Meredith E. Miller1
Stephen A. Marshall1
David A. Grimaldi2
Meredith E. Miller1
Stephen A. Marshall1
David A. Grimaldi2
Despite the distinguished history of biological research on Drosophila in eastern North America, the northeastern fauna has never been fully reviewed, and there is no useful key to the Drosophila species naturally occurring in eastern North America. Keys are provided here to the 12 genera of Drosophilidae in northeastern North America, illustrated with photomicrographs of external features. Keys are further provided to the 35 species of Drosophila in the region, illustrated with photomicrographs of external features and of the male and female genitalia. Each species is diagnosed, with its biology and distribution summarized, based on the literature and examination of over 10,000 specimens (for which all records are provided). Important new information includes the most northerly records of Drosophila cardini Sturtevant, and habitat records for the highly invasive agricultural pest Drosophila suzukii (Matsumura). Eastern North American species are diagnosed and redescriptions are provided for those members of the Drosophila carsoni, melanica, robusta, and tripunctata groups for which species identification has been vague or uncertain. This work should facilitate research on the drosophilids of eastern North America through the provision of accessible species-level identification tools and baseline data on general distribution and habitat preferences.
Drosophila melanogaster Meigen (photo by S.A. Marshall)
The family Drosophilidae Rondani, some species of which are commonly called vinegar flies or lesser fruit flies, is a large, morphologically diverse, cosmopolitan group of acalyptrate flies. Adults are typically 1-6 mm long, yellow to black in colour, with or without bands or stripes on the abdomen and stripes or spots on the thorax. The wings are sometimes darkened or marked with dark areas, and the eyes are typically red in life (Wheeler, 1987).
The family Drosophilidae includes 73 extant and 3 extinct genera, encompassing over 3950 species (Brake & Bächli, 2008). With the exception of two genera of uncertain subfamily affinity, the family is divided into the subfamilies Steganinae (28 genera) and Drosophilinae (43 genera). The largest genus of Drosophilidae is Drosophila Fallén (1157described species). Drosophila species are found in all six biogeographic regions (Australasian, Afrotropical, Nearctic, Neotropical, Oriental and Palearctic), with the largest number found in tropical areas. Several hundred additional undescribed species probably remain to be discovered in tropical regions (Markow & O’Grady, 2006; Markow & O’Grady, 2007).
Drosophila has been an extremely important group for evolutionary biological research since the beginning of the twentieth century. It is one of the best-studied groups of organisms in modern biology in terms of its life history, biology, phylogeny, ecology, and especially genetics, largely attributed to the establishment of Drosophila melanogaster Meigen as the leading model system for genetic research. Approximately 500 species of Drosophila can now be easily reared and studied in a laboratory (Yassin, 2013), and the full genomes of many species have been fully sequenced, so the study of Drosophila has a firm comparative as well as experimental basis.
Seven secondarily widespread or cosmopolitan species of Drosophila are associated with human habitations (Ashburner et al., 1981). Most Drosophila, including the cosmopolitan species, lay eggs in decaying organic materials such as compost, overripe or rotting produce; others breed in live or decaying fungi, dung, slime or sap fluxes of trees, cacti, or flowering plants (Bächli et al., 2004; Carson, 1971; Markow & O’Grady, 2008). The Oriental species Drosophila suzukii (Matsumura) and Drosophila subpulchrella Takamori and Watabe are exceptional in that they oviposit in healthy whole fruit (Matsumura, 1931). Drosophila suzukii has recently spread beyond its native range to become an invasive, damaging and geographically widespread agricultural crop pest, now widely known as the “Spotted Wing Drosophila” (Hauser et al., 2009; Steck et al., 2009). This has resulted in a demand for new tools to identify and monitor D. suzukii and other potentially damaging invasive Drosophila species.
The North American species of genus Drosophila are relatively well studied, notably by Sturtevant (1921), Patterson (1943), Patterson and Stone (1952) and Strickburger (1967). However, there are few identification keys specifically for Nearctic Drosophila species, in contrast to such references as Bächli et al. (2004) for the northern European species. Patterson’s (1943) key to the Drosophilidae of the southwestern United States is now out of date and cannot be used to identify all Drosophila species in the southwest or in other areas of North America. Moreover, that reference did not utilize the most important character system for diagnosing and identifying species: the male genitalia. M.R. Wheeler’s key in Greenberg’s (1971) Flies and Disease covers only the cosmopolitan and synanthropic Drosophila species. Strickberger’s (1967) key is not functionally effective for identification, since not all species are included, and the use of superficial characters fails to adequately distinguish several species. A key provided in Markow and O’Grady (2006) covers only the Drosophila species in the Drosophila Species Stock Centre at the University of California, U.S.A. This key includes numerous Nearctic Drosophila species, and although it is useful for specimens that can be reared in a laboratory, it excludes many species not currently in culture. Thus there are no current, complete keys to Drosophila species of all or a significant part of North America, and the northeastern North American fauna remains effectively unidentifiable.
Considering that northeastern North America is essentially the birthplace of Drosophila genetic research (Ashburner et al., 1981; Koehler, 1994), it is surprising that such a profound gap exists regarding the identification of Drosophila species naturally occurring in the region. The keys to the species of Drosophila and the genera of Drosophilidae offered here provide the identification tools to ensure early detection of invasive species such as D. suzukii, and will facilitate cost-effective and accurate identification of wild Drosophila species in northeastern North America.
