Drosophila melanogaster's history as a human commensal
2007; Elsevier BV; Volume: 17; Issue: 3 Linguagem: Inglês
10.1016/j.cub.2006.12.031
ISSN1879-0445
Autores Tópico(s)Animal and Plant Science Education
ResumoWhen W.E. Castle at Harvard and T.H. Morgan at the Columbia University started using a tiny fly for laboratory experiments in genetics they were probably unaware that the species had only been introduced to the United States a few years earlier. Drosophila melanogaster, now a widely popular organism in biological research, is a human commensal that owes its current cosmopolitan distribution largely to human activity. Since this became clear considerable progress has been made in understanding the historical biogeography of Drosophila melanogaster and its association with human activities. There are even first attempts to describe the ecology of populations not associated with human activities, which might shed light on the evolutionary history of the species. When W.E. Castle at Harvard and T.H. Morgan at the Columbia University started using a tiny fly for laboratory experiments in genetics they were probably unaware that the species had only been introduced to the United States a few years earlier. Drosophila melanogaster, now a widely popular organism in biological research, is a human commensal that owes its current cosmopolitan distribution largely to human activity. Since this became clear considerable progress has been made in understanding the historical biogeography of Drosophila melanogaster and its association with human activities. There are even first attempts to describe the ecology of populations not associated with human activities, which might shed light on the evolutionary history of the species. There has been much speculation about the ancestral home range of Drosophila melanogaster, but today it seems clear that the species is native to equatorial Africa [1Lachaise D. Cariou M.L. David J.R. Lemeunier F. Tsacas L. Ashburner M. Historical biogeography of the Drosophila-Melanogaster species subgroup.Evol. Biol. 1988; 22: 159-225Crossref Google Scholar]. From there it spread to all major continents, and today the northernmost record is from Tampere, Finland [2Hackman W. Die Drosophila-Arten Finnlands.Notulae Entomologicae. 1954; 34: 130-139Google Scholar] and the southernmost record from Tasmania [3Agis M. Schlotterer C. Microsatellite variation in natural Drosophila melanogaster populations from New South Wales (Australia) and Tasmania.Mol. Ecol. 2001; 10: 1197-1205Crossref PubMed Scopus (18) Google Scholar]. The home range of closely related species is a strong indication that Drosophila melanogaster has an African origin. Drosophila melanogaster and eight sister species form the Drosophila melanogaster subgroup. Of these, Drosophila yakuba was discovered in the Ivory Coast in the 1950s [4Burla H. Zur Kenntnis der Drosophiliden der Elfenbeinküste (Franzoesisch West-Afrika).Revue Suisse de Zoologie. 1954; 61: 1-218Google Scholar]. In the 1970s and 1980s, five more species were discovered by Léonidas Tsacas and his coworkers. Drosophila teissieri, Drosophila orena and Drosophila erecta were all found on the African mainland [5Tsacas L. Drosophila teissieri, nouvelle espèce africaine du groupe melanogaster et note sur deux autres especes nouvelles pour l'Afrique.Bulletin de la Société Entomologique de France. 1971; 76: 35-45Google Scholar, 6Tsacas L. David J. Une septieme espece appartenant au sous-groupe Drosophila melanogaster Meigen: Drosophila orena spec. nov. Cameroun (Diptera: Drosophilidae).Beiträge zur Entomologie. 1978; 28: 179-182Google Scholar, 7Tsacas L. Lachaise D. Quatre nouvelles espèces de la Côte d'Ivoire du genre Drosophila, groupe melanogaster, et discussion de l'origine du sous-groupe melanogaster (Diptera: Drosophilidae).Annales de l'Université d'Abidjan. 1974; E7: 193-211Google Scholar], whereas Drosophila mauritiana is endemic to the island of Mauritius [8Tsacas L. David J.R. Drosophila mauritiana n.sp. du groupe melanogaster de I'Île Maurice.Bulletin de la Societe Entomologique de France. 1974; 79: 42-46Google Scholar] and Drosophila sechellia was only found on some islands of the Seychelles archipelago [9Tsacas L. Baechli G. Drosophila sechellia, n.sp., huitième espece du sous-groupe melanogaster des Iles Seychelles (Diptera, Drosophilidae).Revue francaise d'entomologie. 