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A Brief Autobiography Relative to Work with Inbred and Mutant Mice

Earl L. Green

The Jackson Laboratory
Bar Harbor, Maine

I was walking across the campus of Allegheny College in Meadville, Pennsylvania, one day early in June of 1932. Examinations were over. I was almost 19 years old and I had just completed my freshman year of college. Approaching me from the opposite direction was the professor, Dr. Darling, under whom I had taken my first year-long course in biology. Dr. Chester Arthur Darling was a large man with gruff but kindly ways of dealing with students. He had been a professor at Allegheny for nearly 15 years after having completed his study for the Ph.D. degree at Columbia University.

He said to me, "Say, Green, you live in town, don't you? How would you like to take care of the mouse colony this summer? The chap who has been doing the job is going to be away."

I must have said, "Yes," because soon I was engaged in the daily ritual of feeding and watering about 50 pens of mice and the weekly tasks of trying to clean and repair the wooden pens. I got bored with pouring water into clean dishes, placing them in the mouse pens, and observing soon thereafter that the mice had pushed the bedding into the dishes and, a little later, that they had defecated and urinated into the dishes as well. I'm not sure I knew those four-syllable words at that time. I devised an automatic watering system, based on the hanging-drop principle now in universal use. My system was, however, crude and inefficient compared with later devices. I had trouble getting the aperture, through which the droplets of water were to pass, small enough to suspend the drops and not allow water to run continuously. I was grateful for the advances, made by others, of devising glass "goosenecks" and stainless steel sipper tubes. I continued the husbandry of mice through the rest of my years at Allegheny.

Shortly after I started tending the mice, Dr. Darling referred to one of the stocks as "the strong strain." This made me a bit timid about dealing with them. Even though they looked tame enough, I didn't want to test their strength just yet. The next summer, Dr. Darling introduced me to a visitor, Dr. Leonell C. Strong of The Roscoe B. Jackson Memorial Laboratory in Bar Harbor, Maine. It dawned on me eventually that I had been husbanding "the Strong strain," for Dr. Strong had given some breeding pairs of his Strain A mice to Dr. Darling some years earlier. This was my first contact with an inbred strain of mice.

During my second year at Allegheny, I took a course in heredity. One day, in the mouse room, Dr. Darling asked me if I had thought of any project I might undertake with mice. I said I wanted to cross a black mouse with a brown mouse and to mate the offspring together to see if I got a litter with three black mice and one brown mouse in it.

Dr. Darling said, "What are you going to do if the litter has five mice in it?"

The look of perplexity, commingled with chagrin, that swept over my face must have amused Dr. Darling. The next thing I heard was, "Heh, heh, heh."

It wouldn't have been so bad if he had not laughed. I was playing the role of a carefree trout that had taken a beautiful fly; that laugh sunk the hook in. Damn it, why hadn't I thought of that? I know very well that mice had litters ranging from one or two up to 12 or 13. Clearly there was only one thing to do: charge ahead and hope for revelation later.

I made up the matings between black and brown mice and between members of the F1 generation to produce the F2 generation. I devised a system of record-keeping that with successive modifications, served me through four decades. With the data in hand, I went to the library -- "Heh, heh, heh," still sounding in my ears -- to see if I could get help in understanding what I had found. Remember the time is 1933, and the statistical resources available to students in a small general college library were primitive compared with those of the present. Actually, I was not able to resolve the question until 1937 when I was in graduate school. That is when Snedecor's first edition of Statistical Methods appeared. Then I learned about attributes (now called discrete variables), probability, the binomial distribution, the computation of expected frequencies, and the testing of deviations of observed from expected numbers by the use of the chi-square distribution.

