History of research on C. elegans and other free-living nematodes as model organisms.
The nematode Caenorhabditis elegans is now a major model organism in biology. The choice of Sydney Brenner to adopt this species in the mid-1960s and the success of his team in raising it to a model organism status have been told (http://www.wormbook.org/toc_wormhistory.html; Brenner, 2001; Ankeny, 2001). Here we review the pre-Brenner history of the use of free-living nematodes as models for general questions in biology. We focus on the period that started in 1899 with the first publication of Emile Maupas mentioning Rhabditis elegans and ended in 1974 with the first publications by Brenner. A common thread in this period, aided by the variety in modes of reproduction of different nematode species, is found in studies of meiosis, fertilization, heredity, and sex determination. Maupas in his 1900 opus on reproduction had already chosen C. elegans as the species of reference. Hikokura Honda determined its hermaphrodite chromosomal content in 1925. C. elegans was again isolated and chosen as a main subject by Victor Nigon in the 1940-50s. Nigon mastered crosses between C. elegans hermaphrodites and males, described the meiotic behavior of chromosomes in XX hermaphrodites and X0 males and, using tetraploids, correctly inferred that sex was determined by X chromosome to autosome dosage. With Ellsworth Dougherty, Nigon isolated and studied a C. briggsae body size mutant and a C. elegans slow growth mutant. Dougherty and his team devoted most of their work to finding a defined culture medium to screen for physiological mutants, focusing on C. briggsae. With Helene Fatt, Dougherty also performed the first genetic study of natural variation in C. elegans, concerning the difference in heat resistance of the Bergerac and Bristol strains. Jean Brun, a student of Nigon, performed a long and remarkable experiment in acclimatization of C. elegans Bergerac to higher temperatures, the significance of which remains to be clarified.
Université de Lyon, France.
Victor Marc
VM
Nigon
Ecole Normale Supérieure, Paris, France.
Marie-Anne
MA
Félix
D000222:Adaptation, Physiological; D000375:Aging / Q000502:physiology; D000818:Animals; D035843:Biomedical Research / Q000266:history*; D017173:Caenorhabditis elegans / Q000196:embryology / Q000235:genetics / Q000254:growth & development; D005298:Fertility; D057850:Hermaphroditic Organisms; D049672:History, 19th Century; D049673:History, 20th Century; D008540:Meiosis; D023421:Models, Animal; D010312:Parthenogenesis; D012732:Sex Determination Analysis; D013696:Temperature