Drosophila Buzzatii Research Articles

Gametic associations between inversion and allozyme polymorphisms in Drosophila buzzatii.

Gametic disequilibria between second chromosome polymorphic arrangements and seven linked allozyme loci were estimated in seven populations of Drosophila buzzatii from Argentina. Significant and consistent associations across populations were detected for Est-1, Est-2, Aldox, and XDH: Phenograms based on Nei's genetic distance showed that chromosomes carrying the 2ST arrangement were more similar to each other, irrespective of the population from which they were extracted, than to chromosomes carrying the derived 2J and 2JZ3. Restriction of recombination in heterokaryotypes seems to be the best explanation for the significant linkage disequilibria between inversions and the loci located inside the rearranged segments, for example, Est-1 and Aldox, or close to the break points, for example, Est-2. However, epistatic interactions between Xdh, which is outside the inversions and not near the break points, and loci tightly linked to the inversions, is the most likely explanation for the association between Xdh and chromosomal arrangements. Some of the associations detected in endemic Argentinean populations are coincident with data obtained in colonizing populations of the Old World and Australia. Thus historical processes that took place in the original area of the species' distribution can account for these linkage disequilibria in colonized populations of D. buzzatii.

Molecular characterization of two natural hotspots in the Drosophila buzzatii genome induced by transposon insertions.

Transposable elements (TEs) have been implicated in the generation of genetic rearrangements, but their potential to mediate changes in the organization and architecture of host genomes could be even greater than previously thought. Here, we describe the naturally occurring structural and nucleotide variation around two TE insertions in the genome of Drosophila buzzatii. The studied regions correspond to the breakpoints of a widespread chromosomal inversion generated by ectopic recombination between oppositely oriented copies of a TE named Galileo. A detailed molecular analysis by Southern hybridization, PCR amplification, and DNA sequencing of 7.1 kb surrounding the inversion breakpoints in 39 D. buzzatii lines revealed an unprecedented degree of restructuring, consisting of 22 insertions of ten previously undescribed TEs, 13 deletions, 1 duplication, and 1 small inversion. All of these alterations occurred exclusively in inverted chromosomes and appear to have accumulated after the insertion of the Galileo elements, within or close to them. The nucleotide variation at the studied regions is six times lower in inverted than in noninverted chromosomes, suggesting that most of the observed changes originated in only 84,000 years. Galileo elements thus seemed to promote the transformation of these, otherwise normal, chromosomal regions in genetically unstable hotspots and highly efficient traps for transposon insertions. The particular features of two new Galileo copies found indicate that this TE belongs to the Foldback family. Together, our results strengthen the importance of TEs, and especially DNA transposons, as inducers of genome plasticity in evolution.

Systematics and Evolution of the <I>Drosophila buzzatii</I> (Diptera: Drosophilidae) Cluster Using mtDNA

Abstract The Drosophila buzzatii Patterson & Wheeler cluster (repleta group) includes seven species: D. buzzatii Patterson & Wheeler, D. koepferae Fontdevila et al. D. serido Vilela & Sene, D. seriema Tidon-Sklorz & Sene, D. borborema Vilela & Sene, D. sp. D and D. sp. B. These flies are widely distributed in South America outside the Amazon region. The systematics of this cluster has been based on chromosomal inversions and the aedeagus is used to identify species. These species use necrotic cactus tissues as breeding sites. The current hypothesis of differentiation and speciation of these species is related to expansion and retraction of cactus distribution in South America during Quaternary climatic cycles. We investigated the phylogenetic relationship among species of this cluster based on the mtDNA COI gene region and compared it with the relationship established using classical markers. The resulting phylogenetic hypothesis indicated that this cluster is a monophyletic group that can be divided into...

