This document summarizes a bibliometric analysis of global Drosophila melanogaster research from 1900 to 2008. Some key findings include:
- Over 48,000 documents were found in the Science Citation Index with "Drosophila" in the title, with most papers being research articles in English published in the United States.
- The top countries publishing on Drosophila research were the US, France, UK, Germany, and others. The most prolific institutions were from the US, France, Germany, and the UK.
- The most common subject areas were genetics and heredity, biochemistry, molecular biology, cell biology, and developmental biology. The most influential journals were Genetics and PNAS.
Información, informática y cienciometría para envejecimiento
Global drosophila
1. Global Drosophila
melanogaster Research: a
bibliometric analysis
Michán, L; Castañeda-Sortibrán,
A; Rodríguez-Arnaiz, R; Ayala,
FJ Drosophila Information Service, Vol. 93
(2010), 232-243.
http://www.ou.edu/journals/dis/DIS93/Michan%20232.pdf
Complementary material
1
2. Abstract
• We investigate the scientific productivity of Drosophila-related research among
researchers, countries, institutions, journals, and subject areas, by a bibliometric
analysis of Drosophila research from 1900 to 2008. We have searched the Science
Citation Index (SCI) documents with the word Drosophila in the title. 48,981
documents were obtained from SCI 76.9% of the documents are research papers,
mostly (95.2%) written in English, and (55.8%) produced in the United States. The
study includes 4,600 institutions and 45,415 author names. Most prolific are 34
authors, who account for 9% of the articles published, with more than 100 research
papers produced by each author. We also provide a list of the 50 most cited articles.
We considered 1,648 journals; 60 of them (3.6%) published 66% of the articles.
Genetics is the main journal most used for Drosophila research publications (9.9%).
Genetics and heredity as well as biochemistry, molecular biology, and cell biology are
the dominant research subjects. We compare research in Drosophila with 10 other
organisms, frequently used as biological models: Escherichia, Saccharomyces,
Arabidopsis, Zea, Neurospora, Dictyostelium, Chlamydomonas, Caenorhabditis,
Schizosaccharomyces, and Danio. Escherichia coli is the most extensively used
model organism for genetics research since 1950, with 94,873 documents. We
analyzed 36,486 documents in detail with respect to their contents, using the indexing
keywords listed in the medical subject headings (MeSH) thesaurus.
2
3. Materials and methods
• Our search covered papers published during 1900-2008. The search was performed using the
Science Citation Index (SCI) and the PubMed database. SCI was started by the Institute for
Scientific Information (ISI) in 1963. It is now owned by Thomson Reuters and is available online
through the Web of Science database. PubMed Central, which started in 2000, includes articles
and peer-reviewed manuscripts dating back to mid the 1800s or early 1900s for some journals.
These databases include many journals; provide a citation index; and the results of the queries
are comparative concerning mainstream papers in scientific research. PubMed has detailed
document identification by the keywords listed in the medical subject headings (MeSH) thesaurus.
We accessed the Science Citation Index until 2008, in order to find out where research in
Drosophila has been done. We accessed data on documents with the word Drosophila in the title
of the paper, because we were interested only in documents with their main interest in Drosophila.
All records were retrieved for each database and were systematized in a database; then the data
sets were validated and normalized, and a quantitative analysis for each category was done:
document, author, affiliation institution, country, journal, subject area (from Science Citation Index)
and MeSH headings and subheadings (from PubMed). The 50 and the 10 most cited papers from
Science Citation Index were identified. Journals were processed by subject (sensu SCI), Impact
Factors were obtained from Journal Citation Report 2008 and core journals were identified with
Bradford`s method (Bradford, 1948). The same method was used for each of ten additional
biological models: Escherichia, Saccharomyces, Arabidopsis, Zea, Neurospora, Dictyostelium,
Chlamydomonas, Caenorhabditis, Schizosaccharomyces, and Danio. All the information was
organized with scientific, historical, and sociological points of view.
3
4. Results
• Papers. The total number of publications with Drosophila in the title
was 48,981 in the Science Citation Index and 36,486 in PubMed
(Figure 1). The first paper registered was published in 1905 by F.W.
Carpenter . Document type and language according to the Science
Citation Index are shown in Figures 2 and 3. The temporal trends of
publication in Drosophila, as well as in ten other biological models
are shown in Figures 4 and 5. There are 139 different subject
categories in the SCI, the 16 most frequent, each with more than 1%
of the total are shown in Figure 6. The temporal trends for the nine
most frequent subjects are shown in Figures 7 and 8. Information
about documents extracted from PubMed is in Figures 9 and 10.
