Contribution of Cytologia to Drosophila Studies across the World

Abstract

Since its inception in 1929, Cytologia has made several significant contributions to the international community, including supporting various discoveries in Drosophila. These experiments were not only successful in D. melanogaster but also other species, such as D. virilis and D. ananassae. This is because the two founding Fly Rooms in Japan, one at Kyoto University and the other at Tokyo Metropolitan University, included these species in their evaluations. Many other Drosophila species have also been analyzed at the cytological, genetic, and evolutionary levels by various researchers from across the world with many of these findings subsequently discussed in Cytologia papers.

Cytologia, the International Journal of Cytology, was launched in 1929 and was initially edited by Kenjirō Fujii, an Emeritus Professor at Tokyo Imperial University, and 236 standing collaborators from across Europe, North America, and Japan. These collaborators as of October 1930 included three rediscoverers of Mendelism (C. E. Correns, A. v. Tschermak, and H. de Vries) and at least 42 researchers (17.8%) recognized by citation search in the FlyBase (Gramates et al. 2022, flybase.org). Among them those who have publications on Drosophila studies are C. B. Bridges (misprinted as E. B. Bridges), R. E. Clausen, C. D. Darlington, M. Demerec, R. Goldschmidt, O. Heilborn, E. Heitz, G. Hertwig, E. C. Jeffrey, B. P. Kaufmann, H. Kihara, T. Komai, C. W. Metz, O. L. Mohr, T. H. Morgan, T. S. Painter, K. Sax, Y. Sinotô, E. B. Wilson, and K. Yasui. It should be noted that while the inclusion of Hitoshi Kihara and Yosito Sinotô may sound strange since their primary research materials were well known to be plants, the former introduced Japanese papers on Drosophila to the English-speaking world (Kihara 1950) and compared the genetics of Drosophila and silkworm (Kihara 1953) and the latter introduced Drosophila handling techniques to beginners (Sinotô 1931) and completed the initial analysis of the salivary gland chromosomes by himself (e.g., Sinotô and Yuasa 1935). E. Heitz, T. S. Painter, and C. B. Bridges are also important as they were amongst the earliest researchers to note and speculate on the importance of salivary gland chromosomes in the genetic evaluation of Drosophila (Heitz and Bauer 1933, Painter 1933, Bridges 1934). Thomas Hunt Morgan, the Nobel Prize laureate in 1933, and Bridges both from the Fly Room at the California Institute of Technology, which was relocated from Columbia University in 1928, are included in this list, but H. J. Muller, T. Dobzhansky and A. H. Sturtevant are not. Muller moved to the University of Texas in 1920, and F. Schrader who co-authored a paper with Sturtevant (Schrader and Sturtevant 1923) is instead in the list. An additional four Japanese scientists (Umé Tsuda, Naohide Yatsu, Taku Komai, and Yoshitaka Imai) are known to have studied in the Morgan lab, next to the E. B. Wilson lab at Bryn Mawr College and later at Columbia University, but only T. Komai is listed here.

The earliest Cytologia paper that cited Drosophila studies was Sinotô (1929), where Bridges (1925) and Morgan (1926) were mentioned in the context of the cytological basis of sex determination. However, the earliest Cytologia paper included in the FlyBase (Gramates et al. 2022, flybase.org) is Haldane (1931), a theoretical paper dealing with interference during the crossover, a fundamental problem in genetics at the time, which contributed to the elaboration of linkage maps. Strictly speaking, the earliest Cytologia paper discussing Drosophila was Kikkawa (1932a), in which D. virilis was used as the experimental material for evaluations of crossover, interference, and linkage. The Komai lab at Kyoto Imperial University was similar to Morgan’s Fly Room in that they used D. virilis instead of D. melanogaster and published a series of papers in Cytologia (Kikkawa 1932a, b, 1935a, b, Chino and Kikkawa 1933, Fujii 1936). Mitsushige Chino, who had been a high school teacher in Nagano Prefecture before joining the Komai lab, was a mutant hunter, and several members of this lab collaborated with each other. Chino started Drosophila breeding from those collected in Kami-Suwa in 1921 without any knowledge of Morgan’s studies (Chino 1927, 1929, Sinotô 1931). Among the members Hideo Kikkawa also focused on Drosophila taxonomy across Asia (Kikkawa and Peng 1937) and later moved into biochemical genetics using other materials such as silkworms, ultimately helping him produce the one-gene-one-enzyme theory (Kikkawa 1953). Demerec and Lebedeff (1934) also published a D. virilis paper, solving the problem of proximo-distal order in X-linkage, and Yasui (1935) and Prokofyeva-Belgovskaya (1935) published D. melanogaster papers outlining the detailed structures of the salivary gland chromosomes. Kono Yasui was the first female doctor in Japan to work with Kenjirō Fujii and she used the D. melanogaster material provided by Sinotô (Yasui 1935).

