Population and behaviour genetics of Drosophila ananassae

Drosophila ananassae is a cosmopolitan and domestic species. It occupies a nuique status among the Drosophila species due to certain peculiarities in its genetic behaviour. The most unusual feature of this species is spontaneous male recombination in appreciable frequency. The present review summarises the work done on population and behaviour genetics of D. ananassae from India. Population dynamics of three cosmopolitan inversions has been studied in Indian population of D. ananassae and it is evident from the results that there is a considerable degree of genetic divergence at the level of inversion polymorphism. In general, the populations from south India show more differentiation than those from the north. These three cosmopolitan inversions, which are coextensive with the species, exhibit heterosis. Interracial hybridization does not lead to beaakdown of heterosis, which suggests that evidence for coadaptation is lacking in geographic populations of D. ananassae. Heterosis appears to be simple luxuriance rather than populational heterosis (coadaptation). Unlinked inversions occur in random associations, indicating no interchromosomal interactions. However, two inversions of the third chromosome often show strong linkage disequilibrium in laboratory populations, which is due to epistatic gene interaction and suppression of crossing-over. Genetic variations for certain allozyme polymorphism and sternoleural bristle phenotypes in Indian populations of D. ananassae have also been observed.A number of investigations have also been carried out on certain aspects of behaviour genetics of Indian D. ananassae. There is evidence for sexual isolation within D. ananassae. Significant variations in mating propensity of several isofemale strains, inversion karyotypes, the diminishing effects of certain mutations on sexual activity of males and positive response to selection for high and low mating propensity provide evidence for genetic control of sexual behaviour in D. ananassae. Males contribute more to variation and thus are more subject to intra-sexual selection than females. Evidence for rare male mating advantage has also been presented. Geographic strains of D. ananassae show variation with respect to oviposition site preference. The results of studies on pupation site preference, which is an important component of larval behaviour, suggest that larval pupation behaviour in D. ananassae is under polygenic control with a substantial amount of additive genetic variation.     

Female remating inDrosophila ananassae: shorter duration of copulation during second mating as compared to first mating

Drosophila ananassae, a cosmopolitan and domestic species, belongs to theananassae subgroup of themelanogaster species group. Female remating was observed in ten mass culture stocks of this species, which were initiated from flies collected from different geographic localities. The frequency of female remating ranges from 24% to 56% in different strains. Strains show significant variation in remating latency (days). Significant variation has also been found in all the stocks for duration of copulation between first and second matings. The duration of copulation is shorter in second mating as compared to first mating inD. ananassae.     

Female Remating in Drosophila ananassae: Evidence for the Effect of Density on Female Remating Frequency

Drosophila ananassae, a cosmopolitan and domestic species, is largely circumtropical in distribution and belongs to the ananassae species complex of the ananassae subgroup of the melanogaster species group. In the present study, experiments were conducted to investigate the effect of density on female remating frequency by employing different wild-type and mutant strains of D. ananassae. Two experimental designs, i.e., 2-h daily observation and continuous confinement, were used. The results show that there is significant dependence of remating frequency on density in all strains tested under both experimental designs except in a wild-type strain (Bhutan), which shows no dependence of remating frequency on density under 2-h daily observation design. This finding provides evidence that density may increase the frequency of female remating in D. ananassae.     

Molecular and histological characterizations of the Om(2D) mutants in Drosophila ananassae.

A series of transposon-induced optic morphology (Om) mutants found in a hypermutable marker stock of Drosophila ananassae provides a useful system for analyzing the molecular mechanism of eye morphogenesis. In the present study, one of the 25 Om loci so far reported, Om(2D), has been subjected to histological and molecular analyses as a first step toward understanding the role of Om genes in eye morphogenesis. Histological abnormalities observed during eye morphogenesis of the mutant, i.e. cell death within the eye-antennal discs of third instar larvae, and loss of the lamina, disorganized ommatidia and atrophied optic lobes in adults, were all comparable to those reported with various eye morphology mutants of D. melanogaster. Approximately 25 kb of genomic DNA including the Om (2D) locus was cloned by tom tagging. Southern blot and cloning analyses of two alleles of the Om (2D) locus revealed that insertions of the tom element occurred at three sites within 359 bp; two tandemly arrayed toms sharing one long terminal repeat at the junction and an internally deleted tom were present 359 bp apart from each other in Om (2D) 63, while a single tom in reverse orientation was present within the 359 bp in Om (2D) 10a. Host DNA sequences at the three insertion sites were TATAT or AATAT, and ATAT was duplicated upon the tom insertion.(ABSTRACT TRUNCATED AT 250 WORDS)     

