Drosophila: A Guide to Species Identification and Use

By Therese A. Markow and Patrick O'Grady

Anyone wishing to tap the research potential of the hundreds of Drosophila species in addition to D.melanogaster will finally have a single comprehensive resource for identifying, rearing and using this diverse group of insects. This is the only group of higher eukaryotes for which the genomes of 12 species have been sequenced.The fruitfly Drosophila melanogaster continues to be one of the greatest sources of information regarding the principles of heredity that apply to all animals, including humans. In reality, however, over a thousand different species of Drosophila exist, each with the potential to make their own unique contributions to the rapidly changing fields of genetics and evolution. This book, by providing basic information on how to identify and breed these other fruitflies, will allow investigators to take advantage, on a large scale, of the valuable qualities of these other Drosophila species and their newly developed genomic resources to address critical scientific questions.

* Provides easy to use keys and illustrations to identify different Drosophila species* A guide to the life history differences of hundreds of species* Worldwide distribution maps of hundreds of species* Complete recipes for different Drosophila diets* Offers an analysis on how to account for species differences in designing and conducting experiments* Presents useful ideas of how to collect the many different Drosophila species in the wild

• Language: English
• Publisher: Academic Press
• Release date: Nov 1, 2005
• ISBN: 9780080454092

Book preview

Index

Preface

When you say Drosophila to most people, they think of Drosophila melanogaster, the laboratory workhorse that for nearly 100 years has been the premier genetic model system in biology. Many remember the smell of ether while handling flies in their undergraduate biology classes, while others recall curly wings and white eyes and Punnet squares. T. H. Morgan and his students C. Bridges, H. J. Muller, and A. H. Sturtevant pioneered the field of Drosophila genetics during the first half of the twentieth century. Their work has been carried on by countless drosophilists and, in some ways, culminated with the publication of the full genome sequence of Drosophila melanogaster in 2000.

Now Drosophila biology is entering a new era. The genome of a second species, Drosophila pseudoobscura, has recently been completed and more are surely to come. Increasingly, when researchers state that they work on Drosophila they are met with the following question: What species? Scientists in the fields of ecology and evolutionary biology are beginning to co-opt various members of the genus Drosophila to serve as a model system for their own research, largely because of the ease of obtaining molecular markers from these species. As we were preparing this book for publication, the National Human Genome Research Institute approved whole genome sequencing of 10 additional Drosophila species, and the creation of BAC libraries for 20. We feel that this initiative will invigorate Drosophila research for the next 100 years.

The genus Drosophila represents an unprecedented model system not only for understanding genome evolution, but also for comparative experimental research. No other group has such a well-defined phylogeny and an extensive literature on genetics, development, neurobiology and behavior, physiology, and ecology. A. H. Sturtevant, one of the pioneers of Drosophila genetics, was clearly aware of the importance of the evolutionary context in which D. melanogaster is embedded. He described many new Drosophila species, studied their behavior and genetic relationships, and published his 1921 monograph, The North American Species of Drosophila.

A number of excellent resources exist in which the primary literature concerning the distribution, evolutionary relationships, and ecology for most of the known Drosophila species is summarized. In 1952, J. T. Patterson and W. Stone published their still indispensable Evolution in the Genus Drosophila, which, while drawing heavily on work generated from their own activities and those of their students, provided the first overview of the evolutionary relationships and distributions of all known Drosophila species. The international Drosophila community has since contributed its expertise to five volumes of the The Genetics and Biology of Drosophila series, edited by Ashburner, Carson and Thompson between 1981 and 1986. Michael Ashburner (1990, 2004) and Jeff Powell (1997) have both compiled encyclopedic works that effectively summarize decades of basic Drosophila research. A wide range of data for many Drosophila species now can be accessed through web-based resources such as Flybase and Taxodros.

As the number of investigators taking advantage of Drosophila diversity grows, the need for a portable resource for identifying and using the different species becomes increasingly critical. In 2001, the Tucson Stock Center began offering the now annual Drosophila Species Identification Workshop to teach basic approaches to keying out flies and maintaining non-melanogaster species in laboratory culture. The overwhelming interest of the research community in attending this workshop and in becoming comfortable with using species in addition to D. melanogaster has led us to create this guide. We have had the amazing good fortune of having the participation in these workshops of many colleagues who were responsible for the original collections and descriptions of diverse Drosophila species: Wyatt Anderson, Michael Ashburner, Hampton Carson, David Foote, Nicolas Gompel, William Heed, Kenneth Kaneshiro, Thom Kaufman, Margaret Kidwell, Kathy Matthews, Bryant McAllister, Stephen Schaeffer, Valerie Schaworoch, Marvin Wasserman, and Marshall Wheeler. To all of them we express our gratitude for their unselfish sharing of their time and expertise with us and with the students in the workshops. Activities associated with the annual workshops, including input from the attendees, have been instrumental in shaping the contents of this guide.

