Geographic variation in reproductive success of the parasitoid Asobara tabida in larvae of several Drosophila species

Abstract.

• 1 Asobara tabida is a parasitoid of Drosophila larvae in fermenting substrates. Because it is a widespread species, it may encounter different biotic and abiotic circumstances in various parts of its range.
• 2 The species composition of the host population varies over the parasitoid's range: D.obscura-group species (especially D.subobscura) are the main hosts for northwestern and central European parasitoids; D.melanogaster is the main host for southern European parasitoids.
• 3 D.melanogaster larvae can defend themselves against A.tabida by encapsulating the parasitoid egg, and survival in D.melanogaster is always lower than in D.subobscura.
• 4 Parasitoids from southern European populations are much better able to survive in D.melanogaster than their northwestern and central European conspecifics; parasitoids from different populations are equally well able to survive in D.subobscura.
• 5 The lower survival in D.melanogaster may be partly compensated for by the larger size of parasitoids emerging from this host species compared to parasitoids emerging from D.subobscura.
• 6 Within population groups, larger A.tabida females have more eggs in their ovarioles. Additionally, southern European females have more eggs and less fat than northern and western/central European females. The relationship between size and longevity is ambiguous.
• 7 It is concluded that parasitoids from different populations are adapted to region-specific circumstances.

     

Physiological consequences of immune response by Drosophila melanogaster (Diptera: Drosophilidae) against the parasitoid Asobara tabida (Hymenoptera: Braconidae)

Abstract Parasites can exert a wide range of negative effects on their hosts. Consequently, hosts that can resist infection should have a selective advantage over nonresistant conspecifics. Yet, host populations remain susceptible to some parasites. Could genetic heterogeneity in the host's ability to resist parasites reflect costs of mounting an immune response? Previous work on Drosophila melanogaster establishes that maintaining the ability to mount an immune response decreases larval competitive ability. Moreover, mounting an immune response decreases fitness. I report on the impact of mounting an immune response on fitness of D. melanogaster survived parasitism by Asobara tabida. I used isofemale lines to determine whether genotype influences the costs of immune response. I examined fitness consequences both to larvae and adults. Survivors of parasitism show no measurable decrease in larval fitness (development time) but have decreased adult fitness (population growth rates), probably because of their smaller size.     

Host preference and survival in selected lines of a Drosophila parasitoid,Asobara tabida

Host selection behaviour of parasitoids has important fitness consequences, if hosts of different quality are available. Here the host selection behaviour, the ability to distinguish between hosts differing in their suitability, of the Drosophila parasitizing wasp Asobara tabida was studied. Females from five lines selected for higher survival in the encapsulating host species D. melanogaster ( 16 ) were compared with females from control lines. Females from all five selected lines more readily accepted the encapsulating host species for oviposition when offered together with a nonencapsulating host species than females from the control lines. We found no evidence for pleiotropic effects and suggest that host selection behaviour evolved parallel to the ability to escape encapsulation in the hosts. Our results also suggest that given the appropriate selection pressures, host selection behaviour can quickly evolve in parasitoids, enabling them to adapt fast to changing circumstances.     

Evolutionary relationships to parasitism by seven species of the Drosophila melanogaster subgroup

Parasitic wasps are an important component of the niche of Drosophila species. The susceptibility to the Cynipid Leptopilina boulardi was estimated in the seven sibling species of Drosophila belonging to the melanogaster subgroup. Three categories of Hies can be distinguished, according to the level of cellular immune reaction and success of parasitism. Drosophila melanogaster and D. mauritiana belong to the category 1, specified by no encapsulative reaction and a high rate of successful parasitism. Category 2, characterized by a moderate encapsulation rate and a high mortality include D. simulans.5, D. erecta and D. orena . Category 3, with D. yakuba and D. tcissien , is specified by a very low rate or absence of successful parasitism due to a highly efficient immune cellular reaction. This classification parallels the phylogenic relationship based upon polytene chromosome banding sequences. Such specific ditferences in susceptibility to parasites may plan an important role in the competition between these species in Africa.     

Evolutionary relationships to parasitism by seven species of the Drosophila melanogaster subgroup

Parasitic wasps are an important component of the niche of Drosophila species. The susceptibility to the Cynipid Leptopilina boulardi was estimated in the seven sibling species of Drosophila belonging to the melanogaster subgroup. Three categories of Hies can be distinguished, according to the level of cellular immune reaction and success of parasitism. Drosophila melanogaster and D. mauritiana belong to the category 1, specified by no encapsulative reaction and a high rate of successful parasitism. Category 2, characterized by a moderate encapsulation rate and a high mortality include D. simulans.5, D. erecta and D. orena. Category 3, with D. yakuba and D. tcissien, is specified by a very low rate or absence of successful parasitism due to a highly efficient immune cellular reaction. This classification parallels the phylogenic relationship based upon polytene chromosome banding sequences. Such specific ditferences in susceptibility to parasites may plan an important role in the competition between these species in Africa.     