Genetic analysis of female mating recognition between Drosophila ananassae and Drosophila pallidosa: application of interspecific mosaic genome lines

Drosophila ananassae and Drosophila pallidosa are closely related species that can produce viable and fertile hybrids of both sexes, although strong sexual isolation exists between the two species. Females are thought to discriminate conspecific from heterospecific males based on their courtship songs. The genetic basis of female discrimination behavior was analyzed using isogenic females from interspecific mosaic genome lines that carry homozygous recombinant chromosomes. Multiple regression analysis indicated a highly significant effect of the left arm of chromosome 2 (2L) on the willingness of females to mate with D. ananassae males. Not only 2L but also the left arm of chromosome X (XL) and the right arm of chromosome 3 (3R) had significant effects on the females' willingness to mate with D. pallidosa males. All regions with strong effects on mate choice have chromosome arrangements characterized by species-specific inversions. Heterospecific combinations of 2L and 3R have previously been suggested to cause postzygotic reproductive isolation. Thus, genes involved in premating as well as postmating isolation are located in or near chromosomal inversions. This conclusion is consistent with the recently proposed hypothesis that "speciation genes" accumulate at a higher rate in non-recombining genome regions when species divergence occurs in the presence of gene flow.     

Genetics of sexual isolation based on courtship song between two sympatric species: Drosophila ananassae and D. pallidosa

Sexual isolation has been considered one of the primary causes of speciation and its genetic study has the potential to reveal the genetics of speciation. In Drosophila, the importance of courtship songs in sexual isolation between closely related species has been well investigated, but studies analysing the genetic basis of the difference in the courtship songs associated with sexual isolation are less well documented. Drosophila ananassae and Drosophila pallidosa are useful for studies of sexual isolation, because of their sympatric distribution and absence of postmating isolation. Courtship songs are known to play a crucial role in sexual isolation between these two species, and the female discrimination behaviour against the courting male has been revealed to be controlled by a very narrow region on the second chromosome. In this study we investigated the genetic basis controlling the song differences associated with their sexual isolation, using intact and wingless males with chromosomes substituted between species. The results obtained from F₁ hybrid males between these species indicate the dominance of the song characters favoured by D. pallidosa females. In addition, the results obtained from backcross F₂ males indicate that chromosome 2 had a major effect on the control of the song characters associated with sexual isolation.     

Heterosis without selectional coadaptation inDrosophila ananassae

Summary The relative viabilities of homozygous and heterozygous karyotypes were measured by making crosses between strains ofD. ananassae homozygous for ST or inverted gene orders in the second and third chromosomes. The strains utilized during the present study originated from widely separated localities in India, Kuala Lumpur and Kota Kinabaru, Malaysia and Chian Mai, Thailand. The presence of heterosis in many interpopulation crosses is evident from the results which show that the inversion heterozygotes formed by chromosomes coming from distant populations exhibit heterosis. On the other hand, heterosis is absent in two intrapopulation crosses. Thus the present results provide evidence that heterozygosis for many genes and gene complexes does produce high fitness without previous selectional coadaptation.     

Extensive duplication of the Wolbachia DNA in chromosome four of Drosophila ananassae

Background

Lateral gene transfer (LGT) from bacterial Wolbachia endosymbionts has been detected in ~20% of arthropod and nematode genome sequencing projects. Many of these transfers are large and contain a substantial part of the Wolbachia genome.

