Chromosome inversion polymorphisms in Drosophila melanogaster II. Geographic clines and climatic associations in Australasia,North America and Asia

The four paracentric autosomal chromosome inversions In(2L)t, In(2R)NS, In(3L)P and In(3R)R are commonly polymorphic in natural populations of D. melanogaster in Australasia, North America and Asia, with latitudinal clines in the frequencies of each inversion in each region. In each region inversion frequency decreases with increasing distance from the equator, although the precise relationship between frequency and latitude varies between inversions and, for In(2L)t and In(2R)NS, among regions. Each inversion also shows a longitudinal cline in at least one region but none show such a cline in all three. Although no inversion's frequency is associated with the same climatic variable in all three regions, inversion frequencies are generally positively related to annual maximum temperature and, more particularly, minimum temperature and minimum rainfall. The directions of the latitudinal clines and the climatic associations are consonant with evidence from D. melanogaster that inversion frequencies decline in winter. They are also consonant with evidence from some other Drosophila species that inversion heterozygosities are lower at the geographic margins than at the centre of the species' ranges.     

The role of the transposable element hobo in the origin of endemic inversions in wild populations of Drosophila melanogaster

Evidence from in situ hybridizations of DNA from the transposable element hobo to polytene salivary gland chromosome squashes reveals that hobo occupies both cytological breakpoints of three of four endemic inversions sampled from natural populations of Drosophila melanogaster in the Hawaiian islands. The fourth endemic inversion has a single hobo insert at one breakpoint. Cosmopolitan inversions on the same chromosomes do not show this association. Frequencies of both endemic and cosmopolitan inversions in Hawaiian populations fall in ranges typical for natural populations of D. melanogaster sampled worldwide, suggesting that these results may be typical of other regions besides Hawaii. This appears to be the first direct demonstration that transposable elements are responsible for causing specific rearrangements found in nature; consequently, it is also the first direct demonstration that chromosome rearrangements can arise in nature in a manner predicted by results of hybrid dysgenic crosses in the laboratory. Possible population genetic and evolutionary consequences are discussed.     

Inversion Polymorphisms in Populations of Drosophila Melanogaster in the South-West Islands of Japan: Comparisons with the Mainland Populations

Natural populations of D. melanogaster newly collected from the South-West Islands of Japan were examined for the frequencies of inversions, and the results, together with previous data, were compared with those of the mainland populations. The four Common cosmopolitan inversions (2Lt, 2RNS, 3LP, 3RP) were detected from most of the populations with higher frequencies. The three Rare cosmopolitan inversions (3LM, 3RC, 3RMo), three Quasi cosmopolitan inversions (2LA, 3LY, 3RK) and two new Endemic inversions were also found but with lower frequencies. Some of the South-West Island populations still maintained higher levels of inversion polymorphisms compared to the mainland populations, while others lost the polymorphisms to various degrees. The South-West Island populations were characterized by the higher frequency of In(3L)P. The ratios of In(3L)P/In(3R)P in the South-West Islands are significantly higher than those of the mainland populations, suggesting that the In(3L)P is relatively adaptive in the South-West Islands.     

Chromosome inversion polymorphism in natural populations of Drosophila punjabiensis Parshad and Paika

Drosophila punjabiensis, a member of the montium subgroup of the melanogaster species group is a very common and widespread species of Drosophila in the Indian subcontinent. Analysis of different geographic populations of this species in India has revealed altogether nine paracentric inversions. The relationship between inversions and the different environmental conditions is discussed. The pattern of inversion polymorphism in D. punjabiensis and its sibling species, D. jambulina are compared.     

Inference of chromosomal inversion dynamics from Pool‐Seq data in natural and laboratory populations of Drosophila melanogaster

Sequencing of pools of individuals (Pool‐Seq) represents a reliable and cost‐effective approach for estimating genome‐wide SNP and transposable element insertion frequencies. However, Pool‐Seq does not provide direct information on haplotypes so that, for example, obtaining inversion frequencies has not been possible until now. Here, we have developed a new set of diagnostic marker SNPs for seven cosmopolitan inversions in Drosophila melanogaster that can be used to infer inversion frequencies from Pool‐Seq data. We applied our novel marker set to Pool‐Seq data from an experimental evolution study and from North American and Australian latitudinal clines. In the experimental evolution data, we find evidence that positive selection has driven the frequencies of In(3R)C and In(3R)Mo to increase over time. In the clinal data, we confirm the existence of frequency clines for In(2L)t, In(3L)P and In(3R)Payne in both North America and Australia and detect a previously unknown latitudinal cline for In(3R)Mo in North America. The inversion markers developed here provide a versatile and robust tool for characterizing inversion frequencies and their dynamics in Pool‐Seq data from diverse D. melanogaster populations.     

