Drosophila

Drosophila busckii, from Wikimedia Commons.

Belongs within: Drosophilidae.
Contains: Drosophila (Drosophila), Drosophila (Sophophora).

Drosophila is a diverse, cosmopolitan genus of vinegar flies; the monophyly of the genus as generally recognised is currently under debate. Many species have become widely dispersed outside their native ranges as a result of human activity. One of these is southeast Asian native D. busckii, a small, spotted species that breeds in decaying matter (Grimaldi 2010). This species is distinguished by the presence of longitudinal stripes on the pleurae and the absence of preapical setae on the second and third tibiae.

Drosophila forever?
Published January 29 2008
Drosophila funebris, from here.

As I’ve commented before on this blog, taxonomy holds an unusual position in the biological sciences in that it fills two equally significant roles. On the one hand, it is a science in its own right, investigating the best way to describe and express the relationships between organisms. On the other hand, it supplies the means for communication between biologists in all fields. For the most part, these two aims compliment each other, but sometimes they can clash. The first aim implies continual change, as our understanding of the relationships between organisms changes and (hopefully) improves. Wheeler (2007) commented in a recent editorial that “Doing taxonomy as an independent science advances simultaneously both the aims of taxonomy and its users“, a sentiment that I agree with fully (be warned, though, that the general tone of Wheeler’s editorial is fairly incendiary). To fulfil the second aim, however, a certain amount of stability is usually desired, as researchers who are not working in taxonomy may have trouble keeping up with the changes (or, for that matter, appreciating their necessity).

All of the codes of nomenclature have a central commission to regulate taxonomy—zoology has the International Commission on Zoological Nomenclature, botany has the International Association for Plant Taxonomy. One of the main roles of these commissions is to allow suspension of the usual rules in cases where their strict application would cause more trouble for communication than otherwise. In the case of zoology, applications for rulings on such cases that are submitted to the ICZN are published in the journal Bulletin on Zoological Nomenclature, allowing researchers the opportunity to comment on submissions before the Commission decides on them. One submission that appeared in the December 2007 issue of the BZN involves a case that could affect a large number of researchers in many fields—the impending revision of the fly genus Drosophila.

Drosophila is a very large genus containing about 1500 species. However, phylogenetic studies (e. g. Robe et al. 2005) have found that Drosophila as currently defined is significantly paraphyletic with regard to a number of other genera in the family Drosophilidae. There are two options to resolve this situation. One is to sink all the smaller genera arising from Drosophila into the larger genus. However, this is not regarded as a suitable solution—not only would it leave Drosophila with over 2000 species, but it would result in over a hundred secondary homonyms (two or more species ending up with the same name as a result of change in genus assignment) that would require correction. The other option, that seems much more likely to be used, is to divide Drosophila into a number of smaller genera. The name Drosophila would then be restricted to a smaller group of species closely related to the type species.

All this would be fairly routine, except that one of the species affected happens to be one of the most widely used model organisms in genetics—the “fruit fly” Drosophila melanogaster (the inverted commas are because Drosophila isn’t really a fruit fly proper, but a vinegar fly). So familiar is this species that many people simply refer to it as Drosophila without invoking the species name. One might be forgiven for expecting D. melanogaster to be the type species of Drosophila, but it’s not. That honour goes to Drosophila funebris (shown above). And as it happens, the two species are not that closely related. If Drosophila is divided up, the Drosophila melanogaster everyone knows and loves becomes a far less familiar Sophophora melanogaster. How will geneticists respond to the loss of their favourite organism?

To avert an apocalypse in evolutionary biology, van der Linde et al. (2007) have made a submission to the ICZN to redefine the type species of Drosophila. They suggest that that honour be given to D. melanogaster rather than D. funebris, meaning that D. melanogaster would remain forever more Drosophila. But if this is accepted, what will become of D. funebris and its close friends and relatives? Will the ICZN exalt D. melanogaster to the position of type species? Or will the geneticists just have to learn to refer to Sophophora and like it?

