Loss of notum macrochaetae as an interspecific hybrid anomaly between Drosophila melanogaster and D. simulans.

With the aim of revealing genetic variation accumulated among closely related species during the course of evolution, this study focuses on loss of macrochaetae on the notum as one of the developmental anomalies seen in interspecific hybrids between Drosophila melanogaster and its closely related species. Interspecific hybrids between a line of D. melanogaster and D. simulans isofemale lines exhibited a wide range in the number of missing bristles. By contrast, D. mauritiana and D. sechellia lines showed almost no reduction in bristle number in hybrids with D. melanogaster. Genetic analysis showed that the D. simulans X chromosome confers a large effect on hybrid bristle loss, although X-autosome interaction may be involved. This suggests that at least one genetic factor contributing to hybrid anomalies arose recently on a D. simulans X chromosome. Moreover, the results indicate sex dependency: the male hybrids were more susceptible to bristle loss than the female hybrids were. Use of cell type markers suggests that the defect does not lie in cell fate decisions during bristle development, but in the maintenance of neural fate and/or differentiation of the descendants of sensory mother cells.     

Genetic screens for factors involved in the notum bristle loss of interspecific hybrids between Drosophila melanogaster and D. simulans

Interspecific cross is a powerful means to uncover hidden within- and between-species variation in populations. One example is a bristle loss phenotype of hybrids between Drosophila melanogaster and D. simulans, although both the pure species have exactly the same pattern of bristle formation on the notum. There exists a large amount of genetic variability in the simulans populations with respect to the number of missing bristles in hybrids, and the variation is largely attributable to simulans X chromosomes. Using nine molecular markers, I screened the simulans X chromosome for genetic factors that were responsible for the differences between a pair of simulans lines with high (H) and low (L) missing bristle numbers. Together with duplication-rescue experiments, a single major quantitative locus was mapped to a 13F-14F region. Importantly, this region accounted for most of the differences between H and L lines in three other independent pairs, suggesting segregation of H and L alleles at the single locus in different populations. Moreover, a deficiency screening uncovered several regions with factors that potentially cause the hybrid bristle loss due to epistatic interactions with the other factors.     

Compensatory cis-trans evolution and the dysregulation of gene expression in interspecific hybrids of Drosophila

Hybrids between species are often characterized by novel gene-expression patterns. A recent study on allele-specific gene expression in hybrids between species of Drosophila revealed cases in which cis- and trans-regulatory elements within species had coevolved in such a way that changes in cis-regulatory elements are compensated by changes in trans-regulatory elements. We hypothesized that such coevolution should often lead to gene misexpression in the hybrid. To test this hypothesis, we estimated allele-specific expression and overall expression levels for 31 genes in D. melanogaster, D. simulans, and their F1 hybrid. We found that 13 genes with cis-trans compensatory evolution are in fact misexpressed in the hybrid. These represent candidate genes whose dysregulation might be the consequence of coevolution of cis- and trans-regulatory elements within species. Using a mathematical model for the regulation of gene expression, we explored the conditions under which cis-trans compensatory evolution can lead to misexpression in interspecific hybrids.     

Variation in response to CO2 in Drosophila melanogaster and D. simulans

A type of slow-recovery from high temperature CO2 exposure is a wild-type characteristic of Drosophila simulans. Species hybrids of wild-type D. melanogaster and D. simulans have intermediate recovery times. The response to nitrogen exposure at both high and low temperatures is the same for the two species suggesting that the observed CO2 response is more than just anoxia. Since there is no female bias in hybrids, and since injections of D. simulans extract into D. melanogaster produced no increase in CO2 sensitivity in the recipients, we conclude that the prolonged recovery time results from genomic differences between D. simulans and D. melanogaster, and is not due to a sigma-like infectious agent.     

