Immunity to Hymenolepis citelli by Peromyscus maniculatus: Genetic Control and Ecological Implications

Abstract

Acquired resistance to Hymenolepis citelli in Peromyscus maniculatus, the white-footed deer mouse, is shown to be controlled by a single autosomal dominant gene R (recessive gene designated r). This resistance could be transferred to uninfected hosts with lymphoid cells but not serum from infected resistant animals. Treatment with heterologous antilymphocyte serum depressed the ability of competent hosts to resist infections. A comparison of the response elicited against 2 strains of H. citelli (Utah and California) illustrated that chance-bred P. m. sonoriensis respond more rapidly and in greater incidence to the California strain than to the Utah strain. Homozygous recessive (r/r) hosts, susceptible to H. citelli (Utah), respond in significant numbers to the California strain of the tapeworm. Natural infections of H. citelli in Peromyscus do not occur uniformly throughout the environment but occur in small foci favoring existence of both intermediate and definitive hosts. Infections rarely occur outside such foci. We postulate that H. citelli is propagated in such foci by genetically nonimmune (r/r) hosts comprising about 25% of the host population. A previous study (Wassom et al., 1973), utilizing the tapeworm Hymenolepis citelli and its natural host Peromyscus maniculatus, illustrated that a tapeworm living exclusively in the gut lumen could elicit a protective resistance in some individuals. Such hosts, after initial acceptance of infection, responded by eliminating the worms and resisting reinfection. Other individuals were incapable of developing resistance. Primary infections were maintained and secondary infections could be imposed upon initial ones. The present study was conducted to evaluate the genetic aspects of this host resistance, and to determine whether the response is mediated by specific immune mechanisms or by nonspecific factors. MATERIALS AND METHODS All experimental animals were laboratory-reared Peromyscus maniculatus sonoriensis fed Purina Laboratory Chow. The isolation of H. citelli from wild-caught P. maniculatus and its maintenance in the laboratory as well as procedures for infection have been previously reported (Wassom et al., 1973). Immune serum was pooled from 2 groups of chance-bred P. maniculatus infected on day 0 with 10 cysticercoids of H. citelli, challenged with reinfection on day 14 or 21, and bled 7 days later. Received for publication 16 July 1973. * Department of Biology, University of Utah, Salt Lake City, Utah 84112. t Department of Pathology, University of Utah, Salt Lake City, Utah 84112. 47 Lymphoid-cell suspensions from the thymus, spleen, and lymph nodes of infected animals were prepared by mincing the tissues in Minimal Essential Medium for Suspension-Earle's BSS (MEMMicrobiological Associates), filtering through nylon gauze, and centrifuging at 60 g for 10 min. Red blood cells were lysed with Tris-buffered hypotonic ammonium chloride (Boyle, 1968), and the cells washed 4 times in MEM. Viability of cells was determined by trypan blue exclusion (Boyse et al., 1962). Cell concentrations were determined with standard microscopic counting chambers. Antilymphocyte serum (ALS) was prepared in rabbits by injection of Mus musculus lymphoid cell membranes in Freund's complete adjuvant. Injection of 0.5 ml of this ALS intraperitoneally on days 0, 2, and 4 was shown to delay median rejection times of Mus musculus allogeneic skin grafts (H2' to H2k) from 10.5 to 13.7 days. Skin grafts were not attempted in P. maniculatus. However, injection of 0.4 ml ALS intraperitoneally to P. maniculatus on days 0, 2, and 4 was shown to reduce hemagglutinin titers to SRBC by 4 doubling dilutions. This ALS is thus an effective immunosuppressive agent in P. maniculatus.