Intra-and interchromosomal effects of heterozygous inversions on recombination in the third chromosome of Drosophila ananassae

In order to study intra-and interchromosomal effects of heterozygous inversions on recombination in the third chromosome of D.ananassae, experiments were conducted using Stw-pr marker stock and five wild stocks with known karyotypes. The stocks used were homozygous for standard or inverted gene sequence in 2L, 3L, and 3R. Recombination was investigated in both sexes. There was complete absence of crossing-over in males in all the experiments which appeared to be the characteristic of marker stock as spontaneous male crossing-over was reported earlier with the same wild stocks when the second chromosome markers were used. Based on the data of karyotypically homozygous F1 females, the map distance between stw-pr was 36.55 map units. The heterozygosity due to a lengthy inversion in 2L increased the level of crossing-over between stw-pr genes of the third chromosome indicating interchromosomal effect. There was a considerable reduction in the rate of recombination between the same markers due to inversion heterozygosity in 3R indicating intrachromosomal effect. However, 3L inversion heterozygosity had no effect on crossover rate. These results provide evidence for intra-and interchromosomal effects of inversions on crossing-over in the third chromosome of D. ananassae.     

Linkage disequilibrium in laboratory populations of Drosophila nasuta

Summary Natural populations of Drosophila nasuta are polymorphic for many gene arrangements. Two non-overlapping inversions of the third chromosome, III-2 and III-35, are most common and display extreme linkage disequilibrium. Six randomly mating laboratory stocks, each founded by one gravid female heterozygous in coupling for both III-2 and III-35, were observed after 32 generations. Significant linkage disequilibrium was observed in all stocks. Recombinants were found in only two stocks. The absence of effective recombination in some stocks and its presence in others might be due to different genotypic backgrounds. We suggest that natural selection, influencing recombination rates in several ways, and intrachromosomal epistasis between the two inversions were the main factors for the maintenance of linkage disequilibrium in D. nasuta.     

Evolutionary genetics of Drosophila ananassae. I. Effect of selection on body size and inversion frequencies

Adaptive importance of inversion polymorphism has been discussed in Drosophila species at several levels but no study has been carried out demonstrating the individual and combined effects of polymorphic inversions on the fitness of flies through bi‐directional selection. Therefore, artificial bi‐directional selection for thorax length in Drosophila ananassae was carried out for 10 generations. Both, Tukey test for selection difference and regression coefficients of offspring on mid‐parent are highly significant. The realized heritability (h²) in males of both high and low selection lines is more or less similar but is more pronounced in low line females, which suggests the asymmetrical response. This asymmetry in selection is discussed in the light of evidence provided by the study of chromosome inversion frequencies in different selection lines at different generations of selection. Interestingly, chromosome inversion frequency changes towards homozygosity for different gene arrangements in different selection lines. Tests of correlations at G₆ and G₁₀ among different gene arrangements as well as with mean thorax length suggest that 2L‐ST gene arrangement is negatively correlated, while 3L‐ST gene arrangement is positively correlated with thorax length. Furthermore, the present study shows the significant effects of 3L‐ST and 2L + 3L (positive correlation) on thorax length, while 3R‐ST and 2L + 3R show significant effect (negative correlation) on thorax length, which was not evident in the previous study. Present results also suggest how polymorphic inversions and their combinations affect the body size differently in different selection lines. These results suggest that thorax length in D. ananassae is under polygenic control and inversion polymorphism plays crucial role in maintaining body size by modifying genotypic frequency under various selection pressures.     

Patterns of puffing activity in the salivary gland chromosomes of Drosophila

Puffing patterns of chromosome arm 3 L of D. yakuba are compared with those of other members of the melanogaster species subgroup D. melanogaster and D. simulans. Several paracentric inversions on 3L have resulted in a considerable rearrangement of gene order in D. yakuba. However the basic sequence of changes in puffing activity which occurs during late larval and prepupal development is very similar to that of D. melanogaster and D. simulans. A fourth member of this species subgroup (D. teissieri) also has similar puffing patterns to those of D. melanogaster despite considerable chromosome evolution.     