In 1937, Cytologia published a special volume celebrating the 70^th birthday (November 11, 1936) of Kenjirō Fujii with various famous cytologists from across the world contributing to this special issue. Of the 120 papers published, 10 (8.3%) were identified as a citation in FlyBase (Gramates et al. 2022, flybase.org). These included Huskins (1937) who described the general chromosome structure, Mather (1937) who discussed the relationship between crossover and chiasmata, and Metz (1937) who described the salivary gland chromosomes from Sciara, another Dipteran species. Strictly speaking, the other seven studies were all on Drosophila as well. Bridges (1937), Demerec (1937), and Sokolow (1937) studied the salivary gland chromosomes of D. melanogaster. In those days, chromosomal aberrations (e.g., deficiency, duplication, inversion, and translocation) attracted cytologists, who studied the relationship between crossover and changes in chromosome arrangement. Goldschmidt (1937) also used D. melanogaster (although he does not specify the species in this paper) and described the development of a gynandromorph resulting from double fertilization. Interestingly, three other scientists published papers on D. ananassae in this volume: Kaufmann (1937) who analyzed the relationship between karyotypes (mitotic chromosomes) and salivary gland chromosomes; Kikkawa (1937) who was interested in heterochromatic chromosome 4, because of its absence in the salivary gland; and Moriwaki (1937) who studied the complex mechanism of the bobbed (bb) inheritance. Unlike D. melanogaster and D. virilis, D. ananassae is a tropical species that has not been used in many cytological and genetic studies. Daigorô Moriwaki learned Drosophila genetics from Yoshitaka Imai at Furitsu Kôtô-Gakkô (Tokyo Metropolitan University) and started compiling evaluations of D. ananassae independently from Kikkawa. Moriwaki collected D. ananassae from the Kanda fruit and vegetable market in Tokyo in 1931 (Moriwaki 1934), and the flies were assumed to have accidentally been imported into the area on some contaminated fruit imports.

Cytologia published 11 Drosophila studies from Japan between 1938 and 1944, with eight of these studies describing cytological and genetic data from D. virilis (Makino 1938, 1940, 1942, Fujii 1938, 1940, 1942, Komai and Takaku 1940, 1942), including expansions of work from Hokkaido Imperial University by Sajiro Makino. Another two of these papers focused on D. ananassae (Moriwaki 1938, Kikkawa 1939), while the final publication discussed D. kikkawai (Osima 1940), which was misidentified as D. montium at the time (Chozo Oshima=Tyozo Osima, personal communication). One of the major topics in Drosophila cytology at the time was the degree of homology across the chromosomal arms even among diverse species. Linkage maps were constructed for several Drosophila species, and the order of visible mutations was compared among various species (Sturtevant and Plunkett 1926, Muller 1940), uncovering the clear parallelism of some of these mutations, that is, Muller’s element or synteny say now, with these findings discussed in the monumental paper produced by Sturtevant and Noviski (1941). Here, they mentioned 14 species, including D. virilis, D. ananassae, and D. montium (=D. kikkawai), and cited three previous papers published in Cytologia: Fujii (1936), Kaufmann (1937), and Osima (1940).