Variation in Drosophila sensory bristle number at 'Evolution Canyon'

'Evolution Canyon' on Mount Carmel, Israel, displays highly contrasting physical and biotic environments on a micro-geographic scale, and is a natural laboratory for investigating genetic responses to variable and extreme environments across species. Samples of Drosophila melanogaster and D. simulans were collected from three sites each on the north- and south-facing slopes of the canyon along altitudinal transects, and one site on the valley floor. Numbers of abdominal and sternopleural sensory bristles were recorded for each of these subpopulations in three thermal environments. In D. simulans, sternopleural bristle number exhibited micro-geographic differentiation between the north- and south-facing slopes, while abdominal bristle number was stable across subpopulations. In D. melanogaster, the magnitudes of the difference in mean sternopleural bristle number between the north- and south-facing slopes and of mean abdominal bristle number along the altitudinal gradients were both conditional on rearing temperature. Thus, the pattern of genetic variation between sites was consistent with underlying heterogeneity of genetic mechanisms for response to the same environmental gradients between traits and sibling species. In contrast, the genetic architecture of bristle number at the level of variation within populations was very similar between species for the same bristle trait, although the two traits differed in the relative contribution of genotype by temperature and genotype by sex interaction.     

High rate of horizontal transfer of transposable elements in Drosophila

We have conducted molecular population genetics analyses to understand the relationships among the transposable elements (TEs) in Drosophila melanogaster, in combination with sequence comparisons of TEs from two related species, D. simulans and D. yakuba. We observed much lower than expected genetic differences among elements, clear evidence for departure from expectations for equilibrium copy numbers and little divergence between species. This suggests that a large proportion of TEs in D. melanogaster had a recent origin as a result of interspecies movement.     

Identical satellite DNA sequences in sibling species of Drosophila

The evolution of simple satellite DNAs was examined by DNA-DNA hybridization of ten Drosophila melanogaster satellite sequences to DNAs of the sibling species, Drosophila simulans and Drosophila erecta. Seven of these repeat types are present in tandem arrays in D. simulans and each of the ten sequences is repeated in D. erecta. In thermal melts, six of the seven satellite sequences in D. simulans and seven of the ten sequences in D. erecta melted within 1 deg.C of the corresponding values in D. melanogaster. The remaining sequences melted within 3 deg.C of the homologous hybrids. Therefore, there is little or no alteration in those satellite sequences held in common, despite a period of about ten million years since the divergence of D. melanogaster and D. simulans from a common ancestor. Simple satellite sequences appear to be more highly conserved than coding regions of the genome, on a per nucleotide basis. Since multiple copies of three satellite sequences could not be detected in D. simulans yet are present in D. erecta, a species more distantly related to D. melanogaster than is D. simulans, these sequences show discontinuities in evolution. There were major quantitative variations between species, showing that satellite DNAs are prone to massive amplification or diminution events over timespans as short as those separating sibling species. In D. melanogaster, these sequences amount to 21% of the genome but only 5% in D. simulans and 0.4% in D. erecta. There was a general trend of lower abundance with evolutionary distance for most satellites, suggesting that the amounts of different satellite sequences do not vary independently during evolution.     

Evolution of a desaturase involved in female pheromonal cuticular hydrocarbon biosynthesis and courtship behavior in Drosophila

Drosophila species exhibit polymorphism in female pheromonal cuticular hydrocarbons, with 7-monoenes produced in Drosophila simulans and 7,11-dienes in most populations of Drosophila melanogaster (5,9-dienes in several African populations). A female-biased desaturase, desatF, expressed only in D. melanogaster is involved in the synthesis of 7,11-dienes. We investigated the role of desatF in 5,9-diene flies. We constructed a 5,9-diene strain knock-down for desatF and showed that desatF is involved in 5,9-diene formation. We also studied D. melanogaster/D. simulans hybrids. These hybrid females produced dienes and received normal courtship from D. melanogaster males, but copulation success was reduced. With D. simulans males, courtship was decreased and no copulation occurred. Hybrids with a chromosomal deletion of the D. melanogaster desatF gene had no dienes and received normal courtship from D. simulans males; depending on the D. simulans parental strain, 7-19% of them succeeded in mating. D. simulans desatF promoter region shows 21-23% gaps and 86-89% identity with D. melanogaster promoter region, the coding region 93-94% identity, depending on the strain. These differences could explain the functional polymorphism of desatF observed between both species, contributing to different cuticular hydrocarbon profiles, that constitute an effective barrier between species.     