Space limitations prevent us from including all Drosophila species in this guide. We have chosen to focus upon the several hundred species maintained at the Tucson Stock Center, as these are readily available to the community and the demand for them is increasing. Conditions for the successful rearing of these species have been worked out and the life history differences critical to their meaningful use in comparative experimental work have been well documented for a number of them. We hope that this guide encourages and enables researchers to exploit the wealth of diversity offered by Drosophila in their investigations.

Therese Ann Markow and Patrick O’Grady

Part 1

How to look at flies

Outline

Chapter 1: Phylogenetic relationships of Drosophilidae

Chapter 2: Morphological characters

Chapter 3: Key to species

Chapter 1

Phylogenetic relationships of Drosophilidae

Publisher Summary

The understanding of phylogenetic relationships within the family Drosophilidae has increased greatly in the 30 years since Throckmorton’s review. A number of phylogenetic studies have used both morphology and molecules to infer relationships among the many genera in this family. Although no firm consensus exists—and several key relationships are openly contentious—a picture of the evolutionary history of this group is emerging. The largest impediment is that the molecular studies are still woefully inadequate with respect to their taxon sampling. Much phylogenetic work in the Drosophilidae today is comparative. Phylogenetic trees of drosophilid species are employed as necessary tools to understand the evolution of transposable elements, development, and a number of other phenomena. In many cases, these phylogenies are in agreement with previous work and are serving to refine the notions of evolution at the species level. Further, basic systematic work is needed not only to fill in the gaps in the knowledge but also to build upon the comparative framework that is already in place in this family.

Contents

• The origin of the family Drosophilidae

• Drosophilidae: relationships among genera

• Steganinae

• Drosophilinae

• Conclusions

• Acknowledgements

• References

The origin of the family Drosophilidae

The Drosophilidae is an acalyptrate family in the superfamily Ephydroidea (McAlpine, 1989). This superfamily contains two large families, Ephydridae and Drosophilidae, as well as several smaller families, such as Camilidae, Diastatidae, and Curtonotidae. Throckmorton (1975) suggested that Diastatidae was the closest relative of the Drosophilidae, based largely on the fact that diastatids are saprophagous in leaf mold (Oldroyd, 1964; Hennig, 1965). Even though Okada (1962) suggested that the ancestral drosophilid substrate was bleeding tree sap, Throckmorton (1975) believed that the current diversity of substrates was the result of opportunism centering on the saprophagous leaf-mold habit.

Grimaldi (1990) examined the phylogenetic relationships of Ephydroidea using morphological characters. Of the three most parsimonious trees his search recovered, he selected a preferred phylogeny. The strict consensus of all three trees gives the more conservative hypothesis (Figure 1.1a). McAlpine (1989) presents an alternative view of evolution in the superfamily Ephydroidea (Figure 1.1b). These two phylogenetic hypotheses differ mainly in the placement of Drosophilidae. The strict consensus of Grimaldi’s (1990) trees is unable to resolve the sister group of the Drosophilidae (his preferred tree favored the Curtonotidae as the sister family of Drosophilidae). McAlpine’s (1989) phylogeny, however, suggests that the Camilidae is the sister clade of Drosophilidae. The exact placement of Drosophilidae remains an open question, as few ephydroid taxa outside of Drosophilidae and a small number of Ephydridae are well known.

Figure 1.1 (a) Phylogeny of Ephydroidea based on Grimaldi (1990); (b) Phylogeny of Ephydroidea from McAlpine (1989).

Throckmorton (1975) placed the origin of the Drosophilidae in the tropics, based primarily on the pan-tropical distribution of the Lissocephala, a group he considered to be basal within the Drosophilidae. The fossil genus Electrophortica, described from Baltic amber (Hennig, 1965), suggests that the Drosophilidae predate the Eocene and may be 50 million years old or older.