Cytologia could not be published between 1944 and 1946 due to World War II and the ensuing post-war turmoil (Leonard 1951) with these effects delaying the publication of a seminal paper describing the electron microscopic analysis of salivary gland chromosomes from D. virilis, from February 19, 1945, to November 25, 1947 (Yasuzumi 1947). Despite this delay, Gonpachiro Yasuzumi, a leader in clinical electron microscopy, working at Osaka Imperial University, published a series of additional papers in Cytologia (Yasuzumi and Sawada 1950, Yasuzumi and Yoshida 1950, Yasuzumi et al. 1950a, b, 1951) once publication resumed. He also influenced Osamu Tezuka’s decision to become the father of Manga as his mentor. D. virilis was the primary focus of the research published in Cytologia papers from Kyoto as before (Komai and Takaku 1949, Ogaki 1949), but various D. ananassae mutant strains housed in both Kyoto and Tokyo were lost during the war (Crow 1989). Moriwaki and Kitagawa (1955) used the obscura group species, D. bifasciata, collected from the wild, in their research following a suggestion from Theodosius Dobzhansky. Hsiang (1949) observed the chromosomes of D. tumiditarsus, which was later synonymized with D. repletoides. During this time there was also an increase in novel applications of D. melanogaster, including investigation of the nurse cell chromosomes (Hsu and Hansen 1953), the development of male germ cells (Khishin 1957), tissue cultured eye discs (Horikawa 1958), new embryogenesis observations (Imaizumi 1958a, b, 1962), and polytene chromosome puffing (Slizynski 1964). In addition, this period saw a resumption in global submissions to Cytologia including papers from China, the USA, Egypt, and the UK (Hsiang 1949, Hsu and Hansen 1953, Khishin 1957, Slizynski 1964, respectively).

Cytologia papers on Drosophila burgeoned in the late 1960s and 1970s with an exponential increase in the number of international contributions to the journal including five from India (Sharma 1967, Narda 1969, Jha and Rahman 1973, Singh 1974, Parkash and Miglani 1976), four from the USA (Habert and Beckert 1971, Kaufmann and Gay 1971, Beck 1977, Beck and Clayton 1977), two from Japan (Yamaguchi 1973, Moriwaki and Tsujita 1974), one from Brazil (Bicudo 1972), and one from Argentina/Spain (Stockert and Esponda 1973). These included three papers focused on D. melanogaster: Sharma (1967) on oogenesis, Kaufmann and Gay (1971) on salivary gland chromosomes, and Parkash and Miglani (1976) on chemical agents for mutagenesis. Habert and Beckert (1971) also used D. melanogaster as one of their invertebrate subjects when evaluating sex-distinguishing chromatin. An additional two papers used D. virilis and described constitutive heterochromatin in mitotic chromosomes (Beck 1977) and spermatogenesis (Beck and Clayton 1977). Two more were D. ananassae papers dealing with the synaptonemal complex during male crossover (Moriwaki and Tujita 1974) and chromosomal polymorphism in natural populations (Singh 1974), and sibling species from the ananassae group, D. bipectinata and D. malerkotliana, were used for cytological analysis of interspecific hybrids (Narda 1969, Jha and Rahman 1973). Bicudo (1972) used D. parasaltans from the saltans group found in South America, and Yamaguchi (1973), from the Moriwaki lab, continued the study of the obscura group, D. bifasciata and D. imaii. Stockert and Esponda (1973) observed spermatocytes from various species of Drosophila, including D. hydei, D. phalerata, D. immigrans, and D. buzzatii.

Another eight Drosophila studies were published in Cytologia in the 1980s. The first was Guest (1981) who analyzed the chromosomal relationship between sibling species of the virilis group, D. littoralis and D. ezoana, the latter of which was a gift from Eizi Momma. Rinaldi and Subirana (1982) then evaluated the chromosomal structures of D. melanogaster and D. funebris using electron microscopy, and Pessacq-Asenjo (1984) analyzed the nucleolar organization of salivary gland chromosomes using D. hydei. In addition, five of these papers evaluated D. auraria, an oriental species of the montium group, with, surprisingly, all of these contributions coming from Greece and using a strain from Kirishima. Dimitriadis (1985, 1986) and Dimitriadis and Kastritsis (1985) observed larval midgut cells under various conditions while Scouras and Kastritsis (1988) described the fine structures of the salivary gland chromosome. Rodriguez-Arnaiz and Martinez (1986) examined chemical mutagenesis using D. melanogaster. There were only two Drosophila studies published in Cytologia in the 1990s. Suma and Ranganath (1997) from India described mitotic chromosomes and the heterochromatin distribution in montium group species, D. kikkawai, D. jambulina, and D. nagarholensis, and Uysal (1997) analyzed D. melanogaster chromosome aberrations induced by chemical mutagenesis.