More on Drosophila and Sophophora
Published 5 June 2009

Over a year has passed since the proposal was put before the ICZN to make Drosophila melanogaster the type species of the genus Drosophila. At the present point in time, the ICZN has not yet voted on that application. But this does not mean that things have been sitting unremarked—quite to the contrary.

As well as publishing applications to the ICZN and their results, the Bulletin of Zoological Nomenclature also publishes comments from the general taxonomic public on cases being considered, allowing other workers to put forward their arguments for whether the commission should accept or deny an application. To be quite honest, this is usually the dullest part of the Bulletin. The majority of applications are fairly straightforward, and it is fairly uncommon for comments to say anything much more extensive than either “sounds good to me!” or “No sir, I don’t like it”*. The Drosophila case, however, has inspired a barrage of commentary in the pages of the Bulletin to a level that has probably never been seen there before. The June 2008 issue of the Bulletin included nearly fourteen pages of commentary on the application. Some of these “comments” bordered on being full articles—Prigent (in the June 2008 issue), for instance, filled up three full pages (“no sir, I don’t like it”), while McEvey et al. (also June) put their names on two and a half pages (“no sir, I don’t like it, but it should probably happen anyway”). [Disclaimer: I haven’t yet seen the March 2009 issue of the Bulletin, but apparently it’s got even more comments to read.] So what have been the main points raised for and against the proposal?

*This is not to say that the comments are completely pointless—for a start, they’re probably the primary means for the commissioners to gauge the popularity or otherwise of an application. Still, the vast majority of them are not particularly likely to become citation classics.

A common complaint has been that supporting the decision would be to support a particular classification or method of classification (or, to put it another way, “Oh noes! They be taking my paraphylum!“) As stated by Thompson et al. (June 2008):

The proposal declares that the current concept of Drosophila is ‘paraphyletic’ and thus ‘violates modern systematic practice’. That practice is cladistics or Hennigian systematics. For followers of ‘evolutionary’ systematics or phenetics, paraphyletic taxa are acceptable. Then there are the issues of the utility of large and small taxa (i.e. lumping vs splitting). We feel strongly that the Commission should not be endorsing one classification paradigm over another.

Some of you may have been struck by the gratuitous conflations of phylogenetic and taxonomic methodologies in the second and third sentences there*, but let’s ignore those for now and move on, shall we? It would indeed be a strong violation of the ICZN’s principles to judge between paradigms (though I’ve previously questioned the possibility of a truly paradigm-free nomenclatorial system). In this case, however, the Commission is being asked to do no such thing. Those authors who wished to retain Drosophila melanogaster and D. funebris (the current type species) within a single genus, whether paraphyletic or not, would still be perfectly free to do so—from their perspective, the case is largely irrelevant. Even if an author wised to divide up Drosophila by non-cladistic means, then odds are that they would still end up wanting to separate D. melanogaster and D. funebris, because the two species are about as different from each other as any taxa within Drosophila could be—that’s why they’ve been placed in separate subgenera in the first place—and then we’d be facing the exact same question. Indeed, it could be argued (whether validly or not) that the current situation is the one impeding taxonomic freedom, because no-one has been willing to take the step of removing D. melanogaster from Drosophila. So overall, the “no paradigm endorsement” argument is dead in the water from the outset.

I’m not sure that a phenetically-derived classification really can be said to “permit” paraphyly—it’s more that for phenetics, questions of monophyly vs. paraphyly vs. polyphyly become irrelevant.