Contrasting population genetic structures using allozymes and the inversion polymorphism in Drosophila buzzatii

Abstract Second chromosome inversion and genotypic frequencies at seven allozyme loci, differentially associated with inversions, were determined in seven natural populations of Drosophila buzzatii. The patterns of variation of allozymes and the inversion polymorphisms were significantly different, indicating the role of adaptive differentiation for the latter. Moreover, the patterns of population structure varied among allozyme loci, suggesting the operation of diversifying selection for certain loci. Differentiation was negligible for Leucyl-amino peptidase (Lap) and Peptidase-2 (Pep-2), low to moderate for Aldehyde oxidase (Aldox), Peptidase-1 (Pep-1) and Esterase-1 (Est-1) and high for Esterase-2 (Est-2) and Xanthine dehydrogenase (Xdh). Significant linkage disequilibria were detected between inversions and Aldox, Est-1, Est-2 and Xdh. Multiple regression analyses of inversion and allele frequencies on environmental variables revealed the existence of clines for inversions, Est-1, Est-2, Xdh and Aldox along altitudinal, latitudinal and/or climatic gradients. Tests using conditional allele frequencies showed that Est-1 and Aldox clines could be accounted for by hitchhiking with inversions, whereas natural selection should be invoked to explain the clines observed for Est-2 and Xdh.

Remating, sperm transfer, and sperm displacement in the cactophilic species Drosophila buzzatii Patterson & Wheeler (Diptera: Drosophilidae)

The mating system of Drosophila buzzatii is characterized by short copulation duration, frequent remating in both males and females, and male ejaculate partitioning. Additional features of the system are strong sperm displacement and a high frequency of sterile matings. Remating frequencies and the effects of remating on various mating parameters were studied. In order to characterize variation, five isofemale lines from geographically distant localities in Australia (three localities), Brazil and the Canary Islands were used. Mating parameters studied were: premating time, copulation duration, interval between successive matings, and progeny number as a measure of sperm transfer. Variation for sperm displacement was studied in crosses between laboratory stocks and a number of isofemale lines from Australia. There were significant between-line differences in female remating frequencies, premating time, copulation duration, interval between successive matings, and progeny numbers, indicating genetic variation for these traits. Females from the five lines mated on average 1.6 to 3.1 times in 4 h, with a maximum of eight matings for one female. The males were given a maximum of ten virgin females in sequence and more than one-third of the males mated all ten females in the 2 h observation period. Copulation duration decreased and interval between matings increased with copulation number in multiply mated males. Mean copulation duration was c. 2 min. Sperm transfer, measured as the average number of progeny from a single mating, was low (c. 25) and multiply mated females gave more progeny than single mated females, although with much lower progeny numbers than observed in wild-caught non-virgin females. A surprisingly high proportion of observed matings gave no progeny, i.e. they were sterile matings. Sperm displacement was strong in most crosses and remained strong in multiply mated females. The results are discussed in relation to the evolution of mating patterns in Drosophila.

Remating, sperm transfer, and sperm displacement in the cactophilic species Drosophila buzzatii Patterson & Wheeler (Diptera: Drosophilidae)

The mating system of Drosophila buzzatii is characterized by short copulation duration, frequent remating in both males and females, and male ejaculate partitioning. Additional features of the system are strong sperm displacement and a high frequency of sterile matings. Remating frequencies and the effects of remating on various mating parameters were studied. In order to characterize variation, five isofemale lines from geographically distant localities in Australia (three localities), Brazil and the Canary Islands were used. Mating parameters studied were: premating time, copulation duration, interval between successive matings, and progeny number as a measure of sperm transfer. Variation for sperm displacement was studied in crosses between laboratory stocks and a number of isofemale lines from Australia. There were significant between-line differences in female remating frequencies, premating time, copulation duration, interval between successive matings, and progeny numbers, indicating genetic variation for these traits. Females from the five lines mated on average 1.6 to 3.1 times in 4 h, with a maximum of eight matings for one female. The males were given a maximum of ten virgin females in sequence and more than one-third of the males mated all ten females in the 2 h observation period. Copulation duration decreased and interval between matings increased with copulation number in multiply mated males. Mean copulation duration was c. 2 min. Sperm transfer, measured as the average number of progeny from a single mating, was low (c. 25) and multiply mated females gave more progeny than single mated females, although with much lower progeny numbers than observed in wild-caught non-virgin females. A surprisingly high proportion of observed matings gave no progeny, i.e. they were sterile matings. Sperm displacement was strong in most crosses and remained strong in multiply mated females. The results are discussed in relation to the evolution of mating patterns inDrosophila .

