That stupid little saprophyte.

-William Morton Wheeler, on Drosophila melanogaster

Drosophila fruitflies may not have the behavioral repertoire of ants that so fascinated the famous entomologist W. M. Wheeler, but Drosophila has revolutionized biology more than any other organism. Contrary to popular belief, Drosophila does not naturally live in little vials. There are approximately 1,000 species in the genus, which breed in a great variety of plants and other substrates. Some species are highly polyphagous and have followed humans around the globe, the so-called tramp or garbage species. The laboratory fruitfly, Drosophila melanogaster, is one such tramp species. It was originally used by T. H. Morgan and his "fly group" at Columbia University for probing the elements of heredity and the behavior of chromosomes (see Sturtevant, 1965; Kohler, 1994). Because its genetics became so well known, D. melanogaster has been and is still used in all sorts of laboratory research, from cell biology, to physiology, behavior, and ecology (Lachaise et al., 1988; Ashburner, 1989), making it, arguably, the best known eukaryotic organism. To better understand D. melanogaster, there has been intensive comparison of this species to its three closest relatives: D. simu-lans, which is a polyphagous African species introduced around the world; D. mauritiana, endemic to the islands of Mauritius and Rodriguez in the Indian Ocean; and D. sechel-lia, endemic to the Seychelles Islands, also in the Indian Ocean. The ancestral distribution of D. melanogaster is

1.4. Relationships among closely related species in the Drosophila melanogaster complex, differences being best reflected in the male genitalia (shown here). Relationships based on Hey and Kliman (1993) and Kliman et al. (2000).

believed to be central Africa. Collectively, these species comprise the melanogaster complex of species.

Individuals of the melanogaster complex are consistently separated and grouped on the basis of male and female genitalia (Figure 1.4), mating behavior (Cowling and Burnet, 1981; Cobb et al., 1986), chromosomes (Ashburner and Lemeunier, 1976; Lemeunier and Ashburner, 1976), DNA sequences (Hey and Kliman, 1993; Kliman and Hey, 1993; Kliman et al., 2000; Schawaroch, 2002), and other features, including larval diet. For example, even though D. simulans and D. melanogaster breed in a great variety of decaying fruits, D. sechellia is very specialized and breeds naturally only in fruits of Morinda cit-rifolia (Rubiaceae), which contain toxins that the other species can't tolerate. Drosophila simulans, D. sechellia, and D. mauritiana are most closely related, based on DNA sequences (Kliman et al., 2000), their homosequential poly-tene chromosomes (there are no distinguishing inversions), and fertile F1 hybrid females (F1 males are sterile). In a comprehensive study of 14 genes and nearly 40 strains of these species (Hey and Kliman, 1993; Kliman and Hey, 1993; Kliman et al., 2000), all or most strains of these species are grouped according to traditional separation using morphology and chromosomes. Interestingly, though, a few strains of D. simulans grouped with D. sechellia or D. mauritiana, but groupings varied depending on the gene.

Apparently, D. sechellia and D. mauritiana evolved nearly contemporaneously as peripheral, isolated populations of D. simulans. This has fundamental implications for systemat-ics because in this case a living species is considered ancestral and not a simple two-branched divergence from an extinct common ancestor. In a mainstream phylogenetic view, at least some strains of D. simulans would not belong to that species, because they make D. simulans a paraphyletic taxon (basically everything left over after D. mauritiana and D. sechellia were extracted). Yet, D. simulans has distinctive (diagnosable) and consistent differences with other species in the complex. Also, a typical assumption in phylogenetic analyses is that divergence is bifurcating, or two-branched, even though traditional models of speciation allow for the simultaneous origin of species. Traditionally, it has been thought that isolated populations on the periphery of the range of an ancestral species can diverge into species, the old "Reisenkreiss" model of speciation, which may actually be the case for D. simulans, D. mauritiana, and D. sechellia. Most importantly, though, when all the evidence is considered in total, from DNA sequences to behavior, individual flies in the melanogaster complex are consistently categorized into discrete groups of individuals, which can be done even on the basis of morphology alone.

Hybrids in the melanogaster complex have also been intensively studied, and the genetics of hybrid sterility are known to be controlled by at least five genes on the X

chromosome (Coyne and Charlesworth, 1986; Wu et al., 1993), and probably many more loci overall (Wu and Palopoli, 1994). Interestingly, it has been estimated on the basis of molecular clock estimates (Kliman and Hey, 1993; Kliman et al., 2000) that D. sechellia and D. mauritiana diverged from D. simulans merely 420,000 and 260,000 years ago, respectively.

A few other examples in Drosophila show more of a continuum of groupings or divergence among individuals, perhaps the best studied being in the Drosophila willistoni species group. The willistoni group consists of 25 Neotropical species, six of which are "sibling" (cryptic) species, and among these six there are 12 "semispecies" and "subspecies," most of them in Drosophila paulistorum (reviewed by Ehrman and Powell, 1982).1 The semispecies of paulistorum are morphologically indistinguishable so far as is known (one is never sure that very subtle features are being overlooked), and were first identified on the basis of chromosomal inversions. They also have distinct male courtship songs (Kessler, 1962; Ritchie and Gleason, 1995), and the hybrids of most crosses produce sterile males (Ehrman and Powell, 1982). DNA sequences of some paulistorum semispecies were examined (Gleason et al., 1998), and these also group discretely. Thus, under evolutionary and phylogenetic definitions of species, Drosophila paulistorum itself could be considered a complex of cryptic species, but more data are needed to address this.

Interestingly, mating behavior (usually male courtship behavior) appears to diverge in Drosophila more quickly and prior to noticeable differences in morphology (e.g., Chang and Miller, 1978; Gleason and Ritchie, 1998; Grimaldi et al., 1992), and this appears to be the case as well in many insects (Henry, 1994). It is known that just a few amino acid changes in a protein can dramatically affect, for example, an important component of Drosophila courtship song, the pulse interval (coded by the period gene; Wheeler et al., 1991). Most morphological characters, by contrast, such as merely the shape of a lobe on the male terminalia of Drosophila (Coyne et al., 1991), are highly polygenic. Divergence in mating behavior probably leads to further divergence (Liou and Price, 1994), which is eventually expressed morpologically.

1 Sibling species and semispecies are categories devised largely by drosophilists and can be ambiguous terms. Sibling species are morphologically very similar or even identical, but the word "sibling" implies a close relationship, much like "sister group" in phylogenetics (which we discuss later). In fact, there are six sibling species in the willistoni group, some of which are closest relatives. Thus, we prefer the term "cryptic species" to simply mean morphologically indistinguishable or very subtly different species. The terms "semispecies" and "incipient species" imply these are not quite species, but are perhaps in the process of becoming species. But, because we can't predict the future, simply calling them populations and forms also adequately conveys their nature.

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