The second major argument is that changing the type species increases the amount of taxonomic instability rather than decreasing it. Unlike the first argument, this one actually has some legs. As I mentioned in the earlier post, the current subgenus Drosophila is considerably larger than the subgenus Sophophora to which D. melanogaster belongs. Therefore, making D. melanogaster the type species of Drosophila potentially means that more individual species will end up undergoing name changes than if the type species remained D. funebris. Also, while D. melanogaster is the most commonly used Drosophila species in research, it is not the only species used in research. A significant number of other species have also come under the microscope, and some of these other model species (such as D. virilis and D. mojavensis) belong to subgenus Drosophila rather than Sophophora. On the other hand, many more model species (such as D. simulans and D. yakuba) are also members of Sophophora, so changing the type species preserves their names in their current combinations as well.

From a purely taxonomic viewpoint (as many commenters have stated), the answer is a simple one—the current situation is clearly valid under the rules, nomenclatural changes are a perfectly valid part of an developing taxonomic system, there ain’t nothing wrong with Sophophora melanogaster, whaddya complaining about? Unfortunately, the reason why this case was proposed in the first place was that such a change does not only affect taxonomists. The case is most elegantly summarised, I think, by McEvey et al.:

The binomen Sophophora melanogaster would continue to convey a precise meaning, and in this sense there would be no confusion. [However] With respect to nomenclatural instability, there may be considerable reluctance to adopt the unfamiliar binomen Sophophora melanogaster and many would, no doubt, continue using Drosophila melanogaster, Drosophila or just melanogaster. And this would be confusing. Information retrieval would be hampered.

Thompson et al. claim that such fears of confusion are overblown, and specifically cite the case of the mosquito Aedes aegypti, widely studied as a major disease vector, which has been renamed and almost universally accepted as Stegomyia aegypti in recent taxonomic revisions. This was perhaps the most comic moment in the affair to date, because as pointed out by van der Linde et al. in the December 2008 Bulletin, Aedes-errr-Stegomyia aegypti provides a very strong argument in favour of the application. Taxonomists have mostly accepted the name Stegomyia aegypti, but almost everyone else working on the beast—ecologists, parasitologists, epidemiologists—has rejected it, and continues to use the name Aedes aegypti. A wide rift has developed between the two sides, making communication between disciplines increasingly difficult. One should never underestimate the holding power a name can have if it somehow catches the public’s imagination. After all, we still witness the occasional trotting out of Brontosaurus, a name that was in proper use for less than twenty-five years and was sunk into synonymy more than a hundred years ago.

So ultimately the question is whether preserving the names of a smaller number of economically significant taxa is more important than preserving those of a much larger number of taxa of less direct significance to humans. And I have to admit, I’m glad I’m not one of the people having to make an actual decision on this one.

In which, despite not being the crowd favourite, Drosophila funebris holds D. melanogaster down and kicks it repeatedly in the teeth
Published 7 April 2010
The original and still reigning champion, Drosophila funebris. Fear it, I say! Photo by Nicolas Gompel.

It’s been two years in the making, but the ICZN decision on Drosophila has finally been announced (ICZN 2010). And the verdict: by a surprisingly large margin (23 to 4, with one absence), the Commission has turned the proposal down. Drosophila funebris remains the valid type species of the genus; D. melanogaster retains the potential for reclassification. Those of you with a particular interest in the workings of nomenclature* would do well to get hold of a copy of the decision. In light of the higher than usual public interest in this case, the unusual step has been taken of publishing individual comments from each of the commissioners on the reasoning behind their decisions. As well as the insight provided into this particular case (and it’s worth noting that some of the commissioners on both sides of the floor ended up voting against their own initial sympathies), some of the comments provide interesting talking points about the role of nomenclature in general.

*Yes, we do exist. I’m afraid the doctors say that there’s nothing they can do.

