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Perspectives Copyright Ó 2007 by the Genetics Society of America Perspectives Anecdotal, Historical and Critical Commentaries on Genetics Edited by James F. Crow and William F. Dove What Did Sutton See?: Thirty Years of Confusion Over the Chromosomal Basis of Mendelism Matthew Hegreness* and Matthew Meselson†,1 *Department of Systems Biology, Harvard Medical School, Boston, Massachusetts 02115 and Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138 and †Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts 02138 and Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Laboratory, Woods Hole, Massachusetts 02543 N December 1902, 2 years after the rediscovery of of discovery leading to the present understanding of the I Mendel’s 1865 article, America’s leading cytologist, chromosomal basis of inheritance. Edmund Beecher Wilson, announced to the readers of Although correct in its essentials, Sutton’s analysis Science that a graduate student of his at Columbia contained a critical flaw. As did others at the time, University had discovered the physical basis of the Sutton identified the wrong division of meiosis as the ‘‘Mendelian principle,’’ by which Wilson meant the reducing division, the division in which paternal and segregation of Mendelian factors (Wilson 1902). In an maternal chromosomes separate. Sutton thought that article published the following year, which became a the separation of paternal and maternal chromosomes classic of genetics, this student, Walter Stanborough and their independent assortment take place during the Sutton, explained how the behavior of chromosomes second meiotic division, while actually they (or, more during meiosis—as he interpreted it in his observations precisely, their centromeres2) separate and indepen- of spermatogenesis of the grasshopper Brachystola dently assort at the first division. magna—could explain not only Mendelian segregation Estella Eleanor Carothers, who in 1913 presented the but also Mendelian assortment. Sutton had done much first clear cytological evidence for the independent of the cytological work as a student of Clarence Erwin assortment of chromosomes, nevertheless perpetuated McClung at the University of Kansas, but his inter- Sutton’s misconception. Carothers followed Sutton as a pretation of his results in light of Mendelism was done at student of McClung at the University of Kansas and, like Columbia. Supposing that Mendel’s factors were located Sutton, studied spermatogenesis in Brachystola. Exam- on chromosomes, he realized that the ‘‘association of ining slides that Sutton had left behind as well as those paternal and maternal chromosomes in pairs and their she and McClung prepared, Carothers correctly de- subsequent separation during the reducing division scribed the segregation and independent assortment of ½of meiosis’’ could explain Mendelian segregation certain recognizable chromosomes in the first division (Sutton 1902, p. 39) and that Mendelian factors on dif- of meiosis. Nevertheless, she supposed that segregation ferent chromosomes would assort independently if, at and assortment take place in the second division for all the division in which paternal and maternal chromo- other chromosomes. Confusion over which of the two somes separate ‘‘any chromosome pair may lie with meiotic divisions was reductive would linger for another maternal or paternal chromatid indifferently toward 20 years. Despite histories of genetics crediting Sutton either pole irrespective of the positions of other pairs’’ for explaining the chromosomal basis of Mendelism, no (Sutton 1903, p. 234). Although Sutton’s conclusions single work marks the clarification of the understanding gained general acceptance only gradually (Morgan of the meiotic divisions. Instead, clarification came from 1910; Bateson 1922), his brilliant insight brought the gradual accumulation and integration of cytological cytology and genetics together, initiating the long path 1Corresponding author: Department of Molecular and Cellular Biology, 2Because of crossing over, unknown to Sutton, it is more accurate to say Harvard University, Cambridge, MA 02138. that centromeres, rather than whole chromosomes, segregate at the first E-mail: [email protected] division of meiosis. Genetics 176: 1939–1944 (August 2007) 1940 M. Hegreness and M. Meselson and genetic observations over more than a quarter of a camera lucida drawings of its appearance in the meiotic century. divisions of the testis. The second article, written when Sutton was a doctoral candidate at Columbia, ‘‘On the morphology of the chromosome group in Brachystola SUTTON’S THEORETICAL INSIGHTS AND magna’’ (S utton 1902, p. 26), argues that the ‘‘ordinary CYTOLOGICAL CONFUSION chromosomes’’ (i.e., autosomes) may be arranged in To understand the significance of Sutton’s theoretical pairs according to their prophase lengths and volumes advances, as well as the cytological misunderstandings and that ‘‘the same number and size-relations of under which he labored, it is important to understand chromosomes’’ are seen through consecutive cell divi- the state of biology at the turn of the century. Gregor sions. From this and his observations of synapsis, Sutton Mendel’s principles of heredity, so clearly put forward in drew four essential conclusions: (1) chromosomes have his 1865 article, were ignored for 35 years. Their re- morphological individuality; (2) chromosomes come in discovery in 1900 marked the birth of genetics. Neverthe- homologous pairs according to their size, with one from less, the end of the 19th century saw a flourishing of each pair inherited from the mother and one from the cytological observations and theoretical advances that father; (3) chromosomes of each pair synapse before rendered biologists receptive to Mendel’s analysis and the meiotic divisions; and (4) synapsed chromosomes 3 conclusions. The second edition of E. B. Wilson’s The Cell separate during meiosis. in Development and Inheritance, written without any knowl- While these conclusions are correct, Sutton cited no edge of Mendelism, appeared in 1900 and provides an specific observation that would have allowed him to distinguish the maternal and paternal members of a authoritative window on turn-of-the-century cytology. homologous pair of autosomes and therefore had no Many things were already known about chromosome way of identifying the meiotic division in which they behavior by 1900, including that the somatic chromo- separate and independently assort. His unsupported some number is preserved through successive mitoses claim that these events occur in the second division is, in and halved during meiosis. Writing that the reduction in fact, wrong. chromosome number that accompanies meiosis is not What might have led Sutton to misidentify the di- only ‘‘very obviously a provision to hold constant the vision in which parental chromosomes separate? Sutton number of chromosomes characteristic of the species,’’ believed, correctly, that the first of the two meiotic Wilson went on to point out that, if chromatin is the divisions is longitudinal,4 but was wrong in thinking that physical carrier of inheritance, ‘‘aninfinite complexity of it is ‘‘essentially like that occurring in ordinary mitosis’’ the chromatin would soon arise did not a periodic (Wilson 1900, p. 286) and therefore equational. In ilson reduction occur’’ (W 1900, pp. 243 and 245). It Sutton’s words: was this consideration, upon which August Weismann (1887) based his famous prediction, that meiosis must When the ordinary chromosomes ½autosomes divide in the first mitosis of the spermatocytes, the separation takes entail a reduction division. In this sense, reduction refers place along the line of the longitudinal split and there- to a halving of genetic complexity, not merely to a fore, except that the chromosomes are joined together by reduction in chromosome number. pairs, differs in no respect from an ordinary spermatogo- By 1903, when Sutton advanced his interpretation of nial division. Sutton (1902, p. 32) meiosis in terms of Mendelian segregation and assort- ment, there was substantial reason to believe that spe- Sutton’s misidentification of the first division as cific chromosomes carried specific hereditary factors. equational was apparently influenced by the mistaken Thomas Harrison Montgomery (1901), studying sper- belief, then held also by McClung, Montgomery, and matogenesis in Hemiptera, had noted the continuity Wilson, that maternal and paternal chromosomes join and morphological individuality of chromosomes, and end to end during synapsis and that the second meiotic Theodor Boveri (1902), in his studies of double- division is transverse,5,6 separating paternal and mater- fertilized sea urchin eggs, provided evidence that chromo- nal chromosomes: somes differ qualitatively in their effects on development. Also, it had been concluded by Montgomery (1901) that at the synapsis stage, maternal chromosomes unite 3Sutton acknowledged in his 1902 article that Montgomery (1901) with paternal chromosomes rather than maternal with had drawn essentially the same conclusions. 4 maternal and paternal with paternal. Longitudinal separation meant the separation of chromosomes utton aligned side by side. Sutton wrote three articles (S 1900, 1902, 5Transverse separation meant the separation of chromosomes joined 1903) on the morphology and behavior of chromo- end to end. somes in Brachystola. The first, ‘‘The spermatogonial
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