The DAIBAM MITE element is involved in the origin of one fixed and two polymorphic Drosophila virilis phylad inversions

Chromosomal inversions can originate from breakage and repair by non-homologous end-joining. Nevertheless, they can also originate from ectopic recombination between transposable elements located on the same chromosome inserted in opposite orientations. Here, we show that a MITE element (DAIBAM), previously involved in the origin of one Drosophila americana polymorphic inversion, is also involved in the origin of one fixed inversion between D. virilis and D. americana and another D. americana polymorphic inversion. Therefore, DAIBAM is responsible for at least 20% of the chromosomal rearrangements that are observed within and between species of the virilis phylad (D. virilis, D. lummei, D. novamexicana and D. americana), having thus played a significant role in the chromosomal evolution of this group of closely related species.     

The evolutionary history of Drosophila buzzatii. XXXV. Inversion polymorphism and nucleotide variability in different regions of the second chromosome

Inversions are portions of a chromosome where the gene order is reversed relative to a standard reference orientation. Because of reduced levels of recombination in heterokaryotypes, inversions have a potentially important effect on patterns of nucleotide variability in those genomic regions close to, or included in, the inverted fragments. Here we report sequence variation at three anonymous regions (STSs) located at different positions in relation to second-chromosome inversion breakpoints in 29 isochromosomal lines derived from an Argentinean population of Drosophila buzzatii. In agreement with previous findings in Drosophila, gene flux (crossing over and/or gene conversion) between arrangements seems to appreciably increase as we approach the middle sections of inversion 2j, and patterns of nucleotide variability within, as well as genetic differentiation between chromosome arrangements, are comparable to those observed at the molecular marker outside the inverted fragments. On the other hand, nucleotide diversity near the proximal breakpoint of inversion 2j is reduced when contrasted with that found at the other regions, particularly in the case of derived inverted chromosomes. Using the data from the breakpoint, we estimate that the inversion polymorphism is approximately 1.63 N generations old, where N is the effective population size. An excess of low-frequency segregating polymorphisms is detected; mostly in the ancestral 2st arrangement and probably indicating a population expansion that predates the coalescent time of inversion 2j. Heterogeneity in mutation rates between the markers linked to the inversions may be sufficient to explain the different levels of nucleotide diversity observed. When considered in the context of other studies on patterns of variation relative to physical distance to inversion breakpoints, our data appear to be consistent with the conclusion that inversions are unlikely to be "long-lived" balanced polymorphisms.     

Continuing studies on chromosomal polymorphism in a Korean natural population of Drosophila melanogaster

Investigations on the chromosomal inversion polymorphism were conducted on a Korean (Taenung) natural population of D. melanogaster during the period 1978 to 1992. A total of 66 different endemic and cosmopolitan inversions were found on both major chromosome pairs II and III. Some of them proved to be rare cosmopolitan types (2LKA, 2LNS, 2LF, 2RCy, 3LM, 3RKI, and 3RK), while others were endemics. The distribution of breakpoints for endemic and rare cosmopolitan inversions are not random along the two autosome arms.With respect to frequency changes, the 15-year survey revealed that five of the cosmopolitan types (2Lt, 2RNS, 3LP, 3RC, and 3RMo) exhibit cyclical frequency changes, whereas gene arrangement 3RP shows relatively stable frequencies. Tests for correlations between gene arrangement frequencies and several climatic variables gave no clear evidence for such relationships. Only one correlation coefficient out of 64 was statistically significant. This revised version was published online in July 2006 with corrections to the Cover Date.     

Genetic loads and coadaptivity of chromosomal inversions I. Inversion polymorphism and genetic load on chromosome O in a Drosophila subobscura population from Petnica

Inversion polymorphism on chromosome O and polymorphism for the viability of determining genes have been studied in a natural population of Drosophila subobscura from Petnica (Serbia). The range of inversion polymorphism and the abundance of particular gene arrangements in the study population agree with a general pattern of inversion polymorphism of D. subobscura in Europe. The data obtained on the amount of genetic loads show that the D. subobscura population from Petnica displays a moderate degree of that polymorphism, compared to the other studied populations of these species. Therefore, the D. subobscura population from Petnica could be tentatively classified as an ecologically central population. Examination association of chromosomal, thus, inversion polymorphism with gene polymorphism, in the form of genetic loads show that differences exist in the mean viability among certain gene arrangements. The distribution of deleterious genes among chromosome O gene arrangements were non-random.     