Drosophilidae: relationships among genera

Throckmorton (1962, 1975) was the first to propose a higher-level phylogenetic framework for the family Drosophilidae (Figure 1.2). He proposed a number of radiations, meant to represent multiple speciation events with subsequent diversification, based on morphological characters. There have been two major criticisms of Throckmorton’s work: first, his analyses were not based on any explicit cladistic algorithm and are therefore not repeatable; and second, he did not attempt to maintain any concept of monophyly in his study. As a result, species groups of the genus Drosophila are more closely related to other genera than they are to other species groups in their genera. In spite of these criticisms, it is still useful to review Throckmorton’s work as it agrees quite well with recent phylogenetic analyses based on molecular data (e.g. Remsen and O’Grady, 2002). The basal radiation in this family is the Steganinae radiation, which includes all the members of the subfamily Steganinae. A derivative of this radiation led to the Scaptodrosophila radiation, and the diversification of the basal Drosophilidae species. The Sophophoran radiation led to the present day subgenus Sophophora, and some related genera such as Chymomyza (Figure 1.2). The Drosophila radiation is divided into three major parts:

Figure 1.2 Genus-level phylogeny of Drosophilidae based on Throckmorton (1975).

1. A basal radiation containing the funebris species group and related taxa

2. The virilis-repleta radiation

3. The immigrans-Hirtodrosophila radiation.

The virilis-repleta radiation includes about 20 species groups, most of which breed in rotting plant matter. The immigrans-Hirtodrosophila radiation is further divided into the Old World Hirtodrosophila and tripunctata radiations (Figure 1.2).

Grimaldi (1990) proposed a cladistic reclassification of Drosophilidae based on his analysis of 218 morphological characters (Figure 1.3). His analysis suggested that, in agreement with Throckmorton’s work, that some subgenera of Drosophila (Scaptodrosophila and Hirtodrosophila) should be recognized as independent genera. Grimaldi’s (1990) analysis, however, also proposed several unconventional relationships. These are the result of bias in his analytical methodology (see Remsen and O’Grady, 2002), and should perhaps be considered suspect. The most controversial of Grimaldi’s results is the placement of the endemic Hawaiian Drosophilidae − a hypothesis that is discussed at length below.

Figure 1.3 Phylogenetic hypothesis of Drosophilidae based on Grimaldi (1990), after DeSalle and Grimaldi (1991).

A number of molecular phylogenetic studies have proposed genus-level relationships in the family Drosophilidae (DeSalle, 1992; Pelendakis and Solignac, 1993; Russo et al., 1995; Remsen and DeSalle, 1998; Kwiatowski and Ayala, 1999; Tatarenkov et al., 2001; Remsen and O’Grady, 2002). These may vary slightly from one another, but several key relationships are consistently recovered (Figures 1.4, 1.5). The main criticism of the molecular work is that the taxon sampling is much less compared to the morphological studies − a fact largely due to the rarity of some drosophilid groups. Remsen and O’Grady (2002) have greatly expanded both taxon and character sampling in this group (Figure 1.5), but much work remains to be done.

Figure 1.4 (a) Summary of molecular phylogenetic hypotheses from Kwiatowski and Ayala (1999); (b) Summary phylogeny based on Tatarenkov et al. (2001).

Figure 1.5 Phylogenetic hypothesis for Drosophilidae presented by Remsen and O’Grady (2002).

Within the genus Drosophila we follow a version of Throckmorton’s (1975) radiations, modified based on results from recent phylogenetic studies and outlined in Figure 1.6. This scheme, while following the latest developments in drosophilid systematics, is somewhat confusing in that several major groups, including the genus Drosophila, are not monophyletic. The differences and similarities between the various hypotheses will be compared and contrasted below.

Figure 1.6 Taxonomic relationships in Drosophilidae.

Steganinae

The Steganinae is a small, poorly understood subfamily of drosophilid flies that currently contains about 400 described species (Wheeler, 1982, 1986; Baechli, 2005). Many authors consider this group to be primitive within the Drosophilidae, but it is actually the sister taxon of the larger, better studied Drosophilinae (Throckmorton, 1966, 1975; Wheeler, 1982; Grimaldi, 1988, 1990). Grimaldi (1988, 1990) proposed two different phylogenetic hypotheses for this group (Figures 1.7a, 1.7b). These trees mostly differed in the placement of the subgenus Amiota. A few molecular studies have included Steganine taxa, but most have not sampled this group extensively enough to propose a firm hypothesis. Remsen and O’Grady’s (2002) results, while only including four Steganine taxa, do not fully agree with either of Grimaldi’s hypotheses (Figure 1.8). Clearly, additional work expanding the number of taxa sampled with molecular characters will be required to better understand the relationships within the basal Drosophilidae. This will, in turn, enhance our knowledge of host plant adaptation in the Drosophilidae as a whole (see Powell, 1997).

