Ontogenetic and Phylogenetic Development of the Endocrine Pancreas (Islet Organ) in Fishes

General and Comparative Endocrinology 116, 303–335 (1999) Article ID gcen.1999.7376, available online at http://www.idealibrary.com on REVIEW Ontogenetic and Phylogenetic Development of the Endocrine Pancreas (Islet Organ) in Fishes John H. Youson and Azza A. Al-Mahrouki Department of Zoology and Division of Life Sciences, University of Toronto at Scarborough, Scarborough, Ontario M1C 1A4 Canada Accepted August 25, 1999 The morphology of the gastroenteropancreatic (GEP) relatively small islets in the generalized euteleosts and system of fishes was reviewed with the objective of the tendency for the concentration into Brockmann providing the phylogenetic and ontogenetic development bodies of large (principal) islets (with or without second- of the system in this vertebrate group, which includes ary islets) in the more derived forms. The holostean agnathans and gnathostome cartilaginous, actinoptyeryg- actinopterygians (Amiiformes and Semiontiformes) share ian, and sarcopterygian fishes. Particular emphasis is with the basal teleosts (osteoglossomorphs, elopo- placed on the fish homolog of the endocrine pancreas of morphs) the diffuse arrangement of the components of other vertebrates, which is referred to as the islet organ. the islet organ that is seen in generalized euteleosts. The one-hormone islet organ (B cells) of larval lampreys Since principal islets are also present in adult lampreys is the most basic pattern seen among a free-living the question arises whether principal islets are a derived vertebrate, with the two-hormone islet organ (B and D or a generalized feature among teleosts. There is a cells) of hagfish and the three-hormone islet organ (B, D, paucity of studies on the ontogeny of the GEP system in and F cells) of adult lampreys implying a phylogenetic fish but it has been noted that the timing of the trend toward the classic four-hormone islet tissue (B, D, appearance of the islet cell types parallels the time that F,and A cells) in most other fishes. An earlier stage in the they appear during phylogeny; the theory of recapitula- development of this phylogenetic sequence in verte- tion has been revisited. It is stressed that the lamprey life brates may have been the restriction of islet-type hor- cycle provides a good opportunity for studying the mones to the alimentary canal, like that seen in protochor- development of the GEP system. There are now several dates. The relationship of the islet organ to exocrine markers of cell differentiation in the mammalian endo- pancreatic tissue, or its equivalent, is variable among crine pancreas which would be useful for investigating bony, cartilaginous, and agnathan fishes and is likely a the development of the islet organ and cells of the manifestation of the early divergence of these piscine remaining GEP system in fish. ௠ 1999 Academic Press groups. Variations in pancreatic morphology between individuals of subgroups within both the lamprey and Scientific interest in the distribution, structure, and chondrichthyan taxa are consistent with their evolution- function of endocrine tissues associated with the ali- ary distance. A comparison of the distribution and mentary canal (gastroenteropancreatic, GEP, system) degree of concentration of the components of the islet of fishes can be traced back at least to the beginning of organ among teleosts indicates a diffuse distribution of the 19th century. This interest has heightened as we 0016-6480/99 $30.00 303 Copyright ௠ 1999 by Academic Press All rights of reproduction in any form reserved. 304 Youson and Al-Mahrouki approach the end of the 20th century. Thus, through alimentary canal (stomach and intestine) with cells of nearly 200 years of investigation there is still a dual similar type, or elaborating similar hormones, in the fascination with the importance of the GEP tissue to endocrine pancreas. The endocrine cells of these three individual fish species and to how the tissue in fishes components have an intimate ontogenetic history. in general relates to that found in higher vertebrates However, the primary focus of this update will be on (Falkmer, 1995). With commercially valuable species, the fish homolog of the endocrine pancreas present in knowledge of this tissue is essential, for hormones nonpiscine vertebrates. Furthermore, the focus will be elaborated by the GEP system are critical in intermedi- a comparison of the distribution, structure, and ontog- ary metabolism, which in turn is crucial for fish growth eny of the endocrine pancreatic tissue through the and eventual maturity (Plisetskaya, 1990a,b); some various groups of fishes, rather than on the compara- GEP hormones have direct effects even on these latter tive function and structure of the peptides that they two parameters (Plisetskaya