Ecology of body size in Drosophila buzzatii: untangling the effects of temperature and nutrition

Abstract.

• 1 A method of separating the effects of two important determinants of body size in natural populations, temperature of larval development and level of larval nutrition, by making measurements of thorax length and wing length of adult flies is investigated.
• 2 I show that at any given time variation in body size of Drosophila buzzatii from two sites in eastern Australia is determined primarily by variation in the quality of nutrition available to larvae.
• 3 Throughout the year adult flies are consistently at least 25% smaller in volume than predicted for optimal nutrition at their predicted temperature of larval development.
• 4 Nutritional stress is therefore a year-round problem for these flies.
• 5 Measurements of adult flies emerging from individual breeding substrates (rotting cactus cladodes) show that there is substantial variation among these substrates in the nutrition available to larvae.
• 6 This method will allow study of spatial and temporal variation in the temperature of larval substrates and in the nutritional resources available to flies in natural populations.

     

Genomic impacts of chromosomal inversions in parapatric Drosophila species

Chromosomal inversions impact genetic variation and facilitate speciation in part by reducing recombination in heterokaryotypes. We generated multiple whole-genome shotgun sequences of the parapatric species pair Drosophila pseudoobscura and Drosophila persimilis and their sympatric outgroup (Drosophila miranda) and compared the average pairwise differences for neutral sites within, just outside and far outside of the three large inversions. Divergence between D. pseudoobscura and D. persimilis is high inside the inversions and in the suppressed recombination regions extending 2.5 Mb outside of inversions, but significantly lower in collinear regions further from the inversions. We observe little evidence of decreased divergence predicted to exist in the centre of inversions, suggesting that gene flow through double crossovers or gene conversion is limited within the inversion, or selection is acting within the inversion to maintain divergence in the face of gene flow. In combination with past studies, we provide evidence that inversions in this system maintain areas of high divergence in the face of hybridization, and have done so for a substantial period of time. The left arm of the X chromosome and chromosome 2 inversions appear to have arisen in the lineage leading to D. persimilis approximately 2 Ma, near the time of the split of D. persimilis-D. pseudoobscura-D. miranda, but likely fixed within D. persimilis much more recently, as diversity within D. persimilis is substantially reduced inside and near these two inversions. We also hypothesize that the inversions in D. persimilis may provide an empirical example of the 'mixed geographical mode' theory of inversion origin and fixation, whereby allopatry and secondary contact both play a role.     

Divergence in wing morphology among sibling species of the Drosophila buzzatii cluster

The Drosophila buzzatii species cluster consists of the sibling species D. buzzatii, D. koepferae, D. serido, D. borborema, D. seriema, D. antonietae and D. gouveai, all of which breed exclusively in decaying cactus tissue and, except for D. buzzatii (a colonizing subcosmopolitan species), are endemic to South America. Using a morphometric approach and multivariate analysis of 17 wing parameters, we investigated the degree of divergence in wing morphology among the sibling species of this cluster. Significant differences were obtained among the species and discriminant analysis showed that wing morphology was sufficiently different to allow the correct classification of 98.6% of the 70 individuals analysed. The phenetic relationships among the species inferred from UPGMA cluster analysis based on squared Mahalanobis distances (D²) were generally compatible with previously published phylogenetic relationships. These results suggest that wing morphology within D. buzzatii cluster is of phylogenetic importance.     

Contrasting patterns of phenotypic variation linked to chromosomal inversions in native and colonizing populations of Drosophila subobscura

In fewer than two decades after invading the Americas, the fly Drosophila subobscura evolved latitudinal clines for chromosomal inversion frequencies and wing size that are parallel to the long‐standing ones in native Palearctic populations. By sharp contrast, wing shape clines also evolved in the New World, but the relationship with latitude was opposite to that in the Old World. Previous work has suggested that wing trait differences among individuals are partially due to the association between chromosomal inversions and particular alleles which influence the trait under consideration. Furthermore, it is well documented that a few number of effective individuals founded the New World populations, which might have modified the biometrical effect of inversions on quantitative traits. Here we evaluate the relative contribution of chromosomal inversion clines in shaping the parallel clines in wing size and contrasting clines in wing shape in native and colonizing populations of the species. Our results reveal that inversion‐size and inversion‐shape associations in native and colonizing (South America) populations are generally different, probably due to the bottleneck effect. Contingent, unpredictable evolution was suggested as an explanation for the different details involved in the otherwise parallel wing size clines between Old and New World populations of D. subobscura. We challenge this assertion and conclude that contrasting wing shape clines came out as a correlated response of inversion clines that might have been predicted considering the genetic background of colonizers.     

