Masatoshi Tomaru

A locus for female discrimination behavior causing sexual isolation in Drosophila

The genetic basis of sexual isolation that contributes to speciation is one of the unsolved questions in evolutionary biology. Drosophila ananassae and Drosophila pallidosa are closely related, and postmating isolation has not developed between them. However, females of both species discriminate their mating partners, and this discrimination contributes to strong sexual isolation between them. By using surgical treatments, we demonstrate that male courtship songs play a dominant role in female mate discrimination. The absence of the song of D. pallidosa dramatically increased interspecies mating with D. ananassae females but reduced intraspecies mating with D. pallidosa females. Furthermore, genetic analysis and chromosomal introgression by repeated backcrosses to D. pallidosa males identified possible loci that control female discrimination in each species. These loci were mapped on distinct positions near the Delta locus on the middle of the left arm of the second chromosome. Because the mate discrimination we studied is well developed and is the only known mechanism that prevents gene flow between them, these loci may have played crucial roles in the evolution of reproductive isolation, and therefore, in the speciation process between these two species.

Heterospecific inter-pulse intervals of courtship song elicit female rejection in Drosophila biauraria

Abstract The present study investigated the significance of song in sexual isolation in Drosophila biauraria . Interspecific copulation was not observed with a heterospecific D. triauraria male that had intact wings, although it was often observed when the males wings were removed, indicating that heterospecific courtship song elicits female rejection, and prevents copulation. Artificially synthesized songs were played to a female with a wingless, antennaless male. The conspecific inter-pulse interval of artificial song increased mating frequency, whereas the heterospecific, longer or shorter, inter-pulse interval significantly decreased the frequency. The mating frequency with random noise and silence showed intermediate values. Female rejection behaviour was greater with heterospecific than with conspecific inter-pulse intervals of artificial song; with random song and silence female responses were intermediate. This indicates that the inter-pulse interval is used as a species discriminator in D. biauraria females. It is suggested that the females ability to discriminate inter-pulse intervals and her responses, rejection and acceptance, have evolved under the influence of reinforcement, reproductive character displacement, or both, which triggered sexual selection.

COURTSHIP SONG RECOGNITION IN THE DROSOPHILA MELANOGASTER COMPLEX: HETEROSPECIFIC SONGS MAKE FEMALES RECEPTIVE IN D. MELANOGASTER, BUT NOT IN D. SECHELLIA

Abstract. The courtship song emitted by male wing vibration has been regarded as one of the most important signals in sexual isolation in the species of the Drosophila melanogaster complex. Inter‐ and intraspecific crosses were observed using males whose wings were removed (mute) or females whose aristae were removed (deaf). Females of D. melanogaster, D. simulans, and D. mauritiana mated with heterospecific males in the song‐present condition (cross between normal females and winged males) more often than in the no‐song condition (cross between normal females and wingless males or between aristaless females and winged males) or they showed no preference between the two conditions. It is possible that in these females heterospecific courtship songs play a role as if they were conspecific. In contrast, the females of D. sechellia mated with D. melanogaster or D. simulans males in the no‐song condition more often than in the song‐present condition, suggesting that they reject males with heterospecific song. Female mate recognition depending on the courtship song in D. melanogaster, D. simulans, and D. mauritiana is considered to be relatively broader and that in D. sechellia narrower.

Genetic basis and evolution of species-specific courtship song in the Drosophila auraria complex.

The interpulse interval (IPI) of courtship song in the Drosophila auraria complex is the only parameter that is consistently species-specific among the several courtship elements examined within the complex. The genetic basis of the species-specific courtship song was examined by analysing the song of interspecific hybrids and of backcross progeny. IPI of all interspecific hybrids except two showed intermediate values, suggesting autosomal control of species-specific IPI. However, significant deviation for shorter IPI from midparent was found in thirteen out of 20 crosses. The chromosomal analysis between D. auraria and D. biauraria revealed that the two major autosomes had significantly large effects on IPI, but the sex chromosome and cytoplasm had no effect. Since no interaction was detected, it is concluded that each autosome acts additively in the determination of species-specific IPI. The common ancestors of the D. auraria complex may also have had autosomal control of IPI, which has been conserved during speciation in the complex.