and Mommsen, 1996). generate. Since the hormones of the GEP system have equally important roles in higher vertebrates, including hu- mans, the origins of the cells of the GEP system in the DEFINITION OF TERMS context of where and how they develop (ontogenesis) and when they appeared during the history of verte- Ontogeny is development of a single individual, or a brates (phylogenesis) have been continuous curiosities system within the individual, from the fertilized egg to (Bonner-Weir and Weir, 1979; Epple and Brinn, 1986, death (Smith, 1960), i.e., a total life history including 1987). With the refinement of techniques to isolate and embryonic and postnatal (Gould, 1977). This term sequence peptides or to clone cDNAs, the past 2 should be distinguished from phylogeny, which is a decades have seen an explosion in the information on type of development involving modification of a spe- the molecular structure of fish GEP peptides. The cies or a group of species, i.e., ‘‘the family history’’ or primary structures of these peptides in fishes have the evolutionary history of a lineage (Gould, 1977). been crucial for analyses which attempt to explain the This latter type of development is characterized by molecular evolution of GEP peptides of vertebrates accompanying changes in structure and function (e.g., Conlon, 1995; Larhammar, 1996; Plisetskaya and (Smith, 1960). It is the evolutionary trend, or morpho- Mommsen, 1996). The bioactivity of isolated peptides cline (Hildebrand, 1995), of the GEP system of fishes, a from fishes, relative to that of higher animals, has particular phyletic line, that is being considered in this provided examples of both a suspected modern special- review. The word fish has different connotations so it is ization and a regression of function of GEP hormones important to establish the terms of reference for this (Falkmer, 1995). review. The interpretation of Nelson (1994) is adopted, The above paragraph emphasizes the value that can that is, the term ‘‘fish’’ includes both the jawless be placed on investigations into the GEP system of (Agnatha) and the jawed (Gnathostomata) aquatic fishes. This view is certainly not novel, for many vertebrates that ‘‘... have gills throughout life and well-known comparative endocrinologists have illus- limbs, if any, in the form of fins.’’ This broad definition trated this point in extensive, earlier reviews (Epple, includes the agnathans, the hagfishes and lampreys, 1969; Epple and Lewis, 1973; Epple and Brinn, 1986, and the two large extant grades of aquatic gnathos- 1987; Falkmer, 1985a,b, 1995; Plisetskaya, 1989a,b, tome fishes, Chondrichthimorphi and Teleostomi. The 1990a,b). In many ways, this review is dedicated to former grade consists of the class Chondrichthyes, these pioneers and some of their views will be reexam- which possesses the subclasses Holocephali (single ined and placed in the context of more recent litera- order Chimaeriformes) and Elasmobranchi (contain- ture. It is the objective of this report to provide an ing many orders under superorder Euselachii). Grade update of the literature on the GEP system as it Teleostomi contains the classes Sarcopterygii (lobe- pertains to the topics of ontogeny and phylogeny of finned fishes) and Actinopterygii (ray-finned fishes). It this system in fish. As it will soon be demonstrated, it is the former, and certainly not the latter, class which is difficult to separate the endocrine cells within the lead to the tetrapods. Thus in the context of vertebrate Copyright ௠ 1999 by Academic Press All rights of reproduction in any form reserved. Fish Endocrine Pancreas 305 evolution, the actinopterygians, and particularly the application of antisera and immunohistochemistry in teleosts, are a highly specialized group which some the investigations of endocrine cells of the stomach, might consider led to a dead end. Among the piscine intestine, and pancreas of fishes, the use of words such groups are one-half the approximately 50,000 species as argentaffin, argyrophilic, and enterochromaffin is of living vertebrates and these fishes demonstrate gradually disappearing. However, techniques which tremendous diversity in their form and distribution. identify any one of these three features in cells are still Needless to say, this report cannot take advantage of valuable in the identity of putative endocrine cells this diversity and likely will be concerned with only which show no immunoreactivity to antisera against fewer than 1.0% of the living fishes. Despite this, recognized peptides. attempts will be made to provide data on examples The endocrine pancreatic homolog in fishes is re- from as many of the 57 orders of fishes as possible. ferred to as the endocrine pancreas, islet tissue, insular However, since a central theme of this review

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