Development of longitudinal mucosal folds in the intestine of the anadromous sea lamprey, Petromyzon marinus L., during metamorphosis

Abstract

During metamorphosis of the anadromous sea lamprey, Petromyzon marinus L., the larval intestine develops numerous longitudinal folds. The initiation of this event is marked by a decrease in diameter of the intestine and in the height of the typhlosole and is followed by an increase in numbers of cells undergoing DNA synthesis, first in the anterior intestine and later in the posterior intestine. Foci of proliferating cells along the epithelial walls of both regions result in the development of longitudinal folds which seem to elongate by further proliferation of the epithelial cells at their bases and by evagination of the underlying connective tissue and muscle. Slight variations in the mode of development of folds in the anterior and posterior intestines likely reflect the different functions of these regions in the adult. Metamorphosis of the lamprey provides an opportunity to study intestinal development in a vertebrate during a late stage of ontogeny.

Histological Comparisons of Intestines in Parasitic and Nonparasitic Lampreys, with Reference to the Speciation Hypothesis

“…Excluding typhlosole with high mucosal folds for the most part, L. japonicum in the present study revealed the regular pattern of arrangement in the three types of mucosal folds in opposition to some parasitic species previously reported, e.g. Petromyzon marinus, which have no definite pattern of arrangement (Youson and Connelly, 1978;Hilliard et al, 1983), indicating the difference of developing patterns in mucosal folds among species. Mucosal folds appear to have resulted from an elevation of both the epithelium and the underlying connective tissue and muscle, which have commenced after metamorphosis stage 4 in parasitic P. marinus (Youson and Connelly, 1978).…”

“…Apical pits, which indicate the existence of secretory cells releasing the content of the granules, have been reported from only feeding stage of parasitic species, with an example of P. marinus (Youson, 1981). These characteristics indicate increase of nutrient absorption which enables more rapid growth during the parasitic period, as already reported for P. marinus (Youson and Connelly, 1978;Youson, 1981).…”

“…Petromyzon marinus, which have no definite pattern of arrangement (Youson and Connelly, 1978;Hilliard et al, 1983), indicating the difference of developing patterns in mucosal folds among species. Mucosal folds appear to have resulted from an elevation of both the epithelium and the underlying connective tissue and muscle, which have commenced after metamorphosis stage 4 in parasitic P. marinus (Youson and Connelly, 1978). In the present study, low in height of mucosal folds observed at metamorphosed stage in the nonparasitic species were correspond in their proportion to those of tertiary folds at metamorphosed stages in parasitic L. japonicum, indicating the insufficient elevation caused by the later developmental onset or oppression of development in the former.…”

“…Accordingly, the presence of brush borders on the mucosal epithelial cells in the larval stages of all of the species examined in this study, as well as the metamorphosed and feeding adult stages of L. japonicum, should indicate active absorption by epithelial cells in these stages. Judging from the height, the three types, high, middle and low mucosal folds observed at metamorphosed and feeding adult stages in L. japonicum should correspond with primary, secondary and tertiary folds, respectively, proposed in developing order by Youson and Connelly (1978). Excluding typhlosole with high mucosal folds for the most part, L. japonicum in the present study revealed the regular pattern of arrangement in the three types of mucosal folds in opposition to some parasitic species previously reported, e.g.…”

“…In parasitic-anadromous L. japonicum, the development of extensive longitudinal mucosal folds with functional epithelial cells in the intestine at the metamorphosed stage may reflect an adaptive change for parasitic feeding, as well as osmoregulation in a marine environment (Pickering and Morris, 1973;Youson and Connelly, 1978). On the contrary, nonparasitic-fluvial L. kessleri and the northern form of L. reissneri exhibited only shrunk mucosal folds appearing disfunctional structures.…”