Marvin Wasserman

Polytene Chromosomal Maps of 11 Drosophila Species: The Order of Genomic Scaffolds Inferred From Genetic and Physical Maps

The sequencing of the 12 genomes of members of the genus Drosophila was taken as an opportunity to reevaluate the genetic and physical maps for 11 of the species, in part to aid in the mapping of assembled scaffolds. Here, we present an overview of the importance of cytogenetic maps to Drosophila biology and to the concepts of chromosomal evolution. Physical and genetic markers were used to anchor the genome assembly scaffolds to the polytene chromosomal maps for each species. In addition, a computational approach was used to anchor smaller scaffolds on the basis of the analysis of syntenic blocks. We present the chromosomal map data from each of the 11 sequenced non-Drosophila melanogaster species as a series of sections. Each section reviews the history of the polytene chromosome maps for each species, presents the new polytene chromosome maps, and anchors the genomic scaffolds to the cytological maps using genetic and physical markers. The mapping data agree with Mullers idea that the majority of Drosophila genes are syntenic. Despite the conservation of genes within homologous chromosome arms across species, the karyotypes of these species have changed through the fusion of chromosomal arms followed by subsequent rearrangement events.

Character displacement for sexual isolation between Drosophila mojavensis and Drosophila arizonensis.

According to Brown and Wilson (1956) character displacement exists between two closely related species when their allopatric populations are very similar and their sympatric populations are quite distinct in one or more characters. The disparate characters could be either morphological, physiological, ecological, or behavioral. They viewed the phenomenon as a result of species interaction in sympatry, where divergence would decrease competition or reduce hybridization, and thus be at a selective advantage. They gave several instances which have since been widely cited as classical, textbook examples. More recently, Grant (1972, 1975) reexamined the phenomenon of interspecific interaction, including convergent character displacement as well as the divergent character displacement described by Brown and Wilson. Restricting himself to morphological attributes, Grant reviewed the literature and concluded that there really was no good example of character displacement. Where divergent character displacement had been proposed to exist, Grant argued, the data were incomplete or else the reason for the divergence was not a result of interspecific competition but rather other ecological factors. We feel that many of these problems could be avoided if one could demonstrate character displacement for sexual isolation. Although ethological barriers to interspecific mating are expected to be developed in allopatric populations (Muller, 1939, 1942), their reinforcement in sympatric populations can only be attributed to interspecific interaction and not to other correlated factors. Dobzhansky (1940) proposed on theoretical grounds that sexual isolation between closely related species should be greater in sympatric than in allopatric populations. His arguments essentially are that if there is selection against the hybrids, those individuals which are involved in interspecific crosses would be wasting their gametes. Any gene which improved the ability of the species to discriminate would be advantageous and would increase in frequency, or be fixed, in the region of sympatry. Reinforcement of sexual isolation by means of artificial selection against the hybrids can sometimes be accomplished in the laboratory (Koopman, 1950; Thoday and Gibson, 1962; Kessler, 1966; Ehrman, 1971, 1973; Soans et al., 1974). However, despite its theoretical importance and despite the moderate degree of success obtained in the laboratory, evidence for reproductive character displacement in natural populations is poor and controversial (see e.g., Loftus-Hills, 1975 and Jones, 1975). It has only been shown to exist in some anurans (Fouquette, Jr., 1975; Littlejohn and Loftus-Hills, 1968), some grasshoppers (Cohn and Cantrall, 1974), possibly in two species of damselfly (Waage, 1975), and between races of Drosophila paulistorum (Ehrman, 1965). In 1973 we undertook an investigation on the sexual isolation between natural populations of Drosophila mojavensis and Drosophila arizonensis species. The advantages of using Drosophila for this purpose are manifest in the availability of techniques which would not only enable us to detect reinforcement if it exists, but also to measure its strength and perhaps determine its genetic basis. D. mojavensis

Evolutionary cytogenetics of the Drosophila buzzatii species complex

The salivary gland chromosomes of 10 species in the Drosophila mulleri subgroup (repleta group) have been re-analysed. These include the eight members of the South American buzzatii and martensis clusters, previously ascribed to the mulleri complex, and the two Caribbean species D. stalkeri and D. richardsoni, previously comprising the stalkeri complex. The chief results can be summarized as follows. Inversion 3a is not present in the martensis cluster. Hence, there is no cytological link between this cluster, or the buzzatii cluster, and the rest of the mulleri complex. Accordingly, a new species complex, the buzzatii complex, is established with the two South American clusters. D. stalkeri and D. richardsoni share at least two inversions with all the species in the buzzatii and martensis clusters, and produce hybrids in interspecific crosses with many of them. This indicates a close phylogenetic relationship. Therefore, D. stalkeri and D. richardsoni are incorporated as a cluster within the newly erected buzzatii complex. A phylogenetic tree illustrating the chromosomal evolution of the buzzatii complex is presented and all the previous cytological information concerning its members is reviewed.