Having gone to the library for one purpose, I developed the habit of returning for another. The college had just completed a new wing on its library building. In it were individual study carrels near the stacks. The librarian assigned me one of the carrels, and I started to search books and journals for information about mouse genetics. I became familiar with Genetics, The American Naturalist, Journal of Heredity, Science, and many other journals. I also met the names and the works of Morgan, Castle, Little, Wright, Haldane, Darbyshire, Detlefsen, Gates, Snell, Dunn, Keeler, and many others. One day the librarian gave me a copy of a publication she was about to discard. It was a paper-bound monograph of the Carnegie Institution of Washington dated 1914. It contained C.C. Little's doctoral dissertation on mouse breeding experiments, submitted to the Harvard faculty in fulfillment of the requirements for the doctoral degree. It contained several plates, in color, of mice of various coat colors. It would be another 50 years before colored photographs of mice appeared in print for the aid of the novice.

My project as a college student laid the foundation for my lifelong interest in genetics and statistics. What had been an accidental meeting on a college campus led to my decision to major in biology as an undergraduate. That, in turn, led to the decision to pursue graduate work in genetics.

In the fall of 1936, I entered the Graduate School of Brown University in Providence, Rhode Island, as a teaching assistant in comparative anatomy of the vertebrates and as an advisee of Dr. Herbert Eugene Walter and Dr. Paul Baldwin Sawin. The other teaching assistant was a red-haired girl named Margaret Creighton, from New London, Connecticut.

Dr. Sawin advised me to take a course in statistics offered by Professor A.A. Bennett in the Mathematics Department. The course was a valuable introduction to the concepts and methods of statistics. More valuable was a friendship with Professor Bennett that continued throughout my five years at Brown. He helped a small self-organized group of graduate students to conduct a study of Snedecor's first edition of Statistical Methods.

Dr. Sawin had recently discovered a skeletal variation in his stocks of rabbits. I became interested in seeing if similar variations occurred in existing inbred strains of mice. We procured samples of various strains of mice from The Jackson Laboratory in Bar Harbor and from Dr. Strong who was then at Yale University. It turned out that there were four primary types of axial skeletons with respect to the ratio of thoracic-to-lumbar vertebrae. Some strains had 13/6 as the typical numbers. This was regarded as "normal" or "standard." Some strains, however, had 13/5, some had 13/7, and some had 12/7 as typical numbers. The mice within strains were similar, but not identical. Each strain produced a small percentage of mice that were not typical of the strain. This was my own first-hand encounter with the idea of variation within an inbred strain. Many years earlier, in 1905, Johannsen had established that pure lines of beans exhibit variation and do not respond to selection. The idea of nongenetic variation within inbred strains of mice is still, today, a difficult idea for some people to grasp.

I decided to carry out an intensive analysis of the visibly most variable of the strains, the Bagg albino strain (denoted as BALB/cJ in now-conventional symbols), modeled upon the classical analysis that Sewall Wright had then recently published on the inheritance of three and four toes in guinea pigs. I found that, in the Bagg albino strain, the parent-offspring and the sib-sib correlations were essentially zero, showing that variation within the strain had primarily nongenetic causes ( 1).

While I was a graduate student at Brown, I arranged to spend part of two summers, 1938 and 1939, at The Jackson Laboratory, primarily to sample more strains of mice for skeletal variations. Dr. C.C. Little, to whom I first wrote, responded with characteristic enthusiasm inviting me to be under the tutelage of Dr. W.L. Russell, then on the staff. It was then that I also met, for the first time, Dr. Elizabeth Russell, Dr. George D. Snell, and Dr. Walter E. Heston. Aside from the scientific value of those two summers, they were enlightening in another important way. I discovered that to be interested in the genetics of the mouse need not be a solitary endeavor. There were others who were seriously and professionally occupied in advancing knowledge in this domain. At the time I was there, the staff of The Jackson Laboratory was deeply occupied in preparing manuscripts for the Biology of the Laboratory Mouse, published in 1941, under the editorship of George Snell.

While I was at Brown, I became interested in the problem of trying to discover the intimate multiple effects of single named mutations in the mouse. A candidate gene for such studies seemed to be the short-ear ( se) mutation, discovered in 1921 by Dr. Clara Lynch. I decided to make this the major effort of a year of postdoctoral research at the University of Chicago under the sponsorship of Professor Sewall Wright. Brown University awarded me a Corinna Borden Keen Fellowship to make such a year possible ( 2).

