Although the gills of lampreys and teleosts are assumed to perform similar, if not identical, osmoregulatory functions, the cellular composition of their epithelia differs considerably in some respects (Laurent, 1984; Wilson and Laurent, 2002). Thus, in contrast to the situation in lampreys, the gill epithelia of teleosts always only contain pavement and chloride cells, irrespective of whether the fish is living in fresh or seawater. Furthermore, teleosts possess two types of chloride cell. There is thus a freshwater chloride cell, which is typically singly intercalated between the pavement cells, as is the case with the intercalated MR cells in lampreys, and a seawater chloride cell, which is similar to the chloride cells of adult lampreys in seawater (see below).
The freshwater chloride cell of teleosts differs from the intercalated MR cell of lampreys through its possession of a tubular system, which is less elaborate than that of the chloride cell in seawater, and by the absence of rod-shaped particles in its plasma and cytoplasmic membranes. Although the term `MR cell' has been proposed for the freshwater chloride cell of teleosts (Pisam and Rambourg, 1991), the gills of teleosts in freshwater do not contain cells with the cytological characteristics of either the intercalated MR cells of lampreys and higher vertebrates or the ammocoete MR cell. Experimental studies indicate that, in teleosts, the freshwater chloride cell exchanges Cl– for HCO3– while the pavement cell exchanges Na+ for H+ (Goss et al., 1992; Perry, 1997). The latter conclusion is supported by the results of immunocytochemical studies, which showed that the pavement cell is the only cell in the teleost gill epithelium that contains both H+-ATPase and ENac (Sullivan et al., 1995; Wilson et al., 2000a). The freshwater chloride cell of teleosts thus performs the role that we consider is carried out in lampreys by the subtype C of the intercalated MR cell. The function performed by the pavement cell of teleosts in freshwater, in turn, is ascribed in lampreys to the activities of the subtypes A and C of the intercalated MR cell and the pavement cell, coupled in adults and possibly uncoupled in ammocoetes.
The differences between the gill epithelium of teleosts and lampreys in marine environments are less pronounced than those described above for freshwater and are mainly associated with chloride cells, which in both groups are responsible for excreting excess Cl– and Na+. They thereby constitute the main effector cells for osmoregulation in seawater. Although the chloride cells of teleosts and lampreys are both located close to the afferent filament artery and form multicellular complexes, the arrangement and size of these complexes in the two groups differ. Thus, the chloride cells in the gills of teleosts form small groups of 2–4 cells whereas those of lampreys form long rows. Furthermore, while accessory cells, which lack an extensive tubular system and associated Na+/K+-ATPase, also frequently contribute to the groups of chloride cells in teleosts (Hootman and Philpott, 1980), such cells are not found in lampreys (Bartels and Potter, 1991). Moreover, in teleosts, each group of chloride cells and of chloride and accessory cells share an apical crypt (Karnaky, 1986), a structure not found in association with these cells in lampreys (Nakao, 1974; Peek and Youson, 1979a; Bartels and Potter, 1991; Bartels et al., 1993, 1996). The paracellular pathways between the chloride cells in both lampreys and teleosts and between chloride and accessory cells in teleosts contain leaky occluding junctions through which Na+ enters the environment passively (Sardet et al., 1979; Ernst et al., 1980; Bartels and Potter, 1991). However, the increase that occurs in the length of this shunt, following the migration of individuals from fresh to seawater, is achieved in teleosts through the development of interdigitations amongst the cells that form multicellular complexes (Sardet et al., 1979; King et al., 1989) and in lampreys by the retraction of pavement cells (Bartels et al., 1996). Finally, the apical membrane of the chloride cells of teleosts in seawater does not contain the prominent clusters of particles that are found in this membrane in lampreys (Sardet et al., 1979; Ernst et al., 1980; Bartels et al., 1993).
As mentioned earlier, the fact that the osmolality of the sera of all stages in the life cycle of lampreys is far less than that of seawater argues that this agnathan group spent a considerable period in freshwater (Hardisty et al., 1989). However, the discovery of a lamprey-like fossil in Cambrian marine deposits from 545 million years ago strongly indicates that the Petromyzontiformes evolved in marine environments (Janvier, 1999; Shu et al., 1999). If this is the case, the specialised parasitic phase in the life cycle of contemporary anadromous lampreys represents a secondary return to a marine environment. By contrast, the teleosts are believed to have evolved in freshwater and then undergone extensive adaptive radiation in the sea during the Mesozoic, with some groups subsequently reinvading freshwater (Lutz, 1975). The possession of the same basic mechanisms for osmoregulation by lampreys and teleosts thus presumably represents the result of convergent evolution. Such independent evolution of the same mechanisms would account for differences between the characteristics of the cell types used for osmoregulation by these two divergent groups.
Gratitude is expressed to Prof. Wolfram Nagel for helpful discussions and to Ursula Fazekas, Pia Unterberger and Horst Ruß for expert technical assistance. Financial support was provided by the Australian Research Grants Committee and Deutsche Forschungsgemeinschaft.