Results

Here, we re-sequenced three D. ananassae genomes from Asia and the Pacific that contain large LGTs from Wolbachia. We find that multiple copies of the Wolbachia genome are transferred to the Drosophila nuclear genome in all three lines. In the D. ananassae line from Indonesia, the copies of Wolbachia DNA in the nuclear genome are nearly identical in size and sequence yielding an even coverage of mapped reads over the Wolbachia genome. In contrast, the D. ananassae lines from Hawaii and India show an uneven coverage of mapped reads over the Wolbachia genome suggesting that different parts of these LGTs are present in different copy numbers. In the Hawaii line, we find that this LGT is underrepresented in third instar larvae indicative of being heterochromatic. Fluorescence in situ hybridization of mitotic chromosomes confirms that the LGT in the Hawaii line is heterochromatic and represents ~20% of the sequence on chromosome 4 (dot chromosome, Muller element F).

Conclusions

This collection of related lines contain large lateral gene transfers composed of multiple Wolbachia genomes that constitute >2% of the D. ananassae genome (~5 Mbp) and partially explain the abnormally large size of chromosome 4 in D. ananassae.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-1097) contains supplementary material, which is available to authorized users.     

Relationship between chromosomal polymorphism and wing size in a natural population of Drosophila subobscura

Chromosomal polymorphism and wing size (as a measure of body size) were analysed simultaneously in two samples of Drosophila subobscura from Barcelona, Spain. The very rich chromosomal polymorphism of this species makes it difficult to detect the relationship of this polymorphism with any phenotypical character. However, a positive significant regression of wing size on the percentage of the autosome length with standard arrangement was found. Furthermore, for each polymorphic chromosome, except for the J chromosome, an association between the most frequent arrangements and wing size was observed. This trend, which was the same in the two samples, was that expected according to the latitudinal clines of both characters.     

Rapid evolution of wing size clines in Drosophila subobscura

Parallel latitudinal clines across species and continents provide dramatic evidence of the efficacy of natural selection, however little is known about the dynamics involved in cline formation. For example, several drosophilids and other ectotherms increase in body and wing size at higher latitudes. Here we compare evolution in an ancestral European and a recently introduced (North America) cline in wing size and shape in Drosophila subobscura. We show that clinal variation in wing size, spanning more than 15 degrees of latitude, has evolved in less than two decades. In females from Europe and North America, the clines are statistically indistinguishable however the cline for North American males is significantly shallower than that for European males. We document that while overall patterns of wing size are similar on two continents, the European cline is obtained largely through changing the proximal portion of the wing, whereas the North American cline is largely in the distal portion. We use data from sites collected in 1986/1988 (Pegueroles et al. 1995) and our 1997 collections to compare synchronic (divergence between contemporary populations that share a common ancestor) and allochronic (changes over time within a population) estimates of the rates of evolution. We find that, for these populations, allochronically estimated evolutionary rates within a single population are over 0.02 haldanes (2800 darwins), a value similar in magnitude to the synchronic estimates from the extremes of the cline. This paper represents an expanded analysis of data partially presented in Huey et al. (2000).     

Behavioral Sequence Leading to Sexual Isolation Between <Emphasis Type="Italic">Drosophila ananassae</Emphasis> and <Emphasis Type="Italic">D. pallidosa</Emphasis>

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.     

Mating speed and the interplay between female and male courtship responses inDrosophila melanogaster (Diptera: Drosophilidae)

The objective of this study was to compare measures of general activity and sexual behavior for various genotypes within a strain of Drosophila melanogaster, which had known differences in mating speed. Three inbred lines of D. melanogaster differed significantly in mating speed when tested in female-choice and in single-pair experiments. Analyses of locomotor activity and sexual activity of females and males revealed no significant differences between the inbred lines. An analysis of the interplay between female and male courtship behaviors enabled the examination of signal-response differences between the inbred lines. The inbred lines with intermediate and slow mean mating speed showed a decreased number of significant transitions between female and male behavioral responses. This decrease was more severe in the slow mating line. Further, the intermediate- and slow-mating females and males displayed courtship responses toward signals of the opposite sex that were different from those of the fastmating line. Models of the relationship between behavioral activity and mating speed in Drosophila are discussed and a different explanation for variation in mating speed among the three inbred lines is considered.     