Changes in chromosomal polymorphism and global warming: The case of Drosophila subobscura from Apatin (Serbia)

In this study, chromosomal inversion polymorphism data for a natural population of Drosophila subobscura from a swampy region near the town of Apatin (Serbia) were compared with data for the same population collected approximately 15 years earlier. The pattern of chromosomal inversion polymorphism changed over time. There were significant increases in the frequency of characteristic southern latitude ("warm" adapted) chromosomal arrangements and significant decreases in the frequency of characteristic northern latitude ("cold" adapted) chromosomal arrangements in the O and U chromosomes. The chromosomal arrangements O(3+4) and O(3+4) (+) (22) (derived from the O(3+4) arrangement) showed significant increases in 2008 and 2009 with regard to the 1994 sample. There was also a significant increase (～50%) in the U(1) (+) (2) arrangement, while U(1+8) (+) (2) (a typical southern arrangement) was detected for the first time. Since the Apatin swampy population of D. subobscura has existed for a long time in a stable habitat with high humidity that has not been changed by man our results indicate that natural selection has produced chromosomal changes in response to the increase in temperature that has occurred in the Balkan Peninsula of central southeastern European.     

Maintenance of transposable element copy number in natural populations of Drosophila melanogaster and D. simulans

To investigate the main forces controlling the containment of transposable elements (TE) in natural populations, we analyzed the copia, mdg1, and 412 elements in various populations of Drosophila melanogaster and D. simulans. A lower proportion of insertion sites on the X chromosome in comparison with the autosomes suggests that selection against the detrimental effects of TE insertions is the major force containing TE copies in populations of Drosophila. This selection effect hypothesis is strengthened by the absence of the negative correlation between recombination rate and TE copy number along the chromosomes, which was expected under the alternative ectopic exchange model (selection against the deleterious rearrangements promoted by recombination between TE insertions). A cline in 412 copy number in relation to latitude was observed among the natural populations of D. simulans, with very high numbers existing in some local populations (around 60 copies in a sample from Canberra, Australia). An apparent absence of selection effects in this Canberra sample and a value of transposition rate equal to 1–2 × 10^-3 whatever the population and its copy number agree with the idea of recent but temporarily drastic TE movements in local populations. The high values of transposition rate in D. simulans clearly disfavor the hypothesis that the low amount of transposable elements in this species could result from a low transposition rate. This revised version was published online in August 2006 with corrections to the Cover Date.     

Accumulation of Spock and Worf,two novel non-LTR retrotransposons,on the neo-Y chromosome of Drosophila miranda

Transposable elements constitute a major fraction of eukaryotic genomes. Here, I characterize two novel non-LTR retrotransposons, cloned from the neo-Y chromosome of Drosophila miranda. Worf is 4.1 kb in size and shows homology to the T1-2 non-LTR transposon characterized in Anopheles. Spock is 4.9 kb in size and shows similarity to the Doc element of D. melanogaster. Southern blot analysis of both elements yielded stronger signals for male DNA. In situ hybridization to polytene chromosomes revealed that both elements are accumulating on the neo-Y chromosome of D. miranda. PCR analysis was conducted to investigate the frequency of spock and worf and of the previously identified transposons, TRIM and TRAM, at individual chromosomal sites among 12 strains of D. miranda. Contrary to the observation that element frequencies are usually kept low at individual sites in Drosophila, the four transposons investigated are fixed at their genomic locations on the neo-Y chromosome. These results support the hypothesis that transposons accumulate in nonrecombining regions and may be one cause of the heteromorphism of sex chromosomes.     

