Changes in the cellular composition of the gill epithelium during the life cycle of a nonparasitic lamprey: functional and evolutionary implications

Abstract

Several lamprey species form pairs, comprising an anadromous parasitic species and a derivative nonparasitic species that neither leaves fresh water nor feeds as an adult. This paper provides the first description of the radical changes undergone by the cellular composition of the gill epithelium during the major phases in the life cycle of a nonparasitic lamprey (American brook lamprey, Lethenteron appendix (DeKay, 1842) (= Lampetra appendix (DeKay, 1842)) and discusses their potential functional and evolutionary significance. The gill epithelium of the larva of L. appendix contains ammocoete mitochondrion-rich cells (AMRCs), intercalated mitochondrion-rich cells, and pavement cells, as does that of the larva of anadromous parasitic species which likewise lives in fresh water. By the completion of metamorphosis, the AMRCs have disappeared and well-developed chloride cells have been produced, the latter cell type being essential for osmoregulation by its closely related anadromous species in hypertonic environments. By the attainment of sexual maturity, the chloride cells have been lost. Such changes in the timing of chloride cell representation could help account for the ability of some metamorphosing, but not mature individuals of another nonparasitic species ( Lampetra planeri (Bloch, 1784)), to osmoregulate in up to 70% of seawater. The well-developed chloride cells in the nonparasitic L. appendix represent the retention of an ancestral character.