Quantification of Locomotion and the Effect of Food Deprivation on Locomotor Activity in Drosophila

A new method to quantify locomotor behavior in Drosophila is presented, and compared with previous methods. It is based upon a radar wave, reflected by moving flies. A problem associated with the new apparatus is that its output is dependent on fly size. However, for the case the weight of the experimental flies has been determined, a correction is proposed. The method has been used by studying the effect of starvation upon locomotion in Drosophila melanogaster. It was found that starved flies are much more active than well fed flies. The importance of this effect under several conditions is discussed.     

Sexual conflict does not drive reproductive isolation in experimental populations of Drosophila pseudoobscura

Sexual conflict has been predicted to drive reproductive isolation by generating arbitrary but rapid coevolutionary changes in reproductive traits among allopatric populations. A testable prediction of this proposal is that allopatric populations experiencing different levels of sexual conflict should exhibit different levels of reproductive isolation. We tested this prediction using experimentally evolved populations of the promiscuous Drosophila pseudoobscura. We manipulated sexual conflict by enforcing either monogamy, maintaining natural levels of promiscuity, or elevating promiscuity. Within each treatment, we carried out sympatric and allopatric crosses using replicated populations and examined pre-zygotic (number of mating pairs, mating speed and copulation duration) and post-zygotic (hybrid inviability and sterility) indicators of reproductive isolation. After 50 generations of selection, none of the measures conformed to predictions of sexual conflict driving reproductive isolation. Our results cannot be explained by lack of genetic variation or weak selection and suggest that sexual conflict may not be a widespread engine of speciation.     

Effect of directional selection for body size on fluctuating asymmetry in certain morphological traits in <Emphasis Type="Italic">Drosophila ananassae</Emphasis>

Variation in the subtle differences between the right and left sides of bilateral characters or fluctuating asymmetry (FA) has been considered as an indicator of an organism’s ability to cope with genetic and environmental stresses during development. However, due to inconsistency in the results of empirical studies, the relationship between FA and stress has been the subject of intense debate. In this study, we investigated whether stress caused by artificial bidirectional selection for body size has any effect on the levels of FA of different morphological traits in Drosophila ananassae. The realised heritability (h²) was higher in low-line females and high-line males, which suggests an asymmetrical response to selection for body size. Further, the levels of FA were compared across 10 generations of selection in different selection lines in both sexes for sternopleural bristle number, wing length, wing-to-thorax ratio, sex comb-tooth number and ovariole number. The levels of FA differed significantly among generations and selection lines but did not change markedly with directional selection. However, the levels of FA were higher in the G10 generation (at the end of selection) than G0 (at the start of selection) but lower than the G5 generation in different selection lines, suggesting that the levels of FA are not affected by the inbreeding generated during the course of selection. Also, the levels of FA in the hybrids of high and low lines were significantly lower than the parental selection lines, suggesting that FA is influenced by hybridisation. These results are discussed in the framework of the literature available on FA and its relationship with stress.     

Analysis of inbreeding in a colonizing population of Drosophila subobscura

An analysis of the effects of inbreeding on the genetic structure of a colonizing population of Drosophila subobscura has been carried out. Species of Drosophila, particularly D. subobscura, may have lethal alleles associated with chromosomal inversions and our aim was to assess the extent to which the genome is balanced in this way. The frequencies of chromosomal inversions were compared between a large population and a set of 72 lines that were maintained by brother-sister mating for 10 generations. Fisher's matrix method was used to calculate the expected homozygosity in these inbred lines for 5 allozyme loci (Aph, Hk-1, Lap, Odh, and Pept-1) used as markers of large chromosomal segments. Furthermore, the expected rates of fixation corresponding to these allozyme loci were also calculated. The results show that the amount of homozygosis observed did not differ significantly from expectations (with the corresponding loss of lines as a consequence of the reduction in viability). However, two deviations from strict neutrality were observed: there was a heterozygote excess at the Lap locus, and the frequency of the O ₅ inversion (always associated with a lethal gene in colonizing populations) was higher than expected.     