1981; 3: 146-150Google Scholar]. The Seychelles archipelago and the island of Mauritius are both in the Indian Ocean off the coast of Africa. In the year 2000, another species in the Drosophila melanogaster subgroup, Drosophila santomea, was discovered on the island of São Tomé in the Atlantic Ocean near the West African coastline [10Lachaise D. Harry M. Solignac M. Lemeunier F. Benassi V. Cariou M.L. Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from Sao Tome.Proc. Roy. Soc. B. 2000; 267: 1487-1495Crossref PubMed Scopus (146) Google Scholar]. All these flies have so far been found only in the Afrotropical region. The other two members of the subgroup, Drosophila melanogaster and Drosophila simulans, are cosmopolitan, but because all of the closely related species are endemic to the Afrotropical region, it can be assumed that these two originated there, too. The discovery of species closely related to Drosophila melanogaster that are not human commensals opened the interesting possibility of studying their ecology in an attempt to learn how Drosophila melanogaster may have lived before it became associated with humans. All species of the Drosophila melanogaster subgroup breed on fruits, yet they differ considerably in their ecology (reviewed in [1Lachaise D. Cariou M.L. David J.R. Lemeunier F. Tsacas L. Ashburner M. Historical biogeography of the Drosophila-Melanogaster species subgroup.Evol. Biol. 1988; 22: 159-225Crossref Google Scholar]). Little is known about the natural history of Drosophila orena, which has only been reported from a single collection in the West Cameroon mountains at 2100 m [6Tsacas L. David J. Une septieme espece appartenant au sous-groupe Drosophila melanogaster Meigen: Drosophila orena spec. nov. Cameroun (Diptera: Drosophilidae).Beiträge zur Entomologie. 1978; 28: 179-182Google Scholar], or of Drosophila santomea, which was discovered only recently “in the remote, submontane, mist rainforests covering the higher rugged volcanic slopes of São Tomé” [10Lachaise D. Harry M. Solignac M. Lemeunier F. Benassi V. Cariou M.L. Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from Sao Tome.Proc. Roy. Soc. B. 2000; 267: 1487-1495Crossref PubMed Scopus (146) Google Scholar]. Drosophila sechellia and Drosophila erecta are predominantly found on the fruits of a single plant species, Morinda citrifolia and Pandanus candelabrum, respectively. Drosophila mauritiana, Drosophila yakuba and Drosophila teissieri, on the other hand, breed on a wide variety of fruits including mangos (Mangifera indica), figs (Ficus lyrata) and guavas (Psidium guajava) [1Lachaise D. Cariou M.L. David J.R. Lemeunier F. Tsacas L. Ashburner M. Historical biogeography of the Drosophila-Melanogaster species subgroup.Evol. Biol. 1988; 22: 159-225Crossref Google Scholar]. Drosophila simulans and Drosophila melanogaster, the two cosmopolitan species, also exploit a variety of different fruits and can also breed on anthropogenic food sources such as stale beer [11Sturtevant A.H. The North American species of Drosophila. Carnegie Institution of Washington, Washington1921Crossref Google Scholar]. The first hint that Drosophila melanogaster breeds on fruits came in 1864, when it was reported from the raisin stores of Smyrna (now Izmir, Turkey; cited in [11Sturtevant A.H. The North American species of Drosophila. Carnegie Institution of Washington, Washington1921Crossref Google Scholar]). Subsequently Drosophila melanogaster was, like many commensal species, reported to occur in a wide variety of habitats. It was found in a human grave in 1898 [12Motter M.G. A contribution to the study of the fauna of the grave. A study of one hundred and fifty disinterments, with some additional experimental observations.J.N.Y. Entomol. Soc. 1898; 6: 201-230Google Scholar] and was bred from human excrement one year later [13Howard L.O. A contribution to the study of the insect fauna of human excrement.Proc. Wash. Acad. Sci. 1900; 2: 541-604Google Scholar]. More commonly though, it is reported in sources like canned fruits and pickles, decaying apples, cider mill refuse, fermenting vats of grape pomace and raspberry vinegar [13Howard L.O. A contribution to the study of the insect fauna of human excrement.Proc. Wash. Acad. Sci. 1900; 2: 541-604Google Scholar]. It was bred from potatoes, tomatoes and a variety of fruits [11Sturtevant A.H. The North American species of Drosophila. Carnegie Institution of Washington, Washington1921Crossref Google Scholar]. All these food sources are domesticated fruits or other products of human activity. What food source Drosophila melanogaster used in its ancestral home range in equatorial Africa before it became dependent on these man-made sources is unclear. It may be that it used an entirely different fruit than the domesticated species on which it is now most commonly found. A fascinating discussion of the wild-to-domestic habit shift in Drosophila melanogaster can be found in Lachaise and Silvain [14Lachaise D. Silvain J.F. How two Afrotropical endemics made two cosmopolitan human commensals: the Drosophila melanogaster-D. simulans palaeogeographic riddle.Genetica. 2004; 120: 17-39Crossref PubMed Scopus (125) Google Scholar]. Interestingly, a host-plant shift from a natural source to a domesticated fruit was shown for another fly, Rhagoletis pomonella, which originally infested hawthorn. A recently derived population of this species now breeds preferentially on apples that were introduced in the geographic range of the species. In the case of Rhagoletis pomonella, this host–plant shift was associated with, and perhaps causally related to, a shift in olfactory preferences [15Linn C. Feder J.L. Nojima S. Dambroski H.R. Berlocher S.H. Roelofs W. Fruit odor discrimination and sympatric host race formation in Rhagoletis.Proc. Natl. Acad. Sci. USA. 2003; 100: 11490-11493Crossref PubMed Scopus (205) Google Scholar]. Reports of Drosophila melanogaster breeding sites in natural habitats in Africa (reviewed in [1Lachaise D. Cariou M.L. David J.R. Lemeunier F. Tsacas L. Ashburner M. Historical biogeography of the Drosophila-Melanogaster species subgroup.Evol. Biol. 1988; 22: 159-225Crossref Google Scholar]) can help answer the question of what food sources Drosophila melanogaster originally used. The species is said to breed most successfully on bananas [11Sturtevant A.H. The North American species of Drosophila. Carnegie Institution of Washington, Washington1921Crossref Google Scholar, 14Lachaise D. Silvain J.F. How two Afrotropical endemics made two cosmopolitan human commensals: the Drosophila melanogaster-D. simulans palaeogeographic riddle.Genetica. 2004; 120: 17-39Crossref PubMed Scopus (125) Google Scholar] and was reported to occur in a natural habitat with fruits of the banana species Ensete giletti[14Lachaise D. Silvain J.F. How two Afrotropical endemics made two cosmopolitan human commensals: the Drosophila melanogaster-D. simulans palaeogeographic riddle.Genetica. 2004; 120: 17-39Crossref PubMed Scopus (125) Google Scholar]. Other host plants used as breeding sites of Drosophila melanogaster in the Afrotropical region include mangos (Mangifera indica), papaya (Carica papaya) and apple guava (Psidium guajava). A total of 25 plant species in the Afrotropical region have shown to host Drosophila melanogaster larvae. Sixteen of these are native plants, making them possible food sources for Drosophila melanogaster before its association with man [1Lachaise D. Cariou M.L. David J.R. Lemeunier F. Tsacas L. Ashburner M. Historical biogeography of the Drosophila-Melanogaster species subgroup.Evol. Biol. 1988; 22: 159-225Crossref Google Scholar]. Although all nine Drosophila melanogaster sister species originated in the Afrotropical region, only Drosophila melanogaster and Drosophila simulans have spread around the world as a result of human activity. The other seven species have remained restricted to their tropical home range. The ability to colonize depends largely on the broadness of the ecological niche a species occupies. Only species tolerating a wide range of temperatures and using different food sources have the ability to become cosmopolitan. Of the two efficient colonizers in the subgroup, Drosophila simulans seems to lag behind its sister species Drosophila melanogaster. In 1920, when Drosophila melanogaster was already very common throughout northern America, Drosophila simulans was found in the eastern part of the United States, but was not contained in rather extensive collections from the Pacific Coast [16Sturtevant A.H. Genetic studies on Drosophila simulans. I. Introduction. Hybrids with Drosophila melanogaster.Genetics. 