Genetic analysis of speciation by means of introgression into Drosophila melanogaster

Abstract

In the last decade, the genetic basis of reproductive isolation has been shown to be surprisingly polygenic, and yet even the most efficient system currently in use could lend itself to molecular analysis only in highly selected cases. By extending the recent discovery of fertility rescue between Drosophila melanogaster and Drosophila simulans, we show that this hybridization can permit systematic and precise delineation of the genetic and molecular basis of speciation. In a region of 5% of the D. simulans genome introgressed into D. melanogaster, we discover at least six genes of hybrid male sterility and none for female sterility by deficiency mapping. A single case of hybrid inviability has been tracked down to a 3-Kb element that was inserted into the Cyclin E locus during species hybridization. The extent of interspecific genetic divergence underlying hybrid male sterility, especially in contrast with the low degree of inviability and female sterility, is far greater than expected from previous studies.O ne of the important subjects in speciation study is the genetic mechanism of reproductive isolation (1, 2). Drosophila melanogaster, with its wealth of resources, could allow the delineation of genes of reproductive isolation by genetic, cytological, and molecular means. Unfortunately, this species does not produce progeny beyond the F1 generation when crossed to any of its known sibling species, including Drosophila simulans (3-5). Since the time A. H. Sturtevant observed this sterility 80 years ago (3), evolutionary geneticists have relied on other species pairs. Th. Dobzhansky (6) was the first to do so, and many have since followed. Nevertheless, the progress has been slow (7), and not until recently has a gene of reproductive isolation been cloned from Drosophila (8). To move the field at a faster pace, a more efficient system involving D. melanogaster is highly desirable.Various attempts at bringing this species into speciation research have been made, including mating triploid D. melanogaster females to heavily irradiated D. simulans males to obtain the equivalent of F2s (9, 10), searching for sibling species that might be crosshybridizable (4, 5), examining far-flung populations that might be reproductively isolated (11, 12), and surveying for hybrid inviability rescue mutations (13-16). None has succeeded in making this ''model organism'' usable material for systematic studies of the genetics of speciation. The recent discovery of combinations of lines from D. melanogaster and D. simulans that yield fertile hybrid females has perhaps given us the best chance to tap into the resources of D. melanogaster (17). Materials and MethodsNomenclature. We shall briefly explain the conventional Drosophila nomenclature used in this study. For example, Df(2L) J39 (31C-D; 32D-E) denotes a deletion on the left arm of the second chromosome with the two breakpoints determined to be at the locations of 31C (or 31D) and 32D (or 32E) of the polytene chromosome, respectively. This deletion is named J39. Following this ...

A Simple Genetic Incompatibility Causes Hybrid Male Sterility in Mimulus

“…Moreover, the number of factors that cause hybrid male sterility between Drosophila species often greatly exceeds the number of factors that cause hybrid inviability or female sterility (True et al 1996;Sawamura et al 2000;Tao et al 2003a). For example, when Tao et al (2003a) introgressed segments of the Drosophila mauritiana third chromosome into a D. simulans genetic background, they found that many introgressions caused male sterility, but none caused hybrid lethality or female sterility.…”

“…To date, much of our understanding of the genetics of postzygotic isolation is based on empirical studies of divergence between Drosophila species. Indeed, several patterns appear to characterize the genetic basis of hybrid incompatibility in Drosophila (reviewed in Coyne and Orr 2004): (1) hybrid incompatibility alleles are generally recessive (Presgraves 2003;Tao et al 2003a,b;Tao and Hartl 2003), (2) hybrid male sterility is highly polygenic and complex (Davis and Wu 1996;Taoet al 2003b), and (3) hybrid male sterility evolves more readily than female sterility or hybrid lethality (Hollocher and Wu 1996;True et al 1996;Sawamura et al 2000;Tao et al 2003a).…”

Nuclear–Mitochondrial Epistasis and Drosophila Aging: Introgression of Drosophila simulans mtDNA Modifies Longevity in D. melanogaster Nuclear Backgrounds

“…The interspecific mtDNA introgression strains were obtained from K. Sawamura (Sawamura et al 2000). In a search for D. simulans lines (hereafter Dsim) that would rescue the sterility of hybrids from crosses with D. melanogaster (hereafter Dmel), a Dsim line was discovered (C167.4) that produced fertile F 1 females in a Dsim female 3 Dmel male cross (Davis et al 1996).…”

Distribution of the Bari-I transposable element in stable hybrid strains between Drosophila melanogaster and Drosophila simulans and in Brazilian populations of these species

“…In fact, the hybrid strains SM 3 and SM 4 presented Bari-I sequences from D. melanogaster (Figure 3, thick arrows), indicating that hybridization and introgression of the genetic material had occurred. Sawamura et al (2000) also demonstrated introgression of genetic material carrying a complex of six sterility genes from the D. simulans into the D. melanogaster genome. Capy et al (1998) has stated that although horizontal transfer is frequently invoked as a transfer mechanism, in the transfer of genetic material between sexually isolated species at least two mechanisms can operate: transfer by vectors and/or transfer by fertile hybrids retrocrossed with one of the parental species, our results supporting the latter mechanism.…”