Effects of parasitism by Asobara tabida (Hymenoptera: Braconidae) on the development,survival and activity of Drosophila melanogaster larvae

The impact of parasitism by Asobara tabida on Drosophila melanogaster larval development, survival features and larval activity has been investigated using two strains of the parasitoid. The successful parasitism rate of the A1 strain was four times greater than that of the WOPV strain. Both strains induced equivalent mortality rates but hosts parasitized by A1 predominantly died as pupae. The time necessary for the host pupariation and emergence, and the larval weight at 72, 96 and 120 h post-parasitization were measured. Parasitized larvae exhibited longer periods of development and lower weights than controls, especially when parasitized by A1. These results suggest that hosts underwent physiological costs varying with respect to the outcome of the parasitic relationship. Of the parasitoid factors possibly responsible for these costs, we examined venoms for their impact on host mortality. Artificial injections of WOPV venoms induced higher mortality rates than did A1 venoms. Venoms were also found responsible for the induction of a transient paralysis, naturally occuring after parasitization. Again, the strongest effect was observed after parasitization by WOPV or injections of its venoms. This study gives new insights into the intriguing features of A. tabida and constitutes the first report of the paralysing properties of the venoms.     

Toxicity of venom of Asobara and Leptopilina species to Drosophila species

The Drosophila parasitoid Asobara japonica Belokobylskij (Hymenoptera: Braconidae) has highly toxic venom that kills host larvae if its injection is not followed by an injection of lateral oviduct components along with egg‐laying. In the present study, the venoms of seven other Drosophila parasitoids (Asobara rossica, Asobara rufescens, Asobara pleuralis, Leptopilina heterotoma, Leptopilina japonica, Leptopilina ryukyuensis, and Leptopilina victoriae) are tested against three kinds of Drosophila species (i.e. Drosophila species that are suitable as host for focal parasitoids, those that are resistant to the parasitoids, and a cosmopolitan species, Drosophila simulans). Venoms of the three Asobara species are not toxic to any of Drosophila species, whereas those of the four Leptopilina species are toxic to some Drosophila species. The toxicity of venom varies among Leptopilina species, and the susceptibility to venom also varies among host Drosophila species. Furthermore, toxicity and paralytic effects of venom are not correlated. Because the toxicity of venom is not adaptive for parasitoids, it may be an inevitable side effect of some components that play an essential role in parasitism.     

Evolution of the LINE-like I element in the Drosophila melanogaster species subgroup

LINE-like retrotransposons, the so-called I elements, control the system of I-R (inducer-reactive) hybrid dysgenesis in Drosophila melanogaster. I elements are present in many Drosophila species. It has been suggested that active, complete I elements, located at different sites on the chromosomes, invaded natural populations of D. melanogaster recently (1920–1970). But old strains lacking active I elements have only defective I elements located in the chromocenter. We have cloned I elements from D. melanogaster and the melanogaster subgroup. In D. melanogaster, the nucleotide sequences of chromocentral I elements differed from those on chromosome arms by as much as 7%. All the I elements of D. mauritiana and D. sechellia are more closely related to the chromosomal I elements of D. melanogaster than to the chromocentral I elements in any species. No sequence difference was observed in the surveyed region between two chromosomal I elements isolated from D. melanogaster and one from D. simulans. These findings strongly support the idea that the defective chromocentral I elements of D. melanogaster originated before the species diverged and the chromosomal I elements were eliminated. The chromosomal I elements reinvaded natural populations of D. melanogaster recently, and were possibly introduced from D. simulans by horizontal transmission.     

Light wavelength dependency of mating activity in the Drosophila melanogaster species subgroup

The action spectra of mating activity among the six species of the Drosophila melanogaster species subgroup were compared to understand how light wavelength affects mating activity. The species fell into three groups with respect to the action spectrum of mating activity. We chose one representative species from each of the three types for detailed study: D. melanogaster, D. sechellia and D. yakuba. The mating activities were investigated under three different light intensities of three monochromatic lights stimulus. Each species showed a unique spectral and intensity response. To know the evolutionary meaning of the light wavelength dependency of mating activity, we superimposed the type of action spectrum of mating activity in these six species on a cladogram. Mating inhibition under UV was conserved in evolution among these species. Furthermore we clarified that D. melanogaster showed low mating activity under UV because males courted less under UV.     