Label data in this study, with collection dates from January to December, include records from rotting mushroom bait traps, from apple cider vinegar bait traps (in blackberry, blueberry, raspberry, sour cherry, grape and peach fields), from rotting organic materials (onions, grapes, bananas, grass piles and compost), from field sweeps, from a hog barn, from tree wounds, from tulip bulbs (originating from Holland), from damp birch & maple, and from indoor environments.
A list of literature records used in species distribution maps was obtained from publications in Gerhard Bächli’s TAXODROS database (Bächli et al, 2017); these sources are not listed in the materials examined.
Specimens were examined from the following institutions (Codens as in Arnett et al., 1993):
AMNH: American Museum of Natural History, New York, NY, USA
CNCI: Canadian National Collection of Insects, Ottawa, ON, Canada
DEBU: University of Guelph Insect Collection, Guelph, ON, Canada
MCZN: Museum of Comparative Zoology, Harvard University, Cambridge, MA, USA
USNM: United States National Museum, Washington, DC, USA
Specimen data for all specimens examined are available from The Knowledge Network for Biocomplexity (doi: 10.5063/F11J97Q0).
Drosophila (Dorsilopha) busckii Coquillett 1901 (Introduced, Cosmopolitan)
Drosophila (Siphlodora) sigmoides Loew 1872 (New Canadian Distributional Records)
Drosophila (Drosophila) funebris (Fabricius, 1787) (Introduced, Cosmopolitan)
Drosophila (Drosophila) macrospina Stalker & Spencer 1939
Drosophila (Drosophila) paramelanica Griffen 1942
Drosophila (Drosophila) nigromelanica Patterson & Wheeler 1942 (New Can. Distributional Records)
Drosophila (Drosophila) melanura Miller 1944
Drosophila (Drosophila) hydei Sturtevant 1921 (Cosmopolitan)
Drosophila (Drosophila) repleta Wollaston, 1858 (Cosmopolitan)
Drosophila (Drosophila) colorata Walker, 1849
Drosophila (Drosophila) robusta Sturtevant 1916
Drosophila (Drosophila) americana Spencer 1938
Drosophila (Drosophila) borealis Patterson 1952
Drosophila (Drosophila) lacicola Patterson, 1944
Drosophila (Drosophila) virilis Sturtevant 1916 (Cosmopolitan)
Drosophila (Drosophila) carsoni Wheeler 1957 (New Can. Distributional Records)
Drosophila (Drosophila) cardini Sturtevant 1916 (New Distributional Records)
Drosophila (Drosophila) immigrans Sturtevant, 1921 (Introduced, Cosmopolitan)
Drosophila (Drosophila) deflecta Malloch 1924 (New Can. Distributional Records)
Drosophila (Drosophila) falleni Wheeler 1960 (New Can. Distributional Records)
Drosophila (Drosophila) guttifera Walker 1849 (New Can. Distributional Records)
Drosophila (Drosophila) palustris Spencer 1942 (New Can. Distributional Records)
Drosophila (Drosophila) quinaria Loew 1866 (New Can. Distributional Records)
Drosophila (Drosophila) recens Wheeler 1960 (New Can. Distributional Records)
Drosophila (Drosophila) rellima Wheeler 1960 (New E. Can. Distributional Records)
Drosophila (Drosophila) neotestacea Grimaldi, James & Jaenike, 1992
Drosophila (Drosophila) putrida Sturtevant 1916
Drosophila (Drosophila) tripunctata Loew 1862 (New Can. Distributional Records)
Drosophila (Sophophora) melanogaster Meigen 1830 (Introduced, Cosmopolitan)
Drosophila (Sophophora) simulans Sturtevant 1919 (Introduced, Cosmopolitan)
Drosophila (Sophophora) suzukii (Matsumura 1931) (Recently Introduced, Widespread)
Drosophila (Sophophora) affinis Sturtevant 1916
Drosophila (Sophophora) algonquin Sturtevant & Dobzhansky 1936
Drosophila (Sophophora) athabasca Sturtevant & Dobzhansky 1936
Drosophila (Sophophora) narragansett Sturtevant & Dobzhansky 1936
We extend our gratitude to Dr. Jeff Skevington (CNC), Hannah Fraser (OMAFRA) and Dr. Justin Renkema (University of Florida) for your support of the project, your assistance, resources and feedback. Thank you to grad students Steve Paiero, Morgan Jackson & Tiffany Yao in the Insect Systematics Lab at the University of Guelph for your support and feedback. Thank you to undergraduate student Man San Ma for your previous work on Drosophila that preceded this project. Thank you to the Museum of Comparative Zoology at Harvard University and The Smithsonian National Museum of Natural History for providing materials used in this project. We gratefully acknowledge support for M. Miller from the University of Guelph Registrar Travel Grant, the Entomological Society of Canada/Biological Survey of Canada Scholarship, and an Ontario Ministry of Agriculture, Food and Rural Affairs (OMAFRA) HQP scholarship.
Most images are by the authors, but we gratefully acknowledge the following exceptions: An image of Mycodrosophila was provided by Ashley Bradford on BugGuide.net. An image of Stegana was provided by Tom Murray on BugGuide.net. The leaf, fly, magnifying glass, photo, trash can, mushroom, tree stump, cacti, honey jar, strawberry, cherry, grape, apple, flower, test tube, microscope, documents, toilet, beer barrel and lily pad icons are from from www.flaticon.com. The river icon is from www.Iconfinder.com. The oak leaf icon is from http://www.iconarchive.com/. The Drosophilidae silhouette images were provided by Spencer Phillips, European Bioinformatics Institute (EMBL-EBI).
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