1920; 5: 488-500PubMed Google Scholar]. The colonization of Japan by Drosophila simulans dates to around 1972, a time when Drosophila melanogaster was already well-established there [17Watanabe T.K. Kawanishi M. Colonization of Drosophila simulans in Japan.Proc. Japan Acad. 1976; 52: 191-194Google Scholar]. Drosophila simulans may lag behind Drosophila melanogaster in its speed of dispersal because it is less ‘domestic’ than Drosophila melanogaster — for example, less likely to enter houses [17Watanabe T.K. Kawanishi M. Colonization of Drosophila simulans in Japan.Proc. Japan Acad. 1976; 52: 191-194Google Scholar]. The stronger association with humans of Drosophila melanogaster makes it more likely for individuals of this species to be introduced into a new area by human activity. Once a species is introduced to a new location, the number of individuals sometimes increases rapidly. At the ideal temperature and population density, it takes only 10 days for a Drosophila melanogaster egg to develop into a sexually mature fly [18Ashburner M. Drosophila: A Laboratory Handbook and Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York1989Google Scholar]. Because of its short life cycle and the fact that Drosophila can disperse several kilometers in a single day [19Coyne J.A. Boussy I.A. Prout T. Bryant S.H. Jones J.S. Moore J.A. Long-distance migration of Drosophila.Am. Nat. 1982; 119: 589-595Crossref Google Scholar], Drosophila melanogaster — although it relies on humans to be transported across oceans — can spread efficiently once it is introduced into a new area. The introduction and subsequent rapid dispersal of Drosophila melanogaster has been observed directly by entomologists in the United States and on numerous islands. The first entomologist to describe Drosophila melanogaster was the German government employee Johann Wilhelm Meigen [20Meigen J.W. Systematische Beschreibung der bekannten europäischen zweiflügeligen Insekten. Volume 6. Schulz, Hamm1830Google Scholar] (Figure 1A). In 1830, Meigen reported finding Drosophila melanogaster in the two German port cities of Kiel and Hamburg, and in Austria. The occurrence in port cities suggests that these specimens may have been introduced by ships and may have been from temporary populations. Meigen's description of the species is brief, six words in the Latin and 14 in the German version. Because of the lack of detail in the description, Drosophila melanogaster has been frequently redescribed and was therefore known under many synonyms, including Drosophila nigriventris, Drosophila ampelophila and Drosophila uvarum. There are too few reports to decide if Drosophila melanogaster was rare or absent in middle Europe before 1830. It is quite likely that the species just went unnoticed until then and was actually introduced to parts of Europe and Asia in prehistoric times [21David J. Bocquet C. Pla E. New Results on Genetic Characteristics of Far-East Race of Drosophila-Melanogaster.Genet. Res. 1976; 28: 253-260Crossref PubMed Scopus (19) Google Scholar]. In other parts of the world, however, the introduction of Drosophila melanogaster has been witnessed by entomologists. Drosophila melanogaster's colonization of North America in the second half of the 19th century has been observed directly [11Sturtevant A.H. The North American species of Drosophila. Carnegie Institution of Washington, Washington1921Crossref Google Scholar, 22Johnson C.W. The distribution of some species of Drosophila.Psyche. 1913; 20: 202-205Crossref Scopus (9) Google Scholar]. The species was first reported in the State of New York in 1875, where the New York State entomologist Joseph Albert Lintner (Figure 1B) reported that it had been “bred from a jar of pickled plums” [23Lintner J.A. First Annual Report on the Injurious and Other Insects of the State of New York. Weed, Parsons and Co., Albany, New York1882Google Scholar]. The dipteran fauna of the State of New York had been studied before in great detail without any mention of Drosophila melanogaster by Asa Fitch, the entomologist of the New York State Agricultural Society. It seems improbable that Fitch, the first professional entomologist in the United States “who described so many minute diptera” [22Johnson C.W. The distribution of some species of Drosophila.Psyche. 