Evolution of eye morphology and rhodopsin expression in the Drosophila melanogaster species subgroup

A striking diversity of compound eye size and shape has evolved among insects. The number of ommatidia and their size are major determinants of the visual sensitivity and acuity of the compound eye. Each ommatidium is composed of eight photoreceptor cells that facilitate the discrimination of different colours via the expression of various light sensitive Rhodopsin proteins. It follows that variation in eye size, shape, and opsin composition is likely to directly influence vision. We analyzed variation in these three traits in D. melanogaster, D. simulans and D. mauritiana. We show that D. mauritiana generally has larger eyes than its sibling species, which is due to a combination of larger ommatidia and more ommatidia. In addition, intra- and inter-specific differences in eye size among D. simulans and D. melanogaster strains are mainly caused by variation in ommatidia number. By applying a geometric morphometrics approach to assess whether the formation of larger eyes influences other parts of the head capsule, we found that an increase in eye size is associated with a reduction in the adjacent face cuticle. Our shape analysis also demonstrates that D. mauritiana eyes are specifically enlarged in the dorsal region. Intriguingly, this dorsal enlargement is associated with enhanced expression of rhodopsin 3 in D. mauritiana. In summary, our data suggests that the morphology and functional properties of the compound eyes vary considerably within and among these closely related Drosophila species and may be part of coordinated morphological changes affecting the head capsule.     

Divergence and heterogeneity of the histone gene repeating units in the Drosophila melanogaster species subgroup

The repeating units of the histone gene cluster containing the H1, H2A, H2B and H4 genes were amplified by PCR from the Drosophila melanogaster species subgroup, i.e., D. yakuba, D. erecta, D. sechellia, D. mauritiana, D. teissieri and D. orena. The PCR products were cloned and their nucleotide sequences of about 4.6-4.8kbp were determined to elucidate the mechanism of molecular evolution of the histone gene family. The heterogeneity among the histone gene repeating units was 0.6% and 0.7% for D. yakuba and D. sechellia, respectively, indicating the same level of heterogeneity as in the H3 gene region of D. melanogaster. Divergence of the genes among species even in the most closely related ones was much greater than the heterogeneity among family members, indicating a concerted mode of evolution for the histone gene repeating units. Among the species in the D. melanogaster species subgroup, the histone gene regions as well as 3rd codon position of the coding region showed nearly the same GC contents. These results suggested that the previous conclusion on analysis of the H3 gene regions, the gene family evolution in a concerted fashion, holds true for the whole histone gene repeating unit.     

Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora)

The polytene chromosomes of two new species of Drosophila, D. sechellia and D. orena, both members of the melanogaster species subgroup, are described. The chromosomes of D. sechellia, a species endemic to certain islands in the Seychelles, are homosequential with those of D. simulans and D. mauritiana. The chromosomes of D. orena, a species from the mountains of west Africa, are very similar to those of D. erecta. We discuss the interrelationships of the eight known species of the melanogaster species subgroup, based upon an analysis of their chromosome banding patterns.     

Molecular evolution of the histone 3 multigene family in the Drosophila melanogaster species subgroup

Molecular evolution of the histone multigene family was studied by cloning and sequencing regions of the histone 3 gene in the Drosophila melanogaster species subgroup. Analysis of the nucleotide substitution pattern showed that in the coding region synonymous changes occurred more frequently to A or T in contrast to the GC-rich base composition, while in the 3' region the nucleotide substitutions were most likely in equilibrium. These results suggested that the base composition at the third codon position of the H3 gene, i.e., codon usage, has been changing to A or T in the Drosophila melanogaster species subgroup.     

The distribution of satellite and main-band DNA components in the melanogaster species subgroup of Drosophila

Fractionation of total adult DNA of five of the seven species of the melanogaster species sub-group of Drosophila in actinomycin D and distamycin A caesium density gradients has revealed the presence of three main-band DNA components, common to all species, and ten satellite DNAs that are distributed between the species. Satellite DNAs are either unique to a species or common to two or more species. The abundance of a common satellite DNA varies between species. There is no simple relationship between the presence of a satellite DNA and a branch point of phylogenetic divergence; nevertheless the arrangement of the species in a phylogeny that is based on the numbers of satellites held in common accurately reflects the pattern of relationships between the same species based on differences in inversions of polytene chromosomes. The species can be similarly arranged according to the compositions of their mitochondrial DNAs. It is possible that the same basic set of sequences, each of low frequency, is common to all species with arbitrary or selected amplification of particular sequences to differing extents in individual species. The conservation of satellites in the group and the close parallel between the distributions of satellites and inversions between the species suggests that either the processes that operate to change both chromosomal phenomena are similarly time-dependent and occurring at relatively low rates or that their rates of change are restricted according to some undetermined functions of these aspects of the genome.