4
12. • Researchers. We found 45,415 author names. The 34
most prolific, each with more than 100 published articles
and jointly accounting for 9% of all the papers, are
shown in Table 1. There were 119 affiliation countries, 32
(2.6%) of which include each more than 100 papers, and
jointly accounting for 97% of all papers. The 10 countries
with most publications are shown in Figure 11. The
United States was the country most represented. There
were 4,600 different institutions, such as universities,
departments, and corporations. The 18 most highly
represented are shown in Figure 12. Table 2 lists the 50
papers with the highest citation impact.
12
13. Researcher Documents
(48,981)
Rubin, GM 220 (5)
David, JR 203
Dobzhansky, T 185
Perrimon, N 184
Hall, JC 170
Mukai, T 164
Zhimulev, IF 160
Jan, YN 155
Gehring, WJ 149 (2)
Jackle, H 148
Ayala, FJ 143 (1)
Hoffman, AA 139 (1)
Jan, LY 131
Bownes, M 126
Parsons, PA 126
Partridge, L 126
Ashburner, M 123 (2)
Green, MM 122
Belyaeva, ES 122
Glover, DM 119
Levine, M 115 (1)
Mahowald, AP 115
King, RC 111
Singh, BN 111
, SCR 110
Wurgler, FE 110
Korochkin, LI 109
Hartl, DL 109
Georgiev, PG 106
Kaufman, TC 103
Wu, CF 103 (1)
Rosbash, M 101
Ehrman, L 101
Mackay, TFC 101
Table 1. The 34 most prolific researchers in Drosophila, each with 100 or more papers, as
retrieved from the Web of Science. Numbers in parentheses are documents shown in Table 2.
13
17. USA France
England Japan
Germany Canada
Spain Switzerland
USSR Australia
2.9% 2.7%
3.5%
4.0%
4.0%
6.2%
6.4%
55.8%
7.2%
7.4%
Figure 11
18. Cornell
Irvine
Pennsylvania
Max Planck
2
Texas
Zurich
Wisconsin
2
N Carolina
1
Stanford
3
Institution
Figure 18
San Francisco
2
Yale
3
Paris
Berkeley
2
Cambridge
2
Washington
1
Harvard
CNRS, France
Russian Aca Sci
0
1400
1200
1000
600
400
200
800
Documents
19. Adams et al. (2000). The genome sequence of Drosophila melanogaster. Science, 287(5460):2185–2195. 2,751
Rubin, G. M. and Spradling, A. C. (1982). Genetic-transformation of Drosophila with transposable element vectors. Science, 218(4570):348–353. 2,184
Tautz, D. and Pfeifle, C. (1989). A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma, 98(2):81–85. 2,126
Lewis, E. B. (1978). Gene complex controlling segmentation in Drosophila. Nature, 276(5688):565–570. 1,906
Medzhitov et al. (1997). A human homologue of the Drosophila toll protein signals activation of adaptive immunity. Nature, 388(6640):394–397. 1,752
Nüsslein-Volhard, C. and Wieschaus, E. (1980). Mutations affecting segment number and polarity in Drosophila. Nature, 287(5785):795–801. 1,727
Lemaitre et al. (1996). The dorsoventral regulatory gene cassette spatzle/toll/cactus controls the potent antifungal response in Drosophila adults. Cell, 86(6):973–983. 1,277
Spradling, A. C. and Rubin, G. M. (1982). Transposition of cloned p elements into Drosophila germ line chromosomes. Science, 218(4570):341–347. 1,228
Robertson et al. (1988). A stable genomic source of p-element transposase in Drosophila melanogaster. Genetics, 118(3):460–470. 1,153
Hammond et al. (2000). An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature, 404(6775):293–296. 1,147
Ashburner, M. and Bonner, J. J. (1979). Induction of gene activity in Drosophila by heat shock. Cell, 17(2):241–254. 1,135
McDonald, J. H. and Kreitman, M. (1991). Adaptive protein evolution at the adh locus in Drosophila. Nature, 351(6328):652–654. 1,117
Xu, T. and Rubin, G. M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues. Development, 117(4):1223–1237. 1,091
Bateman, A. J. (1948). Intra-sexual selection in Drosophila. Heredity, 2(3):349–368. 1,079
Ephrussi, B. and Beadle, G. W. (1936). A technique of transplantation for Drosophila. American Naturalist, 70:218–225. 942
Clary, D. O. and Wolstenholme, D. R. (1985). The mitochondrial-DNA molecule of Drosophila yakuba - nucleotide-sequence, gene organization, and genetic-code. Journal of Molecular Evolution, 22(3):252–271. 930
Konopka, R. J. and Benzer, S. (1971). Clock mutants of Drosophila melanogaster. Proceedings of the of Sciences of the , 68(9):2112–2116. 902
Ayala et al. (1972). Enzyme variability in the Drosophila willistoni group. IV. Genic variation in natural populations of Drosophila willistoni. Genetics, 70(1):113–139. 900
Ellisen et al. (1991). Tan-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in t-lymphoblastic neoplasms. Cell, 66(4):649–660. 894
Wu, C. (1980). The 5’ ends of Drosophila heat-shock genes in chromatin are hypersensitive to DNase-i. Nature, 286(5776):854–860. 872