There were also eight Drosophila studies published in Cytologia over the course of the 2000s and early 2010s including two studies that followed up on previous reports; Uysal (2003) from Turkey who used different chemical mutagens to mutate D. melanogaster, and Venkat and Ranganath (2007) from India who expanded their evaluations to include other species from the montium group, D. agumbensis, D. anomelani, D. truncata, and D. cauverii. Three others were contributions from Brazil: Mikami et al. (2001) who analyzed the salivary gland nuclear halo of D. melanogaster; dos Passos et al. (2007) who evaluated potential (anti)mutagens using D. melanogaster; and dos Santos-Colares et al. (2004) who detected male recombination in D. willistoni using cytological methods. Matsuda (2002) described the meiotic chromosomes of Chymomyza (Drosophilidae) with a specific focus on the discovery of XO males. El-Din et al. (2009) tested chemical mutagens in D. melanogaster while Yui and Matsuura (2011) used molecular techniques to analyze mitochondrial heteroplasmy in D. melanogaster, where the cytoplasm was transplanted from sibling species, D. mauritiana. Unfortunately, there have been no more novel Drosophila papers in Cytologia since Yui and Matsuura (2011), but recent issues often include colorful cover photos of D. melanogaster studies. Sato et al. (2015) demonstrated histone acetylation of polytene chromosomes. Takase and Suzuki (2018) showed sex-specific gene regulation in the central nervous system. Natori and Kojima (2019) provided a banding pattern for region-specific transcription factors in an imaginal disc. And Kohsaka and Nose (2020) visualized the interneurons involved in specific animal behavior.

Thus, the founders of Cytologia made a significant contribution to the scientific community as a whole, especially Drosophila cytologists and geneticists worldwide (Table 1). While their initial aims were realized in the 1930s, especially in the special volume of 1937, the journal soldiers on, and while contributions from other countries ceased in 1938–1948, Japanese scientists continued their publication helping to keep the field moving forward. International contributions restarted and then grew exponentially in the late 1960s and ‘70s and continue to this day. Most of these more modern papers focus on D. melanogaster, but Cytologia also accepts papers on other Drosophila species, such as D. virilis, D. ananassae, and D. auraria, with more than 26 Drosophila species appeared in the journal to date. This diversity is strongly linked to the fact that while many of the world’s fly labs use D. melanogaster the two Japanese Fly Rooms, the Komai and Moriwaki labs, used D. virilis and D. ananassae. In addition, some of the species distributed across Japan (e.g., D. ezoana and D. auraria) were also selected by scientists outside Japan. In summary, many of the earliest and significant publications on Drosophila and its early cytology and heredity experiments were published in this journal.

Table 1. Drosophila research papers appeared in Cytologia.

Year	D. melanogaster and related spp.	D. virilis and related spp.	D. ananassae and related spp.	montium gr. spp.	other spp.
1929
1930
1931
1932		〇〇
1933		〇
1934		●
1935	●	〇〇
1936		〇
1937	●●●●		●〇〇
1938		〇〇	〇
1939			〇
1940		〇〇〇		〇
1941
1942		〇〇〇
1943
1944–46a
1947	〇
1948
1949		〇〇			●
1950	〇〇〇〇
1951	〇
1952
1953	●
1954
1955					〇
1956
1957	●
1958	〇〇〇
1959
1960
1961
1962	〇
1963
1964	●
1965
1966
1967	●
1968
1969			●
1970
1971	●●
1972					●
1973			●		●◯
1974			●◯
1975
1976	●
1977		●●
1978
1979
1980
1981		●
1982	●b				●b
1983
1984					●
1985				●●
1986	●			●
1987
1988				●
1989
1990
1991
1992
1993
1994
1995
1996
1997	●			●
1998
1999
2000
2001	●
2002					〇
2003	●
2004					●
2005
2006
2007	●			●
2008
2009	●
2010
2011	〇
2012
2013
2014
2015	〇
2016
2017
2018	〇
2019	〇
2020	〇
2021
2022

〇, Paper from Japan; ●, paper from other countries; ^aunpublished; ^bcounted twice because this paper deals with D. melanogaster and D. funebris.

Anecdotes of genetics history mentioned here mainly follow Kihara et al. (1988), Moriwaki (1988), and Sawamura (2022), but some are based on previous-generation scientists.

Acknowledgements

The author would like to acknowledge Drs. Shigeyuki Kawano and Toshiyuki Nagata for inviting him to publish the present report in Cytologia.

References

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