Genomic evidence for role of inversion 3RP of Drosophila melanogaster in facilitating climate change adaptation

Chromosomal inversion polymorphisms are common in animals and plants, and recent models suggest that alternative arrangements spread by capturing different combinations of alleles acting additively or epistatically to favour local adaptation. It is also thought that inversions typically maintain favoured combinations for a long time by suppressing recombination between alternative chromosomal arrangements. Here, we consider patterns of linkage disequilibrium and genetic divergence in an old inversion polymorphism in Drosophila melanogaster (In(3R)Payne) known to be associated with climate change adaptation and a recent invasion event into Australia. We extracted, karyotyped and sequenced whole chromosomes from two Australian populations, so that changes in the arrangement of the alleles between geographically separated tropical and temperate areas could be compared. Chromosome‐wide linkage disequilibrium (LD) analysis revealed strong LD within the region spanned by In(3R)Payne. This genomic region also showed strong differentiation between the tropical and the temperate populations, but no differentiation between different karyotypes from the same population, after controlling for chromosomal arrangement. Patterns of differentiation across the chromosome arm and in gene ontologies were enhanced by the presence of the inversion. These data support the notion that inversions are strongly selected by bringing together combinations of genes, but it is still not clear if such combinations act additively or epistatically. Our data suggest that climatic adaptation through inversions can be dynamic, reflecting changes in the relative abundance of different forms of an inversion and ongoing evolution of allelic content within an inversion.     

Comparative mapping of cosmids and gene clones from a 1.6 Mb chromosomal region of Drosophila melanogaster in three species of the distantly related subgenus Drosophila

The successful hybridization of cosmid clones from Drosophila melanogaster (Sophophora subgenus) to the salivary gland chromosomes of other species as distantly related as those in the Drosophila subgenus attests their great potential for unravelling genome evolution. We have carried out, using 28 cosmids and 13 gene clones, a study of the organization of the D. melanogaster 95A-96A chromosomal region in three Drosophila subgenus species: D. repleta, D. buzzattii and D. virilis. These clones were first used to built an accurate map of this 1.6 Mb region of D. melanogaster chromosome 3R (Muller’s element E). Then, they were hybridized and mapped to the homologous chromosome 2 of the other three distantly related species. The studied region is disseminated over 13 different sites of chromosome 2 in the Drosophila subgenus species, which implies a minimum of 12 inversion breakpoints fixed between the two subgenera. Extrapolation to the entire chromosome gives 90 fixed inversions. The D. melanogaster Pp1-96A-Acr96Aa segment conserved in D. repleta and D. buzzatii is longer than previously thought and is also conserved in D. virilis. In addition, three other D. melanogaster segments conserved in the three Drosophila subgenus species were found. Finally, our data indicate significant statistical differences in the evolution rate of Muller’s element E among lineages, a result that agrees well with the previous cytogenetic data. Received: 22 July 1998; in revised form: 11 November 1998 / Accepted: 12 November 1998     

Inversion polymorphism in Indian natural populations of Drosophila melanogaster

Six natural populations (three urban and three rural) of Drosophila melanogaster from India were analysed for chromosome inversions, revealing the presence of 19 different paracentric autosomal inversions. One new inversion has also been detected in a laboratory stock established from flies collected from Kerala. In total 20 different paracentric inversions in Indian D. melanogaster have been detected during the present study, and of these, 4 are common cosmopolitans; 2 are rare cosmopolitans; 7 are recurrent endemics; and 7 are unique endemics. The quantitative data clearly show that the urban populations are different from the rural ones with respect to inversion polymorphism.     

Genomics of natural populations: Evolutionary forces that establish and maintain gene arrangements in Drosophila pseudoobscura