THE ROLE OF THE USE OF DIFFERENT HOST PLANTS IN THE MAINTENANCE OF THE INVERSION POLYMORPHISM IN THE CACTOPHILIC DROSOPHILA BUZZATII

Abstract. Inversion polymorphisms often have been associated with fitness variation. Cactophilic Drosophila buzzatii has been used widely for the study of the maintenance of chromosomal variation. The purpose of this paper is to address the relative importance of variable selection regimes associated with the use of three different host cacti and antagonistic pleiotropy in the maintenance of chromosomal variation. Using homokaryotypic stocks derived from several lines homozygous for four second-chromosome arrangements, we show that inversions significantly affect first-instar larva to adult viability (VT), developmental time (DT) and adult thorax length (TL). We also show that the effects of inversions on DT and VT are dependent on the cactus rearing media. The effects of polymorphic gene arrangements on life-history traits suggest the existence of trade-offs between early and late fitness components. The dosage of arrangement 2st, the ancestral gene order, was negatively correlated with DT and TL, whereas flies carrying the derived arrangements 2j and 2jq7 had longer DTs and larger TLs. Arrangements 2st and 2jq7 increased viability, at least in one of the cactus media tested. Our results suggest that environmental heterogeneity, as represented by the use of different cactus hosts and the trade-off between DT and TL, may be involved in the maintenance of the polymorphism. In addition, our data suggest that the chromosomal phylogeny may be decoupled from the evolution of the genes affecting life-history traits linked to the inversion system.

The role of the use of different host plants in the maintenance of the inversion polymorphism in the cactophilic Drosophila buzzatii.

Inversion polymorphisms often have been associated with fitness variation. Cactophilic Drosophila buzzatii has been used widely for the study of the maintenance of chromosomal variation. The purpose of this paper is to address the relative importance of variable selection regimes associated with the use of three different host cacti and antagonistic pleiotropy in the maintenance of chromosomal variation. Using homokaryotypic stocks derived from several lines homozygous for four second-chromosome arrangements, we show that inversions significantly affect first-instar larva to adult viability (VT), developmental time (DT) and adult thorax length (TL). We also show that the effects of inversions on DT and VT are dependent on the cactus rearing media. The effects of polymorphic gene arrangements on life-history traits suggest the existence of trade-offs between early and late fitness components. The dosage of arrangement 2st, the ancestral gene order, was negatively correlated with DT and TL, whereas flies carrying the derived arrangements 2j and 2jq7 had longer DTs and larger TLs. Arrangements 2st and 2jq7 increased viability, at least in one of the cactus media tested. Our results suggest that environmental heterogeneity, as represented by the use of different cactus hosts and the trade-off between DT and TL, may be involved in the maintenance of the polymorphism. In addition, our data suggest that the chromosomal phylogeny may be decoupled from the evolution of the genes affecting life-history traits linked to the inversion system.

A genetic analysis of the relationship between life-history variation and heat-shock tolerance in Drosophila buzzatii.

Although exposure to environmental stress is common in most populations, and the physiological effects of stress on individuals are well studied, the evolutionary importance of stress to populations is not well understood. To address multitrait responses to environmental change and potential constraints on character evolution, we analysed, in 100 isofemale lines of Drosophila buzzatii, the genetic relationships between resistance to a short heat shock and several life-history traits: survival in benign conditions, larval developmental time, fecundity and longevity. Estimates of heritability of larval thermotolerance were low, but significant, and all life-history traits varied significantly among isofemale lines. Several of these traits covaried significantly. Most correlations indicated positive life-history relationships, but males and females from lines where female fecundity was higher developed more slowly in the absence of stress, which is a negative life-history relationship. The stress reduced or negated many trait associations, and showed one additional relationship; more larvae from lines that developed fast at 25 degrees C survived to adult after stress than did larvae from slow developing lines. These shifts in fitness relationships, when a single stress bout is applied, suggest that even small increases in environmental stress can have profound effects on evolutionary relationships among life-history traits.

The retrotransposon Osvaldo from Drosophila buzzatii displays all structural features of a functional retrovirus.