1913; 20: 202-205Crossref Scopus (9) Google Scholar] would have overlooked Drosophila melanogaster. Therefore, the species was most likely introduced into the northeastern United States of America shortly before 1875. In subsequent years Drosophila melanogaster was reported in different parts of the continent, in monographs that included the first depictions of Drosophila melanogaster specimens (Figure 2). In 1900, only 25 years after its first report on American soil, Drosophila melanogaster was “the commonest species all over the United States” [13Howard L.O. A contribution to the study of the insect fauna of human excrement.Proc. Wash. Acad. Sci. 1900; 2: 541-604Google Scholar] (Figure 3). To my knowledge, however, it was reported from the West Coast only in 1915, when it was found on dried fruits in California [24Parker W.B. Control of dried-fruit insects in California. Bulletin.United States Department of Agriculture. 1915; 235: 1-15Google Scholar]. By 1921, Drosophila melanogaster's geographical range in northern America was from Nova Scotia to Washington in the north and from Florida to California in the south [11Sturtevant A.H. The North American species of Drosophila. Carnegie Institution of Washington, Washington1921Crossref Google Scholar].Figure 3The dispersal of Drosophila melanogaster in the United States after 1875.Show full captionIn the ten years after is was first reported in New York State in 1875 (orange), Drosophila melanogaster was reported in the District of Columbia (1878) [37Osten-Sacken C.R. Catalogue of the described Diptera of North America (Second edition).Smithsonian Misc. coll. 1878; 270: 1-276Google Scholar], Montreal (1879) [34Bowles G.J. The pickled fruit fly - Drosophila ampelophila, Loew.Can. Entomol. 1882; 14: 101-104Crossref Scopus (1) Google Scholar], New Haven, Connecticut (1879) [38Williston S.W. Drosophila ampelophila, Loew.Can. Entomol. 1882; 14: 138Crossref Scopus (2) Google Scholar], Massachusetts and Pennsylvania (1882) [38Williston S.W. Drosophila ampelophila, Loew.Can. Entomol. 1882; 14: 138Crossref Scopus (2) Google Scholar], and Moline, Illinois (1884) (cited in [35Howard L.O. Marlatt C.L. Chittenden F.H. The principal household insects in the United States. United States Department of Agriculture, Division of Entomology, Washington1896Google Scholar]). It continued its spread to the south and west and was found in St. Augustine, Florida, in Mesilla Valley, New Mexico in 1894 [39Cockerell T.D.A. Notes from New Mexico.Insect Life. 1894; 7: 207-211Google Scholar], and in Phoenix, Arizona in 1899. It was reported in California in 1915 [24Parker W.B. Control of dried-fruit insects in California. Bulletin.United States Department of Agriculture. 1915; 235: 1-15Google Scholar].View Large Image Figure ViewerDownload Hi-res image Download (PPT) In the ten years after is was first reported in New York State in 1875 (orange), Drosophila melanogaster was reported in the District of Columbia (1878) [37Osten-Sacken C.R. Catalogue of the described Diptera of North America (Second edition).Smithsonian Misc. coll. 1878; 270: 1-276Google Scholar], Montreal (1879) [34Bowles G.J. The pickled fruit fly - Drosophila ampelophila, Loew.Can. Entomol. 1882; 14: 101-104Crossref Scopus (1) Google Scholar], New Haven, Connecticut (1879) [38Williston S.W. Drosophila ampelophila, Loew.Can. Entomol. 1882; 14: 138Crossref Scopus (2) Google Scholar], Massachusetts and Pennsylvania (1882) [38Williston S.W. Drosophila ampelophila, Loew.Can. Entomol. 1882; 14: 138Crossref Scopus (2) Google Scholar], and Moline, Illinois (1884) (cited in [35Howard L.O. Marlatt C.L. Chittenden F.H. The principal household insects in the United States. United States Department of Agriculture, Division of Entomology, Washington1896Google Scholar]). It continued its spread to the south and west and was found in St. Augustine, Florida, in Mesilla Valley, New Mexico in 1894 [39Cockerell T.D.A. Notes from New Mexico.Insect Life. 1894; 7: 207-211Google Scholar], and in Phoenix, Arizona in 1899. It was reported in California in 1915 [24Parker W.B. Control of dried-fruit insects in California. Bulletin.United States Department of Agriculture. 