The Agnathan Enteropancreatic Endocrine System: Phylogenetic and Ontogenetic Histories, Structure, and Function(1).

INTRODUCTION

Hagfishes and lampreys are jawless fishes with direct ancestory to a once fluorishing group of Agnatha in the Palaeozoic. Among these agnathans were the ostracoderms which fossil records suggest were among the first vertebrates. In the past, the living agnathans were referred to as cyclostomes (round mouths) and they were grouped within the vertebrate Class, the Cyclostomata, and within distinct subclasses (or orders) as Petromyzontids (the lampreys) or Myxinids (the hagfishes). More recent classification of fishes (Nelson, 1994) has the lampreys and hagfishes within the vertebrate superclass Agnatha and as distinct classes, Cephalaspidomorphi and Myxini, respectively. Petromyzontiformes and Myxiniformes are the distinct orders. The taxanomic relationship of hagfishes and lampreys has always been controversial, for they show many structural, functional, and behavioural differences (Hardisty, 1979, 1982). Recently, lampreys were considered to be more similar to gnathostome fishes than to hagfishes (Forey and Janvier, 1994). In fact, Janvier (1986) has always questioned whether hagfishes should be included among the Vertebrata because they lack segmented vertebral elements.

Fossil evidence of early agnathans suggest that hagfishes may date back to the Cambrian period (Forey and Janvier, 1994) while lampreys originated from a naked anaspid line about 350 million years ago. Thus the ancestors to the two extant agnathan lines diverged early in craniate evolution.

The life histories of the two living agnathans are distinctly different. Hagfishes live their entire life in a marine environment, produce small batches of large yolky eggs and, following hatching, exhibit direct development to sexual maturity (Gorbman, 1997). Lamprey reproduction in freshwater yields many small eggs and, following hatching, there is a larval period of growth and a metamorphosis (indirect development) to a juvenile (Youson, 1988). Juveniles of nonparasitic species immediately commence sexual maturation in freshwater whereas those of parasitic species become predatory and feed on the blood, body fluids, and flesh of host teleosts. In some parasitic species juveniles are capable of marine osmoregulation and they migrate to the open sea for feeding. It is assumed that other species are restricted to feeding within their natal stream because of an inability to osmoregulate in hyperosmotic environments (Hardisty et al., 1989). Genetic, morphometric and meristic analyses have grouped similar parasitic and nonparasitic lamprey species as paired or satellite species with the implication that they arose from a common ancestor, which was likely parasitic. This view also implies that the nonparasitic adult life history type is more recent.

Due to their ancient history, lampreys and hagfishes have been the subject of much anatomical and physiological investigation. In many cases, the objective has been to find clues which might provide a bridge between the earliest and more modern forms of vertebrates or between vertebrates and other members of Phylum Chordata, i.e., the protochordates. Furthermore, all systems of lampreys and hagfishes have been directly compared to provide some answer to questions of their relationship to one another and to their environmental history (Hardisty, 1979, 1982; Hardisty et al., 1989). Among these comparisons are reports of the endocrine cells of the alimentary canal and the pancreas. Collectively these cells are part of a system termed in many other vertebrates, the gastroenteropancreatic (GEP) system. Included in the GEP are enteroendocrine cells of the intestine and endocrine cells of both the pancreas and stomach. Since neither the hagfish nor the lamprey has a stomach (Hardisty, 1979), the enteropancreatic (EP) system seems more appropriate for agnathans.

Hagfishes and lampreys are also distinct among other vertebrates in having their exocrine and endocrine equivalents of the vertebrate pancreas in isolation (Barrington, 1972; Youson, 1981). The exocrine elements are present within the intestinal or diverticular epithelia while the equivalent of the endocrine pancreas is an aggregate of submucosal islets, the islet organ. The presence of a compacted aggregate of zymogen cells in the diverticulum, a so-called protopancreas, in one species of lampreys is often used as evidence that a concentrated mass of pancreatic exocrine cells evolved more than once in vertebrate evolution (Epple and Brinn, 1987).

The hormones elaborated by the EP system of lampreys and hagfishes have, among other functions, an important role in intermediary metabolism. This latter fact was recognized by some of the early pioneers of comparative vertebrate endocrinology and we owe them much for their effort and their inspiration. Among these are Barrington, Epple, Falkmer, Hardisty and Plisetskaya. Falkmer and Plisetskaya have included some discussion of the hagfish and lamprey EP system in their reviews (Plisetskaya, 1990; Falkmer, 1995; Plisetskaya and Mommsen, 1996). A section on the distribution and the structure of agnathan EP can be found in the most recent review of the GEP systems of fishes (Youson and Al-Mahrouki, 1999) This essay will review some of the early work on the ontogenetic and phylogenetic development of the agnathan EP system and the function of the hormones elaborated by this system. Descriptions will be confined to hormones which are shared in common by the islet organ and the endocrine cells of the gut, namely, peptides of the insulin, glucagon, pancreatic polypeptide, and somatostatin families. Ultimately, the description will lead to the present state of affairs in these systems in lampreys and hagfishes, which were last specifically reviewed in 1990 (Van Noorden, 1990; Youson and Cheung, 1990), and to the directions of future research.