The Osvaldo retrotransposon has shown a high transposition rate in some strains of Drosophila buzzatii and in hybrids between D. buzzatii and its sibling D. koepferae. In order to understand the molecular basis of this phenomenon, we developed a procedure to clone a recently transposed copy with the aim of characterizing an active, full- length Osvaldo element. The complete nucleotide sequence of Osvaldo, obtained from a recent insertion site, was determined. Osvaldo is 9,045 bp long and is composed of a central coding region flanked by identical long terminal repeats (LTRs) of 1,196 bp each. Sequences homologous to the polypurine tract and tRNA-primer-binding site of retroviruses are located adjacent to the 3' and 5' LTRs, respectively. The internal region of Osvaldo contains three long open reading frames (ORFs 1, 2, and 3), comparable in size and location to gag, pol, and env retroviral genes. The conceptual translation of Osvaldo ORF1 exhibits sequence homology to HIV1 and SIV capsid (p24) and nucleocapsid (p7) mature proteins. ORF2 encodes the putative protease (PR), reverse transcriptase/ribonuclease H (RT/RH), integrase (IN), and a significant portion of the surface envelope (ENV) protein that is interrupted by a putative intron. A third ORF encodes the remaining part of the ENV protein. The predicted 62-kDa ENV protein shares several general features with membrane glycoproteins, including a potential signal peptide, a transmembrane domain near the C-terminus that could function as a membrane anchor, four consensus N-linked glycosylation motifs, and, finally, a potential protease cleavage site. The phylogenetic relationships of Osvaldo are explored, and they suggest that Osvaldo may constitute a new family of retroviruses in insects, distantly related to the previously described group of gypsy retroviruses.

Characterization of a species-specific satellite DNA of Drosophila buzzatii

The pBuM189 satellite DNA family was found to be species specific for Drosophila buzzatii. It consists of slightly AT-rich tandemly arranged repeats with a high copy number in the genome and shows a very high level of intraspecific sequence similarity. pBuM189 repeats cannot be detected in the genomes of closely related species such as Drosophila serido, Drosophila borborema and Drosophila koepferae. The data support the marginal systematic position of D. buzzatii within the buzzatii cluster of the Drosophila repleta group.

INVERSION POLYMORPHISM, LONGEVITY, AND BODY SIZE IN A NATURAL POPULATION OF DROSOPHILA BUZZATII.

In this study we present the results of an analysis of differential longevity associated with Drosophila buzzatii second chromosome inversion karyotypes based on the assessment of more than 1000 individuals collected in a natural population. Comparisons of inversion frequencies between emerged and bait-collected flies showed not only that inversion arrangements were associated with differential longevity, but also that selection was sex specific. Because each individual fly was scored for thorax length and karyotype, we were able to show that longevity selection favoring larger flies coupled with the average effect of inversions on thorax length can account for the change of inversion frequencies due to longevity in females. The observed genotypic-by-sex interaction could be an important mechanism involved in the maintenance of the polymorphism. Arrangement 2Jz3 , which was shown to impaired fecundity in two independent previous studies, exhibited a positive effect on longevity. This pattern of negative pleiotropy may be another plausible mechanism accounting for the maintenance of the polymorphism.

Inversion Polymorphism, Longevity, and Body Size in a Natural Population of Drosophila buzzatii

Inversion Polymorphism, Longevity, and Body Size in a Natural Population of Drosophila buzzatii

Male sexual ornament size but not asymmetry reflects condition in stalk–eyed flies

Models of sexual selection predict that females use ornament size to evaluate male condition. It has also been suggested that ornament asymmetry provides females with accurate information about condition. To test these ideas we experimentally manipulated condition in the stalk-eyed fly, Cyrtodiopsis dalmanni, by varying the amount of food available to developing larvae. Males of this species have greatly exaggerated eyestalk length and females prefer to mate with males with wider eyespans. Our experiments show that male ornaments (eyestalks) display a disproportionate sensitivity to condition compared with the homologous character in females, and to non-sexual traits (wing dimensions). In contrast, in neither sex did asymmetry reflect condition either in sexual ornaments or in non-sexual traits. We conclude that ornament size is likely to play a far greater role in sexual selection as an indicator of individual condition than does asymmetry.

The Evolutionary History of Drosophila buzzatii XXXIV. The Distribution of the Retrotansposon Osvaldo in Original and Colonizing Populations