Rock et al. (1998). A family of human receptors structurally related to Drosophila toll. Proceedings of the of Sciences of the , 95(2):588–593. 860
Giot et al. (2003). A protein interaction map of Drosophila melanogaster. Science, 302(5651):1727–1736. 853
Cavener, D. R. (1987). Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Research, 15(4):1353–1360. 845
Orr, W. C. and Sohal, R. S. (1994). Extension of life-span by overexpression of superoxide-dismutase and catalase in Drosophila melanogaster. Science, 263(5150):1128–1130. 838
Ingham, P. W. (1988). The molecular-genetics of embryonic pattern-formation in Drosophila. Nature, 335(6085):25–34. 837
Akam, M. (1987). The molecular-basis for metameric pattern in the Drosophila embryo. Development, 101(1):1–22. 834
Stjohnston, D. and Nüsslein-Volhard, C. (1992). The origin of pattern and polarity in the Drosophila embryo. Cell, 68(2):201–219. 831
Ritossa, F. (1962). New puffing pattern induced by temperature shock and dnp in Drosophila. Experientia, 18(12):571–573. 829
Pelham, H. R. B. (1982). A regulatory upstream promoter element in the Drosophila hsp 70 heat-shock gene. Cell, 30(2):517–528. 807
Hahn et al. (1996). Mutations of the human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome. Cell, 85(6):841–851. 800
Lewontin, R. C. and Hubby, J. L. (1966). A molecular approach to study of genic heterozygosity in natural populations. II. Amount of variation and degree of heterozygosity in natural populations of Drosophila pseudoobscura. Genetics, 54(2):595–609. 796
(1972). Cell lines derived from late embryonic stages of Drosophila melanogaster. Journal of Embryology and Experimental Morphology, 27(APR):353–&. 785
Bhanot et al. (1996). A new member of the frizzled family from Drosophila functions as a wingless receptor. Nature, 382(6588):225–230. 758
McGinnis et al. (1984). A conserved DNA-sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes. Nature, 308(5958):428–433. 756
Halder, G., Callaerts, P., and Gehring, W. J. (1995). Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science, 267(5205):1788–1792. 737
Feany, M. B. and Bender, W. W. (2000). A Drosophila model of Parkinson’s disease. Nature, 404(6776):394–398. 729
Krauss, S., Concordet, J. P., and Ingham, P. W. (1993). A functionally conserved homology of the Drosophila segment polarity gene-hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell, 75(7):1431–1444. 723
Cho, K. O., Hunt, C. A., and Kennedy, M. B. (1992). The rat-brain postsynaptic density fraction contains a homolog of the Drosophila disks-large tumor suppressor protein. Neuron, 9(5):929–942. 721
Graham, A., Papalopulu, N., and Krumlauf, R. (1989). The murine and Drosophila homeobox gene complexes have common features of organization and expression. Cell, 57(3):367–378. 719
Tkachuk, D. C., Kohler, S., and Cleary, M. L. (1992). Involvement of a homolog of Drosophila-trithorax by 11q23 chromosomal translocations in acute leukemias. Cell, 71(4):691–700. 714
Poole et al. (1985). The engrailed locus of Drosophila: structural analysis of an embryonic transcript. Cell, 40(1):37–43. 705
Ohare, K. and Rubin, G. M. (1983). Structures of p-transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome. Cell, 34(1):25–35. 700
Vandewetering et al. (1997). Armadillo co-activates transcription driven by the product of the Drosophila segment polarity gene dtcf. Cell, 88(6):789–799. 695
Gu et al. (1992). The t(4-11) chromosome-translocation of human acute leukemias fuses the all-1 gene, related to Drosophila-trithorax, to the af-4 gene. Cell, 71(4):701–708. 694
Tissiere, A., Mitchell, H. K., and Tracy, U. M. (1974). Protein-synthesis in salivary-glands of Drosophila melanogaster: Relation to chromosome puffs. Journal of Molecular Biology, 84(3):389–398. 671
Ingolia, T. D. and Craig, E. A. (1982). Four small Drosophila heat-shock proteins are related to each other and to mammalian alpha-crystallin. Proceedings of the of Sciences of the United States of America-Biological Sciences, 79(7):2360–2364. 651
Smith, D. E. and Fisher, P. A. (1984). Identification, developmental regulation, and response to heat-shock of 2 antigenically related forms of a major nuclear-envelope protein in Drosophila embryos: application of an improved method for affinity 647
purification of antibodies using polypeptides immobilized on nitrocellulose blots. Journal of Cell Biology, 99(1):20–28.