The Significance of Asymmetrical Sexual Isolation

Kaneshiro (1976) observed asymmetrical sexual isolation among the Hawaiian Drosophila planitibia subgroup of flies, and suggested a model of evolution of sexual behavior wherein females of putative ancestral species are sexually more isolated from males of derived species than are females of derived species from males of the ancestral species. The model has subsequently been expanded and new, allegedly supportive data presented (Kaneshiro, 1980, 1983; Ohta, 1978; Arita and Kaneshiro, 1979; Ahearn, 1980; Kaneshiro and Kurihara, 1981; Dodd and Powell, 1985). Ostensibly, the Kaneshiro model provides a reasonable explanation of asymmetrical sexual isolation, which may result from several underlying genetic mechanisms. Kaneshiro (1976) suggested that during a new invasion of a previously uninhabited locality, genetic drift acting upon a small number of migrants may cause the loss of several facets of male courtship behavior. Ancestral females would then be relatively unwilling to accept behaviorally deficient males. Derived females would accept these males as well as ancestral ones whose courtship pattern included all that was still present in the derived males. Ohta (1978), studying yet another group of Hawaiian flies, showed that derived females had a higher sex drive and were more receptive to all males than were ancestral females. Perhaps in a small migrant population, where encounters between flies might be relatively rare events, those females that had a strong sex drive would have been selected for because they were more likely to mate than those females that were innately slower to mate. This scenario could lead to the loss of selection for the complete courtship pattern, particularly if there were no other closely related species present in the newer locality.

Inversion Polymorphism in Island Species of Drosophila

Chromosomal mutations, such as inversions, are major, observable changes in the Drosophila genome, and therefore have been extensively and intensively studied for many years (Bush et al.,1977; Carson and Yoon, 1982; Dobzhansky, 1970; Sperlich and Pfriem, 1986; Wasserman, 1982a,b). The factors involved in their origin, survival in the heterozygous condition, and fixation must be almost as diverse as the species in which they occur. Moreover, those elements that tend to promote polymorphism are almost certainly antagonistic to those that lead to the fixation of these mutations. It should not be surprising, then, to find that there is no single evolutionary mechanism that can fully explain the chromosomal variability found in nature.

SEXUAL PREFERENCE FOR FEMALES REARED ON CACTUS MEDIA BY DROSOPHILA PEGASA MALES

It has long been suggested that a unique shift in habitat of a small segment of an obligatory sexually reproducing population may lead, under certain circumstances, to sympatric speciation (Thorpe, 1945; but see Mayr, 1947). One necessity is the imprinting of the new habitat on its new inhabitants. Some imprinting has been observed in the Drosophila obscura group D. persimilis and D. pseudoobscura (Taylor and Powell, 1978; Klaczko et al., 1986) and D. subobscura (Nigro and Shorrocks, 1982)in which captured, marked, released and recaptured individuals tended to return to their area oforigin. However, in these species, habitat preference tends to maintain polymorphism rather than to initiate speciation. Thus, habitat specificityalone is insufficientfor sympatric speciation. For habitat shifts to be effective in promoting speciation, the shift must rapidly (immediately?) reproductively isolate the subpopulation from its ancestral sympatric population (Bush, 1975; Futuyma and Mayer, 1980). In principal, this might occur in, at least, three ways. First, invasion of a new host may lead to an immediate shift in the time when the individuals reach sexual maturity. Given one generation per year, such a temporal change would effectively and immediately reproductively isolate the two ecotypes. This has been suggested to have occurred in the genus Chrysopa (Tauber and Tauber, 1977; Tauber et al., 1977). Second, courtship, mating and oviposition may be limited to the host: a host shift results in immediate isolation. The best proposed natural example is found in the fruit fly genus Rhagoletis (reviewed by Bush, 1986). In both of these modes, separation of sexual forms occurs immediately and is complete. Third, the ecological separation need not be complete if sexual isolation through positive assortative mating is rapidly developed. Attempts in the laboratory to obtain sexual isolation in Drosophila by changing their food have been unsuccessful (Futuyma and Mayer, 1980). Perhaps much of the difficulty lies in the fact that most of the attempts were made on polyphagous members of the D. melanogaster and D. obscura species groups that are adapted to a variety of diets; a dietary change in a monophagous species is more likely to produce an effect if such effectsdo occur. Drosophila pegasa, a monophagous species, whose only known host is the cactus, Opuntia, has a number of characteristics that make it useful for study. It is unique in that most males make no attempt to court, but rather attack conspecificfemales and forciblymount them (Wasserman et al., 1971). Mounted males ride