The evolution of complex traits in heterogeneous environments may shape the order of genes within chromosomes. Drosophila pseudoobscura has a rich gene arrangement polymorphism that allows one to test evolutionary genetic hypotheses about how chromosomal inversions are established in populations. D. pseudoobscura has >30 gene arrangements on a single chromosome that were generated through a series of overlapping inversion mutations with >10 inversions with appreciable frequencies and wide geographic distributions. This study analyses the genomic sequences of 54 strains of Drosophila pseudoobscura that carry one of six different chromosomal arrangements to test whether (i) genetic drift, (ii) hitchhiking with an adaptive allele, (iii) direct effects of inversions to create gene disruptions caused by breakpoints, or (iv) indirect effects of inversions in limiting the formation of recombinant gametes are responsible for the establishment of new gene arrangements. We found that the inversion events do not disrupt the structure of protein coding genes at the breakpoints. Population genetic analyses of 2,669 protein coding genes identified 277 outlier loci harbouring elevated frequencies of arrangement‐specific derived alleles. Significant linkage disequilibrium occurs among distant loci interspersed between regions with low levels of association indicating that distant allelic combinations are held together despite shared polymorphism among arrangements. Outlier genes showing evidence of genetic differentiation between arrangements are enriched for sensory perception and detoxification genes. The data presented here support the indirect effect of inversion hypothesis where chromosomal inversions are favoured because they maintain linked associations among multilocus allelic combinations among different arrangements.     

Speciation and chromosomal evolution of the Baikalian endemic chironomids of the genus Sergentia Kief. (Diptera, Chironomidae): Karyotype divergence and chromosomal polymorphism in the populations of deep-water species Sergentia nebulosa Linevitsh et al. and Sergentia assimilis Proviz V. et Proviz L.

Specific karyotype structure and chromosomal polymorphism was investigated in the populations of Sergentia nebulosa Linevitsh et al., 1984 and Sergentia assimilis Proviz V. et Proviz L., 1999, the deep-water endemic chironomid species (Diptera, Chironomidae) from the Baikal Lake. The distinguishing feature of the karyotypes of these species, compared to the other Baikalian Sergentia, is well-developed nucleolus in region 6 of arm C. Both species display the presence of interspecific population polymorphism, determined by the structure of this arm. In some populations, chromosome regions from 4 to 6 contain a homozygous inversion, which is absent in the other populations. The distinguishing karyotype feature of S. assimilis, which shares fluctuating homozygous inversions with the other species, is the presence of two species-specific homozygous inversions. These are the secondary overlapping inversion in arm A, regions 2 to 7, and the inversion in regions 4 to 10 of arm G. Both species of interest contain nucleolus organizer in region 10 of arm G. In populations of S. nebulosa, six heterozygous inversions localized in arms A, B, C, F, and G were discovered. The highest number of heterozygotes for inversions (71%) was observed in the population from Southern Baikal. In arm B of S. assimilis, one heterozygous inversion and heterozygosity for nucleolus organizer in the chromosome region 16 was detected. Chromosomal evolution of Baikalian Sergentia, and the role of inversion polymorphism in the population adaptation is discussed. Original Russian Text ? V.I. Proviz, 2008, published in Genetika, 2008, Vol. 44, No. 12, pp. 1627–1637.     

Mapping regions within cosmopolitan inversion In(3R)Payne associated with natural variation in body size in Drosophila melanogaster

Associations between genotypes for inversions and quantitative traits have been reported in several organisms, but little has been done to localize regions within inversions controlling variation in these traits. Here, we use an association mapping technique to identify genomic regions controlling variation in wing size within the cosmopolitan inversion In(3R)Payne in Drosophila melanogaster. Previous studies have shown that this inversion strongly influences variation in wing size, a trait highly correlated with body size. We found three alleles from two separate regions within In(3R)Payne with significant additive effects on wing size after the additional effect of the inversion itself had been taken into account. There were also several alleles with significant genotype-by-inversion interaction effects on wing size. None of the alleles tested had a significant additive effect on development time, suggesting different genes control these traits and that clinal patterns in them have therefore arisen independently. The presence of multiple regions within In(3R)Payne controlling size is consistent with the idea that inversions persist in populations because they contain multiple sets of locally adapted alleles, but more work needs to be done to test if they are indeed coadapted.     