Some of the reasons given for voting against the proposal were reasonable, others less so. A. small number of commissioners voiced the complaint that the proposal was asking the ICZN to endorse a particular taxonomic method; as I argued in one of the previous posts, it did no such thing and I am rather disappointed that this issue was raised. Some commissioners also turned down the proposal on the grounds that it was premature (Miguel Alonso-Zarazaga stated that he “felt that the authors of the case had not allowed the community to have a healthy discussion of their proposals, since the ‘detailed phylogenetic studies’ mentioned in the case were still largely unpublished, and were thus hypothetical“). However, while the proposal may have been precipitated by an as-yet unpublished study, the results of that study are hardly novel. As pointed out by László Papp in his comments on his supporting vote, the issue that any subdivision of Drosophila would require the removal from that genus of D. melanogaster has been under discussion for at least 35 years (a time when, I should note, purely phylogenetic considerations were often considered less significant).

Less trivial are the concerns that the proposal introduced a higher overall nomenclatural instability than the current status quo and that it may have set an uncomfortable precedent. The commission was being asked to choose between maintaining Drosophila for a smaller number (about 300) of species including some very well-known taxa, or a potentially much larger number (up to about 1100) of mostly less familiar species. Should “celebrity names” carry that much greater weight? Also, while the combination Sophophora melanogaster may be unfamiliar, there is no actual ambiguity about to what it refers.

Some commissioners, as well as many of the ICZN’s press statements, raised the argument that “drosophila” could still be used as an informal name for Sophophora melanogaster. True, as far as it goes, and not unprecedented: names such as “azalea” and “cosmos” continue to be used despite the genera of those names being stricken from the technical literature long ago. Nevertheless, this is not anywhere near a satisfactory solution. As a corollary example, a number of recent authors have proposed restricting “Aves” to the crown group of birds on not unreasonable grounds. The supposed divide between technical and vernacular names has done nothing to dissuade people from objecting to the idea that creatures such as Archaeopteryx and Ichthyornis may no longer be “birds”.

My thanks go to Kim van der Linde (first author of the proposal) and Elinor Michel (secretary of the ICZN) for sending me copies of the decision. Kim’s own reaction to the ruling can be read here.

Systematics of Drosophila

Characters (from Grimaldi 2010): Arista plumose; facial carina large, often with flat surface; eyes pubescent; acrostichals in six or more rows; two pairs of dorsocentral setae; prescutellar setae absent; two katepisternal setae present of unequal lengths; wing tip rounded; crossveins distant.

<==Drosophila Fallén 1823 (see below for synonymy)SDF04
    |--D. (Dorsilopha) busckiiRV05
    `--+--D. (Drosophila)RV05
       `--D. (Sophophora)RV05
Drosophila incertae sedis:
  D. acutilabellaS00
  D. artificialisD37
  D. aurariaKVV96
  D. berryiW87
  D. colorataM90
  D. earleiD37
  D. fenestrarumRD77
  D. grimshawiWT11
  D. guttiferaM47
  D. heteroneuraC96
  *Tanygastrella’ hypopygialis Duda 1924SDF04
  D. macrospinaD51
    |--D. m. macrospinaD51
    |--D. m. limpiensisD51
    `--D. m. ohioensisD51
  D. megagenysW91
  *Adrosophila’ minuta Séguy 1938SDF04
  *Spuriostyloptera’ multipunctata Duda 1923SDF04
  D. nasutoidesLG91
  D. neorepletaD51
  D. nigrospiraculaS85
  D. nothaW91
  D. onychophoraG10
  D. orientaceaGJR97
  D. planitibiaG91
  D. prosaltansD51
  D. quadrilineata de Meijere 1911 [=*Chaetodrosophilella quadrilineata]SDF04
  D. recensS00
  D. rubidaW70
  D. silvestrisVD94
  D. sturtevantiD51
  D. subarcticaCE79
  D. suboccidentalisS00
  D. sulcataD37
  D. transversaD37
  D. uvarumB88
  D. vibrissinaD37
  D. wheeleriG84
  D. (Paradrosophila Duda 1923)SDF04
    `--D. (*P.) pictipennis Kertész 1901SDF04
  D. (Phalodoris) lebanonensisCE79
  D. (Pholadoris)T68
    |--D. (P.) lativittataT68
    |--D. (P.) pattersoniT68
    `--D. (P.) victoriaT68
  D. (Spinulophila Duda 1923)SDF04
    `--D. (*S.) signata (Duda 1923) [=*Spinulophila signata]SDF04

