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History of Research on C. Elegans and Other Free-Living Nematodes As History of research on C. elegans and other free-living nematodes as model organisms* Victor Marc Nigon1 and Marie-Anne Félix2§ 1Université de Lyon 1, France 2Ecole Normale Supérieure, Paris, France Table of Contents 1. Introduction ............................................................................................................................3 2. Methods .................................................................................................................................5 2.1. Culture ........................................................................................................................5 2.2. Cytological methods ...................................................................................................... 7 3. Hermaphroditism: selfing and crossing with males ......................................................................... 7 3.1. Protandric hermaphroditism as a modification of the female .................................................. 8 3.2. Variation in hermaphroditism among different species .......................................................... 9 3.3. Crosses in hermaphroditic species .................................................................................... 9 3.4. Biological species test through crosses: C. briggsae discovery ............................................. 10 3.5. Evolution of selfing from male-female ancestors ............................................................... 11 4. Sex determination and meiosis in sexual species .......................................................................... 12 4.1. Chromosomal sex determination in gonochoristic species ................................................... 12 4.2. Chromosomal sex determination in hermaphroditic species ................................................. 12 4.3. Meiosis in a sexual species, C. elegans ............................................................................ 13 4.4. The X-chromosome-to-autosome ratio in sex determination: use of a tetraploid line ................. 15 5. Parthenogenesis ..................................................................................................................... 19 5.1. True parthenogenesis ................................................................................................... 19 5.2. Pseudogamy ............................................................................................................... 19 6. Embryonic development ......................................................................................................... 24 6.1. Asymmetry of the first division ...................................................................................... 24 6.2. Eutely ....................................................................................................................... 28 7. Post-embryonic development ................................................................................................... 28 * Edited by Paul W. Sternberg. Last revised October 11, 2015. Published in its final form September 07, 2017. This chapter should be cited as: Nigon, V.M., and Félix, M.-A. History of research on C. elegans and other free-living nematodes as model organisms. (September, 07, 2017), WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.181.1, http://www.wormbook.org. Copyright: © 2017 Victor Marc Nigon and Marie-Anne Félix. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. §To whom correspondence should be addressed. Email: [email protected] 1 History of research on C. elegans and other free-living nematodes as model organisms 8. The alternation of generations .................................................................................................. 29 8.1. Gonochoristic free-living and hermaphroditic parasitic generations: Rhabdias bufonis .............. 30 8.2. Gonochoristic free-living and parthenogenetic parasitic generations: Strongyloides ratti ........... 30 9. Genetics ............................................................................................................................... 32 9.1. Preliminaries .............................................................................................................. 32 9.2. The first mutants ......................................................................................................... 32 9.3. Natural variation in temperature resistance ....................................................................... 33 9.4. Classical genetics in Brun's team before 1974 ................................................................... 34 9.5. Classical genetics in Brun's team after 1974 ..................................................................... 35 10. Adaptation to high temperature ............................................................................................... 36 10.1. Progressive sterility and acclimatization behaviors ........................................................... 36 10.2. Reversibility of the adaptation and effect on the germ line ................................................. 36 10.3. Hypotheses of non-genic factors and induction by high temperature .................................... 37 11. Effect of parental aging on fertility of the next generation ............................................................ 38 12. Before and after Sydney Brenner ............................................................................................. 39 12.1. C. elegans as a genetic model system ............................................................................ 40 12.2. The advent of molecular biology with C. elegans ............................................................. 44 13. Epilogue ............................................................................................................................. 45 13.1. At the core of genetics: reproduction, sex determination, meiosis, and polyploidy .................. 46 13.2. Progressive multigenerational sterility and acclimatization ................................................ 47 14. Acknowledgements .............................................................................................................. 48 15. References .......................................................................................................................... 48 16. Appendix 1. Table 3. Main species mentioned in the text with their modern names and mode of reproduction. ............................................................................................................................ 66 17. Appendix 2. The C. elegans Bergerac strain. ............................................................................. 68 17.1. France FR sublineage ................................................................................................. 69 17.2. Berkeley sublineage ................................................................................................... 69 17.3. Cambridge sublineage ................................................................................................ 69 17.4. Boulder BO sublineage ............................................................................................... 70 18. Appendix 3. Biographies ....................................................................................................... 70 18.1. Emile Maupas (1842-1916) ......................................................................................... 71 18.2. Paula Hertwig (1889-1983) .......................................................................................... 72 18.3. Karl Franz Joseph Belar (1895-1931) ............................................................................ 74 18.4. Victor Marc Nigon (11 October 1920 - 5 July 2015) ......................................................... 75 18.5. Ellsworth C. Dougherty (1921-1965) ............................................................................. 81 18.6. Jean-Louis Brun (1927-1981) ....................................................................................... 83 Abstract 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
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