Elbashir et al. (2001). Functional anatomy of si RNAs for mediating efficient RNAi in Drosophila melanogaster embryo lysate. Embo Journal, 20(23):6877–6888. 641
Padgett, R. W., Stjohnston, R. D., and Gelbart, W. M. (1987). A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth-factor-beta family. Nature, 325(6099):81–84. 639
Garcia-Bellido, A., Ripoll, P., and Morata, G. (1973). Developmental compartmentalization of wing disk of Drosophila. Nature-New Biology, 245(147):251–253. 636
19
Table 2. The 50 most cited papers according to Science Citation Index.
20. • Journals. A total of 1,648 journal names were obtained, 60 of them (3.6%)
published 66.6% of the articles about Drosophila (Table 3). Genetics has the
most publications, with 10% of the total. Cell and Nature have the highest
impact (Figure 13).
• The 34 authors, each with more than 100 Drosophila research papers,
jointly produced almost 10% of all published papers and are the authors of
13 (26%) of the 50 most cited papers. 55.8% of all the papers had at least
one North American author. After the United States and France, the most
productive countries were England, Japan, and Germany. Jointly, these 5
countries account for 65% of the publications (Figure 11). The most
productive institutions are the Russian Academy of Sciences, the Centre
National de la Recherche Scientifique (CNRS in France), and Harvard
University, each with more than 1,000 publications. Harvard had 5 (10%) of
the most cited documents (Figure 12).
20
22. Source Title Documents %
Genetics 4.860 9.92%
Development 1.765 3.60%
Developmental Biology 1.689 3.45%
PNAS 1.528 3.12%
Japanese Journal of Genetics 1.039 2.12%
Nature 891 1.82%
Mutation Research 843 1.72%
Cell 837 1.71%
Molecular Biology of The Cell 784 1.60%
Genetika 731 1.49%
Journal of Biological Chemistry 699 1.43%
Evolution 693 1.41%
Journal Cell Biology 660 1.35%
Genetica 649 1.33%
Embo Journal 605 1.24%
Chromosoma 592 1.21%
Heredity 588 1.20%
Genes & Development 585 1.19%
Mechanisms of Development 569 1.16%
Molecular and Cellular Biology 544 1.11%
Science 514 1.05%
Nucleic Acids Research 497 1.01%
Current Biology 491 1.00%
American Naturalist 463 0.95%
Genetical Research 446 0.91%
Molecular & General Genetics 442 0.90%
Experientia 436 0.89%
Journal of Neurogenetics 430 0.88%
Hereditas 390 0.80%
Journal of Insect Physiology 387 0.79%
Journal of Neuroscience 368 0.75%
Biochemical Genetics 356 0.73%
Gene 340 0.69%
Journal of Cell Science 317 0.65%
Molecular Biology And Evolution 317 0.65%
Behavior Genetics 312 0.64%
Neuron 300 0.60%
Journal of Experimental Zoology 270 0.55%
Journal of Molecular Biology 252 0.51%
Journal of Cellular Biochemistry 243 0.50%
American Zoologist 236 0.48%
FEBS Letters 234 0.48%
Biochemical And Biophysical Research Communications 233 0.48%
Journal of Heredity 214 0.44%
FASEB Journal 209 0.43%
Journal of Genetics 207 0.42%
Russian Journal of Genetics 202 0.41%
Developmental Genetics 194 0.40%
Developmental Cell 192 0.39%
European Journal of Cell Biology 192 0.39%
Journal of Molecular Evolution 192 0.39%
Canadian Journal of Genetics and Cytology 191 0.39%
Biophysical Journal 189 0.39%
Doklady Akademii Nauk SSSR 185 0.38%
Journal of Experimental Biology 184 0.38%
Journal of Neurobiology 176 0.36%
Development Genes and Evolution 167 0.34%
Insect Biochemistry and Molecular Biology 166 0.34%
Wilhelm Roux’s Archives of Developmental Biology 166 0.34%
Animal Behaviour 164 0.33%
Table 3. Core journals (60, with 66.6% of all published papers) of Drosophila research. 22
23. Discussion
• We have analyzed 48,981 documents in the Science Citation Index (Figure 1), mostly articles
(nearly 77%) (Figure 2), the majority written in English (95%) (Figure 3).
