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- Cellular composition and ultrastructure of the gill epithelium of larval and adult lampreys : Implications for osmoregulation in fresh and seawater


The agnathan (jawless) stage in vertebrate evolution is represented in the contemporary fauna only by the hagfishes (Myxiniformes) and lampreys (Petromyzontiformes) (Hardisty, 1982Go). Although analyses of morphological and physiological data strongly indicate that lampreys are more closely related to the gnathostomatous (jawed) vertebrates than to the hagfishes (Hardisty, 1982Go; Forey and Janvier, 1993Go), the results of certain molecular studies support the view that the hagfishes and lampreys constitute a monophyletic group (Stock and Whitt, 1992Go; Mallatt and Sullivan, 1998Go; Kuraku et al., 1999Go; Delarbre et al., 2002Go). Yet, there can be no doubt that these two agnathan groups have been separated for a very long period and probably from as long ago as the lower Cambrian (Janvier, 1999Go).

Hagfishes, which are found only in marine habitats, are osmoconformers (McFarland and Munz, 1965Go; Cholette et al., 1970Go). The concentrations of Na+ and Cl in their sera approximate those in full-strength seawater, a situation unique amongst vertebrates and which results in their internal milieu being essentially iso-osmotic with that of their marine environment (Robertson, 1974Go). These characteristics imply that hagfishes have always lived in marine habitats (Robertson, 1957Go, 1974Go; Lutz, 1975Go).

In contrast to hagfishes, the anadromous species of lampreys spend a substantial part of their life cycle in freshwater (Hardisty and Potter, 1971Go; Hardisty et al., 1989Go). The efficient osmoregulatory mechanisms evolved by lampreys enable the concentrations of Na+ and Cl in their internal milieu to be maintained at levels well above that of freshwater, when the animal is living in rivers, and well below that of full-strength seawater, when the animal is residing in marine environments (Morris, 1972Go; Beamish et al., 1978Go). Since the osmolality of their serum is far lower than that of seawater, it has been concluded that lampreys have an ancient freshwater history and that the marine parasitic phase of their life cycle was developed relatively late in their evolution (Hardisty et al., 1989Go). However, the recent discovery of a lamprey-like fossil in lower Cambrian marine deposits (Shu et al., 1999Go) strongly suggests that the initial evolution of lampreys occurred in a marine environment at a very early date, i.e. over 545 million years ago, and thus prior to the time when this group invaded freshwater.

The marked differences between both the ionic composition and osmolality of the body fluids of hagfishes and lampreys are consistent with the long period that these two agnathan groups are believed to have been separated. Indeed, as long ago as 1932, Homer Smith stated that "these two groups lead back to a parting of the ways in the evolution of body fluids".

The teleost fishes are found in a wide range of fresh, brackish and marine habitats and thus, as a group, are faced with the same variety of osmotic problems as those experienced by the anadromous species of lampreys during the course of their life cycle. The diversity and abundance of teleosts account for this group having been the subject of the majority of the studies aimed at elucidating the mechanisms by which fish regulate the ionic composition and osmolality of their serum (Smith, 1930Go, 1932Go; Krogh, 1939Go; Karnaky, 1980Go, 1986Go; Zadunaisky, 1984Go; Perry, 1997Go; Wilson et al., 2000aGo,bGo). Although lampreys are not closely related to teleosts, their gills and kidneys likewise constitute the main organs responsible for osmoregulation, and their overall mechanisms for regulating the concentrations of Na+ and Cl in their body fluids are similar (Morris, 1972Go; Beamish, 1980Go; Hardisty et al., 1989Go). However, ultrastructural studies have demonstrated that, particularly when lampreys are in freshwater, the cellular composition of their gill epithelium differs from that of teleosts (Bartels et al., 1996Go, 1998Go). These studies have also revealed that certain epithelial cells in the lamprey gill possess highly distinctive ultrastructural features, which they share with particular cell types in specific ion-transporting epithelia in other vertebrates and for which a function has been determined.

In the present review, the ultrastructural characteristics of each of the cell types present in the gill epithelium at the different stages in the life cycle of lampreys are described. The characteristics of each cell type are then considered in the context of both the type of environment in which the animal containing that cell is found, i.e. freshwater or seawater, and the roles played by analogous cells in other vertebrates. This then enables each of these various cell types to be assigned a presumptive role in lamprey osmoregulation.

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