Ancestral polymorphism and recent invasion of transposable elements in Drosophila species

ABSTRACT: BACKGROUND: During the evolutionary history of transposable elements, some processes, such as ancestral polymorphisms and horizontal transfer of sequences between species, can produce incongruences in phylogenies. We investigated the evolutionary history of the transposable elements Bari and 412 in the sequenced genomes of the Drosophila melanogaster group and in the sibling species D. melanogaster and D. simulans using traditional phylogenetic and network approaches. RESULTS: The maximum likelihood (ML) phylogenetic analyses revealed incongruences and unresolved relationships for both the Bari and 412 elements. The DNA transposon Bari within the D. ananassae genome is more closely related to the element of the melanogaster complex than to the sequence in D. erecta, which is inconsistent with the species phylogeny. Divergence analysis and the comparison of the rate of synonymous substitutions per synonymous site of the Bari and host gene sequences explain the incongruence as an ancestral polymorphism inherited stochastically by the derived species. Unresolved relationships were observed in the ML phylogeny of both elements involving D. melanogaster, D. simulans and D. sechellia. A network approach was used to attempt to resolve these relationships. The resulting tree suggests recent transfers of both elements between D. melanogaster and D. simulans. The divergence values of the elements between these species support this conclusion. CONCLUSIONS: We showed that an ancestral polymorphism and recent invasion of genomes due to introgression or horizontal transfer between species occurred during the evolutionary history of the Bari and 412 elements in the melanogaster group. These invasions likely occurred in Africa during the Pleistocene, before the worldwide expansion of D. melanogaster and D. simulans.     

Cis-by-Trans regulatory divergence causes the asymmetric lethal effects of an ancestral hybrid incompatibility gene

The Dobzhansky and Muller (D-M) model explains the evolution of hybrid incompatibility (HI) through the interaction between lineage-specific derived alleles at two or more loci. In agreement with the expectation that HI results from functional divergence, many protein-coding genes that contribute to incompatibilities between species show signatures of adaptive evolution, including Lhr, which encodes a heterochromatin protein whose amino acid sequence has diverged extensively between Drosophila melanogaster and D. simulans by natural selection. The lethality of D. melanogaster/D. simulans F1 hybrid sons is rescued by removing D. simulans Lhr, but not D. melanogaster Lhr, suggesting that the lethal effect results from adaptive evolution in the D. simulans lineage. It has been proposed that adaptive protein divergence in Lhr reflects antagonistic coevolution with species-specific heterochromatin sequences and that defects in LHR protein localization cause hybrid lethality. Here we present surprising results that are inconsistent with this coding-sequence-based model. Using Lhr transgenes expressed under native conditions, we find no evidence that LHR localization differs between D. melanogaster and D. simulans, nor do we find evidence that it mislocalizes in their interspecific hybrids. Rather, we demonstrate that Lhr orthologs are differentially expressed in the hybrid background, with the levels of D. simulans Lhr double that of D. melanogaster Lhr. We further show that this asymmetric expression is caused by cis-by-trans regulatory divergence of Lhr. Therefore, the non-equivalent hybrid lethal effects of Lhr orthologs can be explained by asymmetric expression of a molecular function that is shared by both orthologs and thus was presumably inherited from the ancestral allele of Lhr. We present a model whereby hybrid lethality occurs by the interaction between evolutionarily ancestral and derived alleles.     

Incompatibility between X chromosome factor and pericentric heterochromatic region causes lethality in hybrids between Drosophila melanogaster and its sibling species