But first things first. A few days after I arrived in Chicago, Margaret Creighton also, by prearrangement, arrived. Less than a week later, we were married. Margaret had stayed at Brown as a graduate student for two years and then had gone to the State University of Iowa at Iowa City to complete her work for the Ph.D. degree in cytogenetics under the supervision of Dr. William Rees Brebner Robinson. Together, Margaret and I undertook the analysis of the effects of the short-ear gene. Our study was designed as a comparison of mice of two short-eared strains, P and NB, with mice of a normal-eared strain, Bagg albino. It took very little imagination to realize that any difference we might find between the strains could be due to any number of causes other than the alleles of the se locus ( 3).

I spent much of that year trying to comprehend the details of a paper by Bartlett and Haldane, published in 1935, on the theory of inbreeding with forced heterozygosis. The idea of mating brother and sister mice, deliberately selected to preserve heterozygosity at a specified locus, was easy enough to comprehend. But the method of analysis -- the generation matrix method introduced by Bartlett and Haldane -- required a bit more study. In any case, we decided to create some new inbred strains, each segregating for the two alleles at the se locus. Of the five strains we started at the time, two have survived to the present: SEA/GnJ and SEC/1Gn. To the best of our knowledge, these were the first strains of mice deliberately bred as segregating inbred strains. Now there are dozens of such strains. They are among the strains of choice when one wishes to discover the effects of a named mutation on any aspect of the biology of the mouse.

We moved to Columbus, Ohio, -- mice and all -- in 1941 upon my appointment to the faculty of the Ohio State University. The pursuit of the multiple effects of the alleles of the se locus was carried forth after that time largely by Margaret Creighton Green ( 4). In the time available, which was not much because of military service and, after the war, because of heavy teaching loads, I continued the analysis of skeletal variations by carrying out classical crosses between several pairs of strains differing in skeletal types ( 5, 6, 7, 8, 9, 10, 11).

During our period in Ohio State University, I discovered a marked difference in skeletal types between sublines of the C3H strain. I had procured samples of C3H mice from eight sources and found that they fell into to groups: one group with five lumbar vertebrae, the other with six. I recommended that C3H mice be carefully denoted as C3H/St or C3H/He ( 12). During this same period, I also carried out the genetic analysis of a new condition, called furless ( fs) ( 13).

In 1956, Margaret and I moved our household goods to Bar Harbor and our mouse colony to The Jackson Laboratory. I had just been appointed to succeed D. C.C. Little as director of the Laboratory, and we had both been appointed to the research staff.

My major research effort, starting at this time and continuing for about 18 years, was an attempt to detect the effects of various levels of ionizing radiation on the genetic makeup of small populations of mice. I started the experiments with two kinds of mice: 1) a founding population, called "inbred," that traced ancestry to a single pair in the C57BL/10Gn strain, and 2) a founding population, called "hybrid," that traced ancestry to four inbred strains, C57BL/6J, DBA/2J, C3HeB/FeJ, and BALB/cJ. I deliberately varied the sizes of the experimental populations to provide four levels of inbreeding in the populations in each experiment. The idea was that lower levels of inbreeding favor the accumulation of recessive mutations, both viable and lethal, and that the "hybrid" populations would be able to withstand the effects of accumulated mutations more easily than the "inbred." The surprising outcome of these experiments was that essentially nothing affecting fitness traits seemed to happen in the populations. They continued for 20 generations with essentially no change ( 14, 15, 16, 17, 18, 19).

Several other investigators had designed somewhat comparable experiments about the same time. At a symposium held at The Jackson Laboratory in 1964 and in subsequent publications, they reported essentially negative results as well ( 20, 21).

Another project required less of my time. In the early 1960s, The Jackson Laboratory was producing about a million mice per year in 18 different inbred strains and six F1 hybrid generations. I organized a large-scale study to estimate the natural mutation rates of the mouse. The project extended over seven years and entailed examining seven million mice; it became a major endeavor of Dr. Margaret M. Dickie and Dr. Gunther Schlager ( 22).