The frequency distribution of the retrotransposon Osvaldo in the haploid genome of Drosophila buzzatii has been studied in five natural populations from the Iberian Peninsula and six natural populations from Argentina. In Iberian populations, Osvaldo insertion sites do not follow a Poisson distribution, most probably due to eight euchromatic sites with high occupancy, found in all populations. The estimated alpha and beta parameters, which measure the relative importance of drift and negative selection in shaping frequency distributions, indicate that drift is the main force acting upon the distribution of Osvaldo in natural populations of D. buzzatii in the Iberian Peninsula. On the other hand, Osvaldo distribution in populations from Argentina is similar to the distribution of elements with low copy numbers, such as those described for Drosophila melanogaster and Drosophila simulans: there are no indications for deviation from a Poisson distribution, there is a low occupancy per insertion site, and genetic drift has no apparent effect on the frequency distribution. We propose that the unusual distribution found in the populations from the Iberian Peninsula is a consequence of the colonization process. Iberian Peninsula populations suffered a genomic redistribution of Osvaldo, most probably after a founder effect. Consequently, certain copies that arrived at high frequencies are showing a high occupancies today, and the mean copy number of Osvaldo is higher in Iberian Peninsula populations than in populations from Argentina. All other copies are the result of recent (after colonization) transposition events.

Antagonistic Pleiotropic Effect of Second-Chromosome Inversions on Body Size and Early Life-History Traits in Drosophila buzzatii

Antagonistic Pleiotropic Effect of Second-Chromosome Inversions on Body Size and Early Life-History Traits in Drosophila buzzatii

Correlations among size-related traits are affected by chromosome inversions in an adaptive polymorphism in Drosophila buzzatii

Genetic variation in correlations among size-related traits of head, thorax and wings was examined in Drosophila buzzatii, by comparing the correlation pattern of the phenotypic correlation matrix (CP-Rp) between inversion karyotypes of the second chromosome. CP-Rp differed between some karyotypes in a natural population. CP-Rp in homokaryotypic classes of wild-reared flies, but not in heterokaryotypes, differed from the whole population represented by laboratory-reared flies. Similarity in CP-Rp was highly significant for a same homokaryotype in two populations. In one of them, the chromosome is polymorphic for four inversions. In the other population, one of the inversions is almost fixed. CP-Rp was significantly similar between these populations, illustrating that similarity of CP-Rp may even occur between populations which have greatly diverged in frequencies of some genotypes affecting correlation patterns. It is suggested that chromosomal inversions are factors affecting genetic correlations among traits known to be phenotypically correlated with fitness components.

INVERSION LENGTH AND BREAKPOINT DISTRIBUTION IN THE DROSOPHILA BUZZATII SPECIES COMPLEX: IS INVERSION LENGTH A SELECTED TRAIT?

Length and position of breakpoints are characteristics of inversions that can be precisely determined on the polytene chromosomes of Drosophila species, and they provide crucial information about the processes that govern the origin and evolution of inversions. Eighty-six paracentric inversions described in the Drosophila buzzatii species complex and 18 inversions induced by introgressive hybridization in D. buzzatii were analyzed. In contrast to previous studies, inversion length and breakpoint distribution have been considered simultaneously. We conclude that: (1) inversion length is a selected trait; rare inversions are predominantly small while evolutionarily successful inversions, polymorphic and fixed, are predominantly intermediate in length; a nearly continuous variation in length, from small to medium sized, is found between less and more successful inversions; (2) there exists a significant negative correlation between length and number of polymorphic inversions per species which explains 39% of the inversion length variance; (3) natural selection on inversion length seems the main factor determining the relative position of breakpoints along the chromosomes; (4) the distribution of breakpoints according to their band location is non-random, with chromosomal segments that accumulate up to eight breakpoints.

Inversion Length and Breakpoint Distribution in the Drosophila buzzatii Species Complex: Is Inversion Length a Selected Trait?

Inversion Length and Breakpoint Distribution in the Drosophila buzzatii Species Complex: Is Inversion Length a Selected Trait?

Effects of extreme temperatures on phenotypic variation and developmental stability in Drosophila melanogaster and Drosophila buzzatii

The effect of stressful and nonstressful rearing temperatures on phenotypic variation of four quantitative characters (thorax length, wing length, number of sternopleural chaetae, number of arista branches) and on developmental stability (fluctuating asymmetry) of the three latter characters was estimated in twoDrosophilaspecies:Drosophila melanogasterandDrosophila buzzatii. In both species, a general trend for increasing of phenotypic variation and fluctuating asymmetry at stress temperatures was observed; in fluctuating asymmetry, this effect was more pronounced. An increase of phenotypic variation under stress was shown for all characters examined except sternopleural chaeta number inD. buzzatii. Comparison of species responses suggests that the increase of variation inD. melanogasterwas somewhat higher than inD. buzzatii.