Figure 1.7 (a) Phylogeny of Steganinae after Grimaldi (1988); (b) phylogeny of Steganinae after Grimaldi (1990).

Figure 1.8 Phylogeny of some Steganinae species based on molecular characters (Remsen and O’Grady, 2002).

Drosophilinae

The phylogenetic relationships of the subfamily Drosophilinae have been addressed in a number of studies (Throckmorton, 1975; Okada 1989; Grimaldi, 1990; Remsen and DeSalle, 1998; Tatarenkov and Ayala, 2001; Remsen and O’Grady, 2002). No consensus view can, at this point (however, see Figures 1.4, 1.5), be proposed, so we will review the phylogenetic relationships within this subfamily sequentially below, as we treat each of the major lineages in this group (Figure 1.6; Ashburner, 1989, 2004; Powell, 1997).

Genus Chymomyza

The genus Chymomyza is a genus of about 60 described species (Table 1.1), the majority of which are found in the Old and New World tropics. This genus is characterized by having the proclinate orbital setae inserted posterior to the anterior reclinate seta (see Chapter 2 for detailed discussion of all morphological characters). Most members of this group also possess femoral spines (see Grimaldi, 1986:356, 1990:65). Okada (1976) used morphological characters to divide Chymomyza into five species groups: aldrichii, costata, fuscimana, obscura, and procnemis (Figure 1.9). Grimaldi (1986) described seven new species in the aldrichii species group, all of which are found in the Neotropics, and presented a phylogeny of this group (Figure 1.10) that greatly improves the resolution in this clade over Okada’s tree. The aldrichii species group is notable because at least five species placed in it are hypercephalic.

Table 1.1

Species placed in various genera and selected genus Drosophila groups

*Species in culture at the Tucson Stock Center; + All taxa in these groups were not listed.

Figure 1.9 Subdivision and phylogenetic relationships within the genus Chymomyza, after Okada (1976).

Figure 1.10 Phylogeny of the aldrichii species subgroup (genus Chymomyza), after Grimaldi (1988).

Many members of the genus Chymomyza are attracted to cut wood, and this may serve as a lek or oviposition site for these species. Grimaldi (1986) considered the use of this substrate to be a specialization, possibly derived from a polyphagous habit. A number of Neotropical Chymomyza species display elaborate courtship behaviors, including male display and aggression (Grimaldi, 1986; Grimaldi and Fenster, 1989).

Genus Drosophila

The genus Drosophila is a very large group of well over 1500 described species. Sturtevant (1939, 1942) divided Drosophila into a number of subgenera. Currently, Drosophila is divided into ten subgenera (Ashburner, 1989, 2004), the largest of which is undoubtedly the subgenus Drosophila. The subgenus Sophophora, with over 300 described species, is the second largest. Together, the subgenera Drosophila and Sophophora account for roughly 90 per cent of the diversity in the genus Drosophila. Although no single study has extensively sampled this entire group, several studies have treated parts of this genus. What is clear at this time is that the genus Drosophila is not monophyletic and should probably be divided into several clades (see sections below). Throckmorton’s (1975) review of phylogeny in the family Drosophilidae included a number of radiations, or assemblages of closely related species groups (Figure 1.2). This higher-level taxonomic group, fitting between subgenus and species group, is unique to the Drosophilidae. We have adopted its use, particularly within the large, diverse subgenus Drosophila, as a way to organize our discussions of phylogeny in this family. Further phylogenetic analyses employing greatly expanded taxon and character sampling will lead to a firmer understanding of this group, and will serve as the groundwork for further revisionary studies of this family.

Genus Drosophila: subgenus Dorsilopha

The subgenus Dorsilopha was described by Sturtevant (1942) as a subgenus of Drosophila containing a single species, D. busckii. Recently, two additional species have been described from Burma (Toda, 1986), bringing the total number of taxa in this subgenus to three (Table 1.1). Remsen and O’Grady (2002) placed this subgenus close to the genus Zaprionus (Figure 1.5), similar to its placement in other molecular phylogenies (Figures 1.4a, 1.4b).

Genus Drosophila: subgenus Drosophila

Below, we follow a version of Throckmorton’s radiations, modified after a number of recent molecular and morphological analyses (Tatarenkov and Ayala, 2001; Remsen and O’Grady, 2002). The major groups covered (Figure 1.6) include (1) the virilis-repleta radiation; (2) the immigrans-tripunctata radiation; and (3) the Hawaiian Drosophilidae, a group containing the Hawaiian Drosophila and the genus