Functional and evolutionary implications of the cellular composition of the gill epithelium of feeding adults of a freshwater parasitic species of lamprey, Ichthyomyzon unicuspis

Abstract

This paper provides the first description of the cellular composition of the gill epithelium of feeding adults of Ichthyomyzon unicuspis Hubbs and Trautman, 1937 (silver lamprey), a parasitic species of lamprey that is confined to fresh water. The surface layer of this epithelium consists solely of pavement cells and intercalated mitochondria-rich cells, which are the only cell types found in all freshwater stages of lampreys and thus considered responsible for the uptake of Na+ and Cl– in hypotonic environments. This epithelium does not contain, however, the chloride cells present during the marine parasitic phase of anadromous lamprey species, such as Petromyzon marinus L., 1758 (sea lamprey), and which are responsible for secreting excess Na+ and Cl–. The absence of this cell type in parasitic adults of I. unicuspis also differs from its presence in parasitic adults of landlocked P. marinus and metamorphosing individuals of the exclusively freshwater nonparasitic species Lethenteron appendix (DeKay, 1842) (American brook lamprey), and which thus reflects the retention of a cell type that was crucial for osmoregulation during the marine phase of their respective anadromous parasitic ancestors. The absence of chloride cells in I. unicuspis is consistent with the hypothesis that Ichthyomyzon, which is at or close to the base of the phylogenetic tree for Northern Hemisphere lampreys (Petromyzontidae), evolved in fresh water or has been confined to fresh water for a very long period.