions in the preoptic area and hypothalamus before metamorphosis.

Variable effects of goitrogens in inducing precocious metamorphosis in sea lampreys (Petromyzon marinus).

The ability of different goitrogens (anti-thyroid agents) to induce precocious metamorphosis in larval sea lampreys (Petromyzon marinus) was assessed in four separate experiments. Two of these goitrogens (propylthiouracil [PTU] and methimazole [MMI]) are inhibitors of thyroid peroxidase-catalyzed iodination, and three (potassium perchlorate [KClO(4)], potassium thiocyanate [KSCN], and sodium perchlorate [NaClO(4)]) are anionic competitors of iodide uptake. Because, theoretically, all of these goitrogens prevent thyroid hormone (TH) synthesis, we also measured their influence on serum concentrations of thyroxine and triiodothyronine. All goitrogens except PTU significantly lowered serum TH concentrations and induced metamorphosis in some larvae. The incidence of metamorphosis appeared to be correlated with these lowered TH concentrations in that KClO(4), NaClO(4), and MMI treatments resulted in the lowest serum TH concentrations and the highest incidence of metamorphosis in sea lampreys. Moreover, fewer larvae metamorphosed in the KSCN and low-KClO(4) treatment groups and their serum TH concentrations tended to be greater than the values in the aforementioned groups. MMI treatment at the concentrations used (0.087 and 0.87 mM) was toxic to 55% of the exposed sea lampreys within 6 weeks. The potassium ion administered as KCl did not alter serum TH concentrations or induce metamorphosis. On the basis of the results of these experiments, we have made the following conclusions: (i) In general, most goitrogens other than PTU can induce metamorphosis in larval sea lampreys, and this induction is coincident with a decline in serum TH concentrations. (ii) The method by which a goitrogen prevents TH synthesis is not directly relevant to the induction of metamorphosis. (iii) PTU has variable effects on TH synthesis and metamorphosis among lamprey species. (iv) Unlike in protochordates, potassium ions do not induce metamorphosis in sea lampreys and are not a factor in the stimulation of this event.

Lamprin: A new vertebrate protein comprising the major structural protein of adult lamprey cartilage

Chemical analysis of lamprey cartilage showed that its major constituent was a newly defined structural protein termed lamprin. Amino acid analysis of lamprin revealed that it has a unique composition which is distinct from previously identified structural proteins.

Immunoreactivity to peptides belonging to the pancreatic polypeptide family (NPY, aPY, PP, PYY) and to glucagon-like peptide in the endocrine pancreas and anterior intestine of adult lampreys, Petromyzon marinus: An immunohistochemical study

Immunoreactivity of antisera directed against human neuropeptide Y (NPY), anglerfish polypeptide YG (aPY), bovine pancreatic polypeptide (bPP), salmon pancreatic polypeptide (sPP), porcine peptide tyrosine tyrosine (PYY), and salmon glucagon-like peptide (GLP) was investigated in the endocrine pancreas and anterior intestine of adult lampreys, Petromyzon marinus, by immunohistochemical analysis. There was no immunoreactivity to anti-sPP and anti-bPP in any tissue and anti-GLP immunostaining was only present in the anterior intestine. The immunoreactivity to antisera raised against NPY, aPY, and PYY was colocalized within the same small number of cells in the caudal and cranial pancreas of juveniles and the caudal pancreas of upstream migrant adults. These antibodies did not immunostain B- or D-cells and thus, NPY, aPY, and PYY were likely localized in a third cell type (3a) in the lamprey pancreas. Immunostaining of a few cells with only anti-aPY suggested the possibility of a fourth cell type (3b). Immunoreactivity was similar in the cranial and caudal pancreas of male upstream migrants; however, in the female cranial pancreas, a few cells demonstrated intense immunoreaction to anti-aPY, while weaker immunostaining with this antiserum was observed in B-cells. In the intestine of juvenile and upstream migrant lampreys, positive immunostaining to GLP, NPY, aPY, and PYY antibodies was colocalized within the same cell. We believe that this cell may contain PYY/glucagon family peptides. Other intestinal cells immunostained with either GLP or somatostatin-34 antiserum.