Drosophila Fallén 1823 [incl. Adrosophila Séguy 1938, Chaetodrosophilella Duda 1923, Chaetodrosophila (l. c.), Spuriostyloptera Duda 1923, Tanygastrella Duda 1924]SDF04

*Type species of generic name indicated

References

[B88] Bouček, Z. 1988. Australasian Chalcidoidea (Hymenoptera): A biosystematic revision of genera of fourteen families, with a reclassification of species. CAB International: Wallingford (UK).

[C96] Campbell, N. A. 1996. Biology 4th ed. The Benjamin/Cummings Publishing Company, Inc.: Menlo Park (California).

[CE79] Coyne, J. A., W. F. Eanes, J. A. M. Ramshaw & R. K. Koehn. 1979. Electrophoretic heterogeneity of α-glycerophosphate dehydrogenase among many species of Drosophila. Systematic Zoology 28 (2): 164–175.

[D37] Dobzhansky, T. 1937. Genetics and the Origin of Species. Columbia University Press: New York.

[D51] Dobzhansky, T. 1951. Genetics and the Origin of Species 3rd ed. Columbia University Press: New York.

[GJR97] Giordano, R., J. J. Jackson & H. M. Robertson. 1997. The role of Wolbachia bacteria in reproductive incompatibilities and hybrid zones of Diabrotica beetles and Gryllus crickets. Proceedings of the National Academy of Sciences of the USA 94: 11439–11444.

[G84] Gosling, E. M. 1984. The systematic status of Mytilus galloprovincialis in western Europe: a review. Malacologia 25 (2): 551–568.

[G10] Grimaldi, D. 2010. Drosophilidae (small fruit flies, pomace flies, vinegar flies). In: Brown, B. V., A. Borkent, J. M. Cumming, D. M. Wood, N. E. Woodley & M. A. Zumbado (eds) Manual of Central American Diptera vol. 2 pp. 1197–1206. NRC Research Press: Ottawa.

[G91] Groves, C. P. 1991. A Theory of Human and Primate Evolution revised ed. Clarendon Press: Oxford.

ICZN. 2010. Opinion 2245: Drosophila Fallén, 1823 (Insecta, Diptera): Drosophila funebris Fabricius, 1787 is maintained as the type species. Bulletin of Zoological Nomenclature 67 (1): 106–115.

[KVV96] Kroon, A., R. L. Voenendaal & A. Veerman. 1996. Does the spider mite Tetranychus urticae Koch (Tetranychidae) respond to photoperiod in a quantitative manner? In: Mitchell, R., D. J. Horn, G. R. Needham & W. C. Welbourn (eds) Acarology IX vol. 1. Proceedings pp. 5–7. Ohio Biological Survey: Columbus (Ohio).

[LG91] Li, W.-H., & D. Graur. 1991. Fundamentals of Molecular Evolution. Sinauer: Sunderland (MA).

Linde, K. van der, G. Bächli, M. J. Toda, W.-X. Zhang, Y.-G. Hu & G. S. Spicer. 2007. Case 3407: Drosophila Fallén, 1832 (Insecta, Diptera): proposed conservation of usage. Bulletin of Zoological Nomenclature 64 (4).

Linde, K. van der, G. Bächli, M. J. Toda, W.-X. Zhang, T. Katoh, Y.-G. Hu & G. S. Spicer. 2008. Comment on the proposed conservation of usage of Drosophila Fallén, 1823 (Insecta, Diptera). Bulletin of Zoological Nomenclature 65 (4): 304–307.

[M47] Mayr, E. 1947. Ecological factors in speciation. Evolution 1: 263–288.