Remating and sperm displacement in a natural population of Drosophila buzzatii inferred from mother-offspring analysis of microsatellite loci

Prospects for estimation of parameters of models of sperm competition from field data have improved recently with the development of methods that employ multilocus genotype data from brood-structured samples. Sperm competition in Drosophila buzzatii is of special interest because it is possible to directly observe the breeding behaviour of this species in its natural habitat of rotting cactus. Previous laboratory experiments showed that this species exhibits an unusual pattern of frequent remating and sperm partitioning. This paper reports the first attempt to estimate the frequency of female remating and sperm competition in natural populations of D. buzzatii. For the Australian population studied, the mean remating frequency was lower (alpha = 2.12-2.20) than previously estimated in laboratory experiments with the same population, whereas mean sperm displacement (beta = 0.69-0.71) fell within the limits of previous laboratory results. The evolution of the D. buzzatii mating system is discussed.     

Integration specificity of the hobo element of Drosophila melanogaster is dependent on sequences flanking the integration site

We analyzed the integration specificity of the hobo transposable element of Drosophila melanogaster. Our results indicate that hobo is similar to other transposable elements in that it can integrate into a large number of sites, but that some sites are preferred over others, with a few sites acting as integration hot spots. A comparison of DNA sequences from 112 hobo integration sites identified a consensus sequence of NTNNNNAC, but this consensus was insufficient to account for the observed integration specificity. To begin to define the parameters affecting hobo integration preferences, we analyzed sequences flanking a donor hobo element, as well as sequences flanking a hobo integration hot spot for their relative influence on hobo integration specificity. We demonstrate experimentally that sequences flanking a hobo donor element do not influence subsequent integration site preference, whereas, sequences contained within 31 base pairs flanking an integration hot spot have a significant effect on the frequency of integration into that site. However, sequence analysis of the DNA flanking several hot spots failed to identify any common sequence motif shared by these sites. This lack of primary sequence information suggests that higher order DNA structural characteristics of the DNA and/or chromatin may influence integration site selection by the hobo element. This revised version was published online in July 2006 with corrections to the Cover Date.     

Numerous groups of chromosomal regional paralogies strongly indicate two genome doublings at the root of the vertebrates

The appearance of the vertebrates demarcates some of the most far-reaching changes of structure and function seen during the evolution of the metazoans. These drastic changes of body plan and expansion of the central nervous system among other organs coincide with increased gene numbers. The presence of several groups of paralogous chromosomal regions in the human genome is a reflection of this increase. The simplest explanation for the existence of these paralogies would be two genome doublings with subsequent silencing of many genes. It is argued that gene localization data and the delineation of paralogous chromosomal regions give more reliable information about these types of events than dendrograms of gene families as gene relationships are often obscured by uneven replacement rates as well as other factors. Furthermore, the topographical relations of some paralogy groups are discussed.     

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.     

Inferring the evolutionary history of Drosophila americana and Drosophila novamexicana using a multilocus approach and the influence of chromosomal rearrangements in single gene analyses

The evolutionary history of closely related organisms can prove sometimes difficult to infer. Hybridization and incomplete lineage sorting are the main concerns; however, genome rearrangements can also influence the outcome of analyses based on nuclear sequences. In the present study, DNA sequences from 12 nuclear genes, for which the approximate chromosomal locations are known, have been used to estimate the evolutionary history of two forms of Drosophila americana ( Drosophila   americana americana and Drosophila americana texana ) and Drosophila novamexicana ( virilis group of species). The phylogenetic analysis of the combined data set resulted in a phylogeny showing reciprocal monophyly for D. novamexicana and D. americana . Single gene analyses, however, resulted in incongruent phylogenies influenced by chromosomal rearrangements. Genetic differentiation estimates indicated a significant differentiation between the two species for all genes. Within D. americana , however, there is no evidence for differentiation between the chromosomal forms except at genes located near the X/4 fusion and Xc inversion breakpoint. Thus, the specific status of D. americana and D. novamexicana is confirmed, but there is no overall evidence for genetic differentiation between D. a. americana and D. a. texana , not supporting a subspecific status. Based on levels of allele and nucleotide diversity found in the strains used, it is proposed that D. americana has had a stable, large population during the recent past while D. novamexicana has speciated from a peripheral southwestern population having had an ancestral small effective population size. The influence of chromosomal rearrangements in single gene analyses is also examined.