• Temporal scientific production in Drosophila research is fairly similar (and with similar
exponential growth in both SCI and PubMed. There is a continuous increase from 1950 to 2007,
with a decrease in 2008 (Figure 1). This decrease may only be apparent and reflect a usual
delay in the indexation process. The comparison with other biological models is interesting: Zea
and Chlamydomonas show a reasonably stable publication trend (after 1970). From
approximately 1980 on, Arabidopsis and Caenorhabditis exhibit exponential growth, while
Neurospora and Dictyostelium decrease. Escherichia is the most extensively used model
organism for genetics research; from 1950 till 2007, nearly twice as many articles are published
as for Drosophila.
• One factor contributing to the extensive research with Drosophila may have been the free flow
of materials and ideas among its researchers [79]. Morgan's style of research and leadership
was distinctively focused on an experimental, rather than a descriptive approach to science.
Between 1940 and 1970 new techniques were developed, mutants increased in number and
complexity, all fairly freely shared by a gradually increasing number of investigators.
• In the 1970s and 1980s, genetics, developmental, and molecular biology came together in a
successful combination, which brought Drosophila research to a climax. Molecular biology rose
later than the other subjects, associated mostly with the ability to manipulate DNA and RNA, so
that researchers could work with individual genes that produced phenotypic alterations. E.B.
Lewis [80] studied mutations which caused bizarre transformations of the body plan: mutations
in genes in the 'bithorax complex' led to flies with two sets of wings or legs on abdominal
segments. The strangeness of the changes produced became a clue to discover the crucial role
of master control genes that program the final body plan of the organism. 23
24. • Christiane Nüsslein-Volhard and Eric Wieschaus (1980) [81] began working together with Drosophila
flies in a laboratory in Heidelberg, Germany. They systematically searched for mutant genes that
affect the formation of segments in the fly embryo. They identified a series of new genes that drive the
early development of the organism, and also were able to classify the genes into functional groups.
They showed that these genes are conserved in vertebrates. It would soon become clear that close
relatives of these genes, performing similar roles, exist in many other different organisms, including
humans. Indeed, it is now thought that more than 60 percent of the genes involved in human diseases
may have counterparts in the fly.
• An important breakthrough for manipulating the genome was made in 1982 by A.C. Spradling and
G.M. Rubin [82]. They developed a method for making transgenic flies by means of transposable
element vectors. They used this method to achieve the first rescue of a mutant phenotype in an
animal by gene transfer.
• New technologies are also being brought to bear on the study of Drosophila. Since 1999, the genome
sequence of Drosophila has been available, and researchers are using functional genomics to
investigate global patterns of gene and protein expression. The genome sequences of several other
Drosophila species have now become available, which opens up new opportunities for functional
genomics studies, looking at gene and protein expression on a large scale. Such experiments can
produce huge amounts of data, difficult to interpret, organize, and store.
• As pointed out, genetics and heredity, biochemistry, molecular biology and cell biology are the leading
research subjects in SCI. Some journals in our survey are multidisciplinary, such as Nature and
Science. We have shown that there are temporal trends with respect to research subject as well as to
model organisms and prevailing methodologies: toxicology, cell biology, and descriptive
developmental research are decreasing, while evolutionary biology, biochemistry, and molecular
biology are increasing. The most frequent terms in Drosophila research have genetics, heredity, or a
molecular connotation.
• The most cited paper, providing the complete sequence of the euchromatic region of the Drosophila
genome was published in Science in 2000, with 2,751 citations at the time of our survey.
24
25. Figure Legends
• Figure 1. Temporal trend in global Drosophila publications, 1905-2008 (from WoS
and PubMed).
• Figure 2. Document type in Drosophila research according to the Science Citation
Index.
• Figure 3. Document language in Drosophila research according to the Science
Citation Index.
• Figure 4. Temporal trend and total number of publications in Drosophila and four
other biological models.
• Figure 5. Temporal trend and total number of publications in five biological models.
• Figure 6. The 16 most frequent subjects and number of documents (% most cited
papers).
• Figure 7. Temporal trends of Drosophila research for the most frequent subject.
• Figure 8. Temporal trends of Drosophila research for four additional subjects.
• Figure 9. Most frequent MeSH headings from PubMed: number and percent of
documents.
• Figure 10. Most frequent MeSH subjects from PubMed: numbered percent of
documents.
25