1915; 235: 1-15Google Scholar]. In other geographical regions, Drosophila melanogaster was introduced even more recently. In the early 1980s, it was reported for the first time from the Mahé island in the Seychelles archipelago [25David J.R. Capy P. Genetics and origin of a Drosophila-melanogaster population recently introduced to the Seychelles.Genet. Res. 1982; 40: 295-303Crossref Scopus (8) Google Scholar]. On Hokkaido, the second largest island of Japan, Drosophila melanogaster was not found in an extensive survey of the Drosophilidae in 1961, but later was introduced [26Beppu K. Kaneko A. Toda M.J. Kimura M.T. Methods in the studies of wild drosophilid flies in Hokkaido. 2. Key to species of Drosophilidae in Hokkaido, with a supplementary note on phylogeny.Seibutsu Kyozai. 1977; 12: 1-40Google Scholar]. The sudden appearance and rapid spread of Drosophila melanogaster around Honolulu in the early 1940s has been attributed to escapes from culture bottles at the University of Hawaii [27Zimmerman E.C. Immigrant species of Drosophila in Hawaii (Diptera: Drosophilidae).Proc. Hawaiian Entomol. Soc. 1943; 11: 345-350Google Scholar], and on the Galapagos Islands, Drosophila melanogaster was not found in 1966 [28Linsley E.G. Usinger R.L. Insects of the Galapagos Islands.Proc. Calif. Acad. Sci. (4th Series). 1966; 33: 113-196Google Scholar], but later an expedition to the Islands with the specific purpose of investigating Drosophilidae found it in the fruit room of the restaurant at the Charles Darwin Biological Station, suggesting that it was introduced directly to the islands through the human food supply [29Carson H.L. Val F.C. Wheeler M.R. Drosophilidae of the Galapagos-Islands, with descriptions of two new species.Int. J. Entomol. 1983; 25: 239-248Google Scholar]. A population that, like the one in the Charles Darwin Biological Station, is restricted to a single source of food, is generally unstable and may eventually disappear. This happened in Okinawa, an island belonging to Japan, where Drosophila melanogaster was reported in the 1930s [30Kikkawa H. Peng F.T. Drosophila species of Japan and adjacent localities.Japanese J. Zool. 1938; 7: 507-552Google Scholar]. Thirty years later two independent surveys of the Drosophilidae were carried out and failed to find Drosophila melanogaster, despite the large scale of the efforts [31Okada T. Drosophilidae of the Okinawa Islands.Kontyû. 1965; 33: 327-350Google Scholar, 32Takada H. Wakahama K.-I. A Drosophila Survey in Okinawa Main Island.Annotationes Zoologicae Japonenses. 1967; 40: 55-60Google Scholar]. This example shows that, while Drosophila melanogaster is a very efficient colonizer and its spread around the world is still ongoing, its populations outside its home range are very vulnerable and highly dependent on human activity. Some researchers have even suggested that, outside the tropical regions, some populations die out during the winter and new populations are established in the spring from individuals reintroduced from warmer regions [11Sturtevant A.H. The North American species of Drosophila. Carnegie Institution of Washington, Washington1921Crossref Google Scholar]. It may be surprising that an animal that is now encountered so frequently in laboratories and kitchens all over the world used to be a forest-dwelling species restricted to a small part of equatorial Africa. The success of Drosophila melanogaster as a commensal and its popularity as a laboratory animal has the same reasons. The flies have a short generation span and the capacity to produce lots of offspring and they can utilize a wide variety of food sources and are not afraid to enter human settlements. Drosophila melanogaster shares these characteristics with another popular laboratory animal that started as a human commensal and was spread all over the world by human activity, the common house mouse (Mus musculus) [33Boursot P. Auffray J.C. Brittondavidian J. Bonhomme F. The Evolution of house mice.Annu. Rev. Ecol. Syst. 1993; 24: 119-152Crossref Scopus (381) Google Scholar]. I thank Angela Larkin-Matthews of The Rockefeller University library who obtained copies of many of the references used here. The library of the American Museum of Natural History in New York was also an indispensable source of historical scientific literature. I thank Leslie B. Vosshall and members of the Vosshall lab. Maurizio Pellegrino and Kenta Asahina translated reports published in Italian and Japanese. AK received support from a Marco S. Stoffel Postdoctoral Fellowship in Mind, Brain and Behavior and from NIH DC005036 to L.B. Vosshall.
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