[M90] McAlpine, J. F. 1990. Insecta: Diptera adults. In: Dindal, D. L. (ed.) Soil Biology Guide pp. 1211–1252. John Wiley & Sones: New York.

McEvey, S. F., M. Schiffer, J.-L. Da Lage, J. R. David, F. Lemeunier, D. Joly, P. Capy & M.-L. Cariou. 2008. Comment on the proposed conservation of usage of Drosophila Fallén, 1823 (Insecta, Diptera). Bulletin of Zoological Nomenclature 65 (2): 147–150.

Prigent, S. R. 2008. Comment on the proposed conservation of usage of Drosophila Fallén, 1823 (Insecta, Diptera). Bulletin of Zoological Nomenclature 65 (2): 137–140.

[RD77] Richards, O. W., & R. G. Davies. 1977. Imms’ General Textbook of Entomology 10th ed. vol. 2. Classification and Biology. Chapman and Hall: London.

[RV05] Robe, L. J., V. L. S. Valente, M. Budnik & E. L. S. Loreto. 2005. Molecular phylogeny of the subgenus Drosophila (Diptera, Drosophilidae) with an emphasis on Neotropical species and groups: a nuclear versus mitochondrial gene approach. Molecular Phylogenetics and Evolution 36: 623–640.

[S00] Siddiqi, M. R. 2000. Tylenchida: Parasites of plants and insects 2nd ed. CABI Publishing: Wallingford (UK).

[SDF04] Singh, B. K., S. Dash & R. S. Fartyal. 2004. Revision of the species of the subgenus Drosophila (Drosophila) of the Kumaon region, India, with the description of eight new species. Senckenbergiana Biologica 83 (2): 163–176.

[S85] Slatkin, M. 1985. Gene flow in natural populations. Annual Review of Ecology and Systematics 16: 393-430.

Thompson, F. C., N. L. Evenhuis, T. Pape & A. C. Pont. 2008. Comment on the proposed conservation of usage of Drosophila Fallén, 1823 (Insecta, Diptera). Bulletin of Zoological Nomenclature 65 (2): 140–141.

[T68] Throckmorton, L. H. 1968. Concordance and discordance of taxonomic characters in Drosophila classification. Systematic Zoology 17 (4): 355–387.

[VD94] Vogler, A. P., & R. Desalle. 1994. Diagnosing units of conservation management. Conservation Biology 8 (2): 354–363.

[W87] Wheeler, M. R. 1987. Drosophilidae. In: McAlpine, J. F. (ed.) Manual of Nearctic Diptera vol. 2 pp. 1011–1018. Research Branch, Agriculture Canada.

Wheeler, Q. D. 2007. Invertebrate systematics or spineless taxonomy? Zootaxa 1668: 11–18.

[W70] White, M. J. D. 1970. Cytogenetics. In: CSIRO. The Insects of Australia: A textbook for students and research workers pp. 72–82. Melbourne University Press.

[W91] Whitten, M. J. 1991. Australian insects in scientific research. In: CSIRO. The Insects of Australia: A textbook for students and research workers vol. 1 pp. 236–251. Melbourne University Press: Carlton (Victoria).

[WT11] Wiegmann, B. M., M. D. Trautwein, I. S. Winkler, N. B. Barr, J.-W. Kim, C. Lambkin, M. A. Bertone, B. K. Cassel, K. M. Bayless, A. M. Heimberg, B. M. Wheeler, K. J. Peterson, T. Pape, B. J. Sinclair, J. H. Skevington, V. Blagoderov, J. Caravas, S. N. Kutty, U. Schmidt-Ott, G. E. Kampmeier, F. C. Thompson, D. A. Grimaldi, A. T. Beckenbach, G. W. Courtney, M. Friedrich, R. Meier & D. K. Yeates. 2011. Episodic radiations in the fly tree of life. Proceedings of the National Academy of Sciences of the USA 108 (14): 5690–5695.

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