Chromosomal polymorphisms in the pitcher-plant mosquito,Wyeomyia smithii

A local population of the pitcher-plant mosquito, Wyeomyia smithii (Diptera: Culicidae, Culicini) in western New York State contains naturally polymorphic salivary gland chromosomes. Maps depicting the proposed standard sequence of bands along each of the three chromosomes are presented. Structural conformations of heterokaryotypes reveal ten paracentric inversions. Four inversions occur in chromosome 1, and three in each of chromosomes 2 and 3. All the inversions are small, occupying 3–17% of the length of their respective chromosomes, and all are located in the terminal 1/5 to 1/2 of a chromosome arm. Three inversions are almost adjacent on chromosome 1. On chromosome 2 one inversion lies completely within another. Three inversions on chromosome 3 partially overlap. The remaining two inversions occur alone, one on chromosome 1 and the other on chromosome 2. Another polymorphism, with no visible alteration of band sequence, produces asynapsis of all but the tip of the left arm of chromosome 1, and shows a significant change in frequency between two successive years. No inversion exhibits a significant seasonal change in frequency, though some fluctuation in frequency was noted in two cases. The rarest inversion in the population exists at a frequency below 0.01, and the two most common inversions at frequencies of 0.44 and 0.52. The average inversion heterozygosity of an individual is between 1.7 and 2.4 based on two different estimation procedures. Heterokaryotypes for several of the inversions were significantly more frequent than they should have been, given binomial expectations. Cytogenetic analysis of W. smithii was deemed particularly desirable because this species has been and continues to be the subject of extensive biometrical-genetic, ecological, and evolutionary investigation.This paper is the seventh in a series on the ecology and evolution of the pitcher-plant mosquito     

Inversion polymorphism in populations of Drosophila sulphurigaster albostrigata and Drosophila nasuta albomicans from Phuket,Thailand

Two species of the Drosophila nasuta subgroup of the Drosophila immigrans group, D. sulphurigaster albostrigata and D. nasuta albomicans were investigated in this study. Collections of both species were made from Phuket, Thailand. Both species have similar salivary chromosomes, with four autosomal arms and one sex chromosome arm, and both are highly polymorphic for paracentric inversions. D. s. albostrigata accounted for the majority of the isolines collected and exhibited the greater number of inversions. One inversion, C₁, was common to both species, indicating common ancestry.A non-random distribution of inversions was observed on the proximal end of chromosome II in both D. s. albostrigata and D. n. albomicans. An inter-collection comparison revealed that both rigid and flexible chromosomal polymorphism were operating in the two species, with a seasonal variation noted for one inversion in D. s. albostrigata. A non-random association of two inversions was observed in D. n. albomicans.Based on a comparison of the indices of crossing over, both D. s. albostrigata and D. n. albomicans were found to be more heterozygous than in previous studies, with D. n. albomicans appearing to have evolved further than D. s. albostrigata.Based on a thesis submitted for the degree of Ph. D. at the University of Queensland.     

Arm-specific dynamics of chromosome evolution in malaria mosquitoes

Background  

The malaria mosquito species of subgenus Cellia have rich inversion polymorphisms that correlate with environmental variables. Polymorphic inversions tend to cluster on the chromosomal arms 2R and 2L but not on X, 3R and 3L in Anopheles gambiae and homologous arms in other species. However, it is unknown whether polymorphic inversions on homologous chromosomal arms of distantly related species from subgenus Cellia nonrandomly share similar sets of genes. It is also unclear if the evolutionary breakage of inversion-poor chromosomal arms is under constraints.     

Parallel effects of the inversion In(3R)Payne on body size across the North American and Australian clines in Drosophila melanogaster

Chromosomal inversions are thought to play a major role in climatic adaptation. In D. melanogaster, the cosmopolitan inversion In(3R)Payne exhibits latitudinal clines on multiple continents. As many fitness traits show similar clines, it is tempting to hypothesize that In(3R)P underlies observed clinal patterns for some of these traits. In support of this idea, previous work in Australian populations has demonstrated that In(3R)P affects body size but not development time or cold resistance. However, similar data from other clines of this inversion are largely lacking; finding parallel effects of In(3R)P across multiple clines would considerably strengthen the case for clinal selection. Here, we have analysed the phenotypic effects of In(3R)P in populations originating from the endpoints of the latitudinal cline along the North American east coast. We measured development time, egg‐to‐adult survival, several size‐related traits (femur and tibia length, wing area and shape), chill coma recovery, oxidative stress resistance and triglyceride content in homokaryon lines carrying In(3R)P or the standard arrangement. Our central finding is that the effects of In(3R)P along the North American cline match those observed in Australia: standard arrangement lines were larger than inverted lines, but the inversion did not influence development time or cold resistance. Similarly, In(3R)P did not affect egg‐to‐adult survival, oxidative stress resistance and lipid content. In(3R)P thus seems to specifically affect size traits in populations from both continents. This parallelism strongly suggests an adaptive pattern, whereby the inversion has captured alleles associated with growth regulation and clinal selection acts on size across both continents.     

The role of genic selection in the establishment of inversion polymorphism in Drosophila subobscura

A model for explaining the establishment of newly arisen inversions in