Throughout my period at The Jackson Laboratory, I tried to make various aspects of the mouse-breeders art comprehensible to research workers in other fields, so they could make better choices of the kinds of mice to use in their research. For instance, when should one use inbred vs. random-bred mice? How much genetic uniformity can one expect after a given number of generations of brother-sister inbreeding? How efficient are the methods of producing segregating inbred strains and congenic inbred strains? What is the special value of coisogenic inbred strains? I had two opportunities to write expository papers on these questions for publication in the scientific literature ( 23, 24).

Another major endeavor was the organizing and editing of a second edition of the Biology of the Laboratory Mouse, which came put in 1966 and was republished in 1975 ( 25).

I had the good fortune to discover four useful mutations in the mice in my research stocks: opossum ( Raop), pale ears ( ep), shambling ( shm), and a remutation to albinism ( c2J) ( 26, 27, 28, 29).

Between the summer of 1932, when I started working with mice, and the summer of 1975, when I retired, I think I have learned a fair amount about the genetics and biology of the mouse. I might even be able to handle a questions such as, "What will you do if there are five mice in the litter?"

REFERENCES

1. Green, E.L. (1941). Genetics 26: 192.

2. Green, E.L., and McNutt, C.W. (1941). J. Hered. 32: 94.

3. Green, E.L., and Green, M.C. (1942). J. Morphol. 70: 1.
See also MGI.

4. Green, E.L., and Green, M.C. (1946). Am. Naturalist 80: 619.

5. Green, E.L., and Green, M.C. (1946). J. Morphol. 78: 105.

6. Green, E.L., and Green, M.C. (1946). J. Morphol. 78: 113.
See also MGI.

7. Green, E.L. (1951). Genetics 36: 391.

8. Green, E.L., and Russell, W.L. (1951). Genetics 36: 641.

9. Green, E.L. (1954). J. Natl. Cancer Inst. 15: 609.
See also PubMed.

10. Green, E.L., and Green, M.C. (1959). J. Hered. 50: 109.

11. Green, E.L. (1962). Genetics 47: 1085.
See also MGI.

12. Green, E.L. (1953). Science 117: 81.
See also MGI.

13. Green, E.L. (1954). J. Hered. 45: 115.
See also MGI.

14. Green, E.L. (1964). Genetics 50: 417.
See also PubMed.

15. Green, E.L. (1964). Genetics 50: 423.
See also PubMed.

16. Green, E.L., and Les, E.P. (1964). Genetics 50: 497.
See also PubMed.

17. Green, E.L., Roderick, T.H., and Schlager, G. (1964). Genetics 50: 1053.
See also PubMed.

18. Green, E.L. (1968). Radiat. Res. 35: 263.
See also PubMed.

19. Green, E.L. (1968). Mutat. Res. 6: 437.
See also PubMed.

20. Green, E.L. (ed.). (1964). Genetics 50: 1023.

21. Green, E.L. (1968). Ann. Rev. Genetics 2: 87.

22. Green, E.L., Schlager, G., and Dickie, M.M. (1965). Mutat. Res. 2: 457.
See also PubMed.

23. Green, E.L., and Doolittle, D.P. (1963). In "Methods in Mammalian Genetics" (W.J. Burdette, ed.), p. 3. Holden-Day, Inc., San Francisco.

24. Green, E.L. (1966). In Biology of the Laboratory Mouse, 2nd edition (E.L. Green, ed.) p. 11. McGraw-Hill Book Co., New York.

25. Green, E.L. (ed.). (1966). Biology of the Laboratory Mouse, 2nd edition. McGraw-Hill Book Co., New York; 1975, Dover Publications, Inc., New York.

26. Green, E.L., and Mann, S.J. (1961). J. Hered. 52: 223.
See also MGI.

27. Lane, P.W., and Green, E.L. (1967). J. Hered. 58: 17.
See also PubMed.

28. Green, E.L. (1967). J. Hered. 58: 65.
See also MGI.

29. Green, E.L. (1968) J. Hered. 59: 59.
See also MGI.

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