Sexual isolation between Drosophila melanogaster females and D. simulans males: sexual maturation of males

Isofemale lines of D. simulans were examined to determine the age of sexual maturity of males with conspecific females, and for the frequency of hybridization with D. melanogaster females. Males started to mature sexually on the first day after eclosion but their ability to mate slowly increased during the following day. The estimates of both the age sexual maturation started and the switch from immature to mature males were strongly dependent on the female genotypes used in the tests. No clear differences in speed of maturation were apparent between male lines. In contrast, differences in frequency of hybridization with D. melanogaster females did occur. From the above results it is concluded that the differential hybridization success of male D. simulans lines is not related to the speed at which males mature sexually.

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Résumé Des lignées isofemelles de D. simulans ont été examinées pour déterminer l'âge de la maturité sexuelle des mâles avec des femelles conspécifiques et pour établir la fréquence de l'hybridation avec des femelles de D. melanogaster. Les mâles ont commencé à être sexuellement mûrs le premier jour après l'émergence, mais leur aptitude à la copulation a augmenté lentement pendant le jour suivant. Les estimations, tant de l'âge du début de la maturation sexuelle que de l'âge du passage de mâle immature à mâle sexuellement mûr dépendaient étroitement des génotypes des femelles utilisées dans les expériences. Il n'y avait pas de différences nettes entre les lignées de mâles. Par contre, des différences dans les fréquences d'hybridation avec les femelles de D. melanogaster ont été observées. De ces résultats, on peut conclure que les différences dans la réussite des hybridations des lignées de mâles de D. simulans n'étaient pas dues à la vitesse de maturation sexuelle des mâles.

     

Sexual Selection of Zorion guttigerum Westwood (Coleoptera: Cerambycidae: Cerambycinae) in Relation to Body Size and Color

Zorion guttigerum is a flower-visiting longhorned beetle endemic to New Zealand. Sexual selection of this species in relation to the body size and color form of different sexes was investigated in the field. The population sex ratio, based on censuses of feeding and mating sites (flowers), is male-biased. Females are significantly larger than males. Both sexes have antennae of similar length but the antennal length relative to the elytral length is greater in males than in females, and the antennal length of males increases more with an increase in body size than that of females. Both sexes have dark blue (DB) and yellowish-brown (YB) individuals. Both pair-bonded and solitary males are similar in elytral and antennal length. In pair-bonded males, DB individuals are significantly more numerous than YB ones, but in solitary males, the number of both color forms is similar. Males tend to have territory protection behavior, fighting with and chasing away rival males from feeding and mating sites. Larger males usually win the fight but the size-dependent fighting advantage does not translate into mating success. Male color plays an important role in mating success, with DB males having a significantly better chance to mate than YB males. Furthermore, male body size and color also have interactions in mating success: males of DB color morph obtain a greater mating advantage according to body size. Pair-bonded females are significantly larger and have longer antennae than solitary females, suggesting that males prefer larger females for mating. In addition, females of DB color morph with longer antennae are also preferred by males for mating. The significance of these findings is discussed.     

Sexual Isolation Between Drosophila Melanogaster, D. Simulans and D. Mauritiana: Sex and Species Specific Discrimination

The sexual isolation among the related species Drosophila melanogaster, D. simulans and D. mauritiana is asymmetrical. While D. mauritiana males mate well with both D. melanogaster and D. simulans females, females of D. mauritiana discriminate strongly against males of these two species. Similarly, D. simulans males mate with D. melanogaster females but the reciprocal cross is difficult. Interspecific crosses between several populations of the three species were performed to determine if (i) males and females of the same species share a common sexual isolation genetic system, and (ii) males (or females) use the same genetic system to discriminate against females (or males) of the other two species. Results indicate that although differences in male and female isolation depend on the populations tested, the isolation behaviour between a pair of species is highly correlated despite the variations. However, the rank order of the isolation level along the populations was not correlated in both sexes, which suggests that different genes act in male and female sexual isolation. Neither for males nor for females, the isolation behaviour of one species was paralleled in the other two species, which indicates that the genetic systems involved in this trait are species-pair specific. The implications of these results are discussed. This revised version was published online in August 2006 with corrections to the Cover Date.