Rice Dwarf Viruses with Dysfunctional Genomes Generated in Plants Are Filtered Out in Vector Insects: Implications for the Origin of the Virus

ABSTRACT Rice dwarf virus (RDV), with 12 double-stranded RNA (dsRNA) genome segments (S1 to S12), replicates in and is transmitted by vector insects. The RDV-plant host-vector insect system allows us to examine the evolution, adaptation, and population genetics of a plant virus. We compared the effects of long-term maintenance of RDV on population structures in its two hosts. The maintenance of RDV in rice plants for several years resulted in gradual accumulation of nonsense mutations in S2 and S10, absence of expression of the encoded proteins, and complete loss of transmissibility. RDV maintained in cultured insect cells for 6 years retained an intact protein-encoding genome. Thus, the structural P2 protein encoded by S2 and the nonstructural Pns10 protein encoded by S10 of RDV are subject to different selective pressures in the two hosts, and mutations accumulating in the host plant are detrimental in vector insects. However, one round of propagation in insect cells or individuals purged the populations of RDV that had accumulated deleterious mutations in host plants, with exclusive survival of fully competent RDV. Our results suggest that during the course of evolution, an ancestral form of RDV, of insect virus origin, might have acquired the ability to replicate in a host plant, given its reproducible mutations in the host plant that abolish vector transmissibility and viability in nature.

Biology of reproductive isolation in Drosophila: toward a better understanding of speciation

Abstract Mechanisms of premating and postmating isolation between Drosophila melanogaster and its sibling species, D. simulans, D. mauritiana, and D. sechellia, are reviewed here. As D. melanogaster has been used as a “model organism” in a variety of studies, we can apply much knowledge about this species to interspecific hybridizations. Mating success between species is low because of species specificity of pheromonal and acoustic signals and the receivers, although other factors are also involved. On the other hand, genetic incompatibility between species results in inviability and sterility in F1 and backcross hybrids. Studies of reproductive isolation between these Drosophila species will shed light on animal speciation and the origin of biodiversity.

Courtship behavior and sexual isolation between Drosophila auraria and D. triauraria in darkness and light

Sexual isolation between two species of the Drosophila auraria complex, D. auraria and D. triauraria is different in darkness and light. In darkness there is complete isolation while in light it is only partial. The sensory bases of these differences were investigated by behavioral studies in darkness and light. In darkness there was no normal courtship sequence but males of both species displayed attempted copulation to homospecific and heterospecific females, as well as homospecific males. After a few hours together, homospecific copulations were observed after females displayed a characteristic posture: spreading the wings. Such an acceptance posture, also observed in other Drosophila species, was probably released by the wing vibration of a homospecific male. In light, visual signals alone are able to elicit males orientation and following, whether flies are housed together or physically separated. Intense homosexual courtships were observed. All these data suggest that males have a low discrimination ability and females play the main role in sexual isolation.

Genetic analysis of Drosophila virilis sex pheromone: genetic mapping of the locus producing Z-(11)-pentacosene.

Z-(11)-pentacosene, Drosophila virilis sex pheromone, is predominant among the female cuticular hydrocarbons and can elicit male courtship behaviours. To evaluate the genetic basis of its production, interspecific crosses between D. novamexicana and genetically marked D. virilis were made and hydrocarbon profiles of their backcross progeny were analysed. The production of Z-(11)-pentacosene was autosomally controlled and was recessive. Of the six D. virilis chromosomes only the second and the third chromosomes showed significant contributions to sex pheromone production, and acted additively. Analysis of recombinant females indicated that the locus on the second chromosome mapped to the proximity of position 2-218.

Effects of Courtship Song in Interspecific Crosses Among the Species of the Drosophila auraria Complex (Diptera: Drosophilidae)

The courtship behavior and the effects of courtship song in inter- and intraspecific crosses were studied in the four sympatric species of the Drosophila auraria complex: D. auraria, D. biauraria, D. subauraria, and D. triauraria. Orientation, tapping, and vibration (the repertoires of male courtship) were observed in both inter- and intraspecific crosses, suggesting that signals from heterospecific females were enough to elicit such male behaviors. The crossability tests with wingless or winged heterospecific males (tests for wing effects) revealed that winged heterospecific males copulated less than wingless ones in all four species but not all the pairwise cases. Since the crossability tests with aristaless females (deaf) or normal females showed essentially the same results as the tests for wing effects, we concluded that the sound produced by wing vibration plays an important role and that the wing movement itself is less important. These findings suggest that courtship songs are of great importance in mate discrimination and the sexual isolation between the species of this complex.

Behavioral Sequence Leading to Sexual Isolation Between Drosophila ananassae and D. pallidosa

Drosophila ananassae and D. pallidosa are closely related, sympatric species that lack postmating isolation. Sexual isolation has been considered important in maintaining them as independent species. To clarify the behavioral processes leading to sexual isolation, we analyzed behavioral sequences and examined the effect of courtship song on mating success and on behaviors of both sexes by surgically removing male wings (song generators), female aristae (song receivers), or female wings (means of fluttering). We found that heterospecific courtship songs evoked female wing fluttering, whereas conspecific courtship song did not. Furthermore, female wing fluttering made courting males discontinue courtship. These findings suggest that strong sexual isolation is achieved through the following behavioral sequence: heterospecific song→female wing fluttering→courtship discontinuation.