The Dobzhansky-Muller model posits that postzygotic reproductive isolation results from the evolution of incompatible epistatic interactions between species: alleles that function in the genetic background of one species can cause sterility or lethality in the genetic background of another species. Progress in identifying and characterizing factors involved in postzygotic isolation in Drosophila has remained slow, mainly because Drosophila melanogaster, with all of its genetic tools, forms dead or sterile hybrids when crossed to its sister species, D. simulans, D. sechellia, and D. mauritiana. To circumvent this problem, we used chromosome deletions and duplications from D. melanogaster to map two hybrid incompatibility loci in F(1) hybrids with its sister species. We mapped a recessive factor to the pericentromeric heterochromatin of the X chromosome in D. simulans and D. mauritiana, which we call heterochromatin hybrid lethal (hhl), which causes lethality in F(1) hybrid females with D. melanogaster. As F(1) hybrid males hemizygous for a D. mauritiana (or D. simulans) X chromosome are viable, the lethality of deficiency hybrid females implies that a dominant incompatible partner locus exists on the D. melanogaster X. Using small segments of the D. melanogaster X chromosome duplicated onto the Y chromosome, we mapped a dominant factor that causes hybrid lethality to a small 24-gene region of the D. melanogaster X. We provide evidence suggesting that it interacts with hhl(mau). The location of hhl is consistent with the emerging theme that hybrid incompatibilities in Drosophila involve heterochromatic regions and factors that interact with the heterochromatin.     

Patterns of Microsatellite Variability in the Drosophila Melanogaster Complex

Forty-seven microsatellite loci were amplified in Drosophila melanogaster, Drosophila simulans, Drosophila mauritiana and Drosophila sechellia. The two cosmopolitan species D. melanogaster and D. simulans were found to be the most variable ones, followed by D. mauritiana and D. sechellia. A model based clustering algorithm was applied to the population samples of D. melanogaster, D. simulans and D. sechellia. No evidence for population substructure was detected within species--most likely due to insufficient power. A Markov chain Monte Carlo method developed for demographic inference based on microsatellites provided unambiguous evidence for population contraction in D. melanogaster, D. simulans and D. sechellia, despite that the D. melanogaster and D. simulans population samples were of non-African origin and represented recently expanded populations.     

Nup96-dependent hybrid lethality occurs in a subset of species from the simulans clade of Drosophila

The cross of Drosophila melanogaster females to D. simulans males typically produces lethal F(1) hybrid males. F(1) male lethality is suppressed when the D. simulans Lhr(1) hybrid rescue strain is used. Viability of these F(1) males carrying Lhr(1) is in turn substantially reduced when the hybrids are heterozygous for some mutant alleles of the D. melanogaster Nup96 gene. I show here that similar patterns of Nup96-dependent lethality occur when other hybrid rescue mutations are used to create F(1) males, demonstrating that Nup96 does not reduce hybrid viability by suppressing the Lhr(1) rescue effect. The penetrance of this Nup96-dependent lethality does not correlate with the penetrance of the F(1) hybrid rescue, arguing that these two phenomena reflect genetically independent processes. D. simulans, together with two additional sister species, forms a clade that speciated after the divergence of their common ancestor from D. melanogaster. I report here that Nup96(-) reduces F(1) viability in D. melanogaster hybrids with one of these sister species, D. sechellia, but not with the other, D. mauritiana. These results suggest that Nup96-dependent lethality evolved after the speciation of D. melanogaster from the common ancestor of the simulans clade and is caused by an interaction among Nup96, unknown gene(s) on the D. melanogaster X chromosome, and unknown autosomal gene(s), at least some of which have diverged in D. simulans and D. sechellia but not in D. mauritiana. The genetic properties of Nup96 are also discussed relative to other hybrid lethal genes.     

Transposable Element Dynamics in Two Sibling Species: Drosophila Melanogaster and Drosophila Simulans

Transposable elements (TEs) in the two sibling species, Drosophila melanogaster and D. simulans, differ considerably in amount and dynamics, with D. simulans having a smaller amount of TEs than D. melanogaster. Several hypotheses have been proposed to explain these differences, based on the evolutionary history of the two species, and claim differences either in the effective size of the population or in genome characteristics. Recent data suggest, however, that the higher amount of TEs in D. melanogaster could be associated with the worldwide invasion of D. melanogaster a long time ago while D. simulans is still under the process of such geographical spread. Stresses due to new environmental conditions and crosses between migrating populations could explain the mobilization of TEs while the flies colonize. Colonization and TE mobilization may be strong evolutionary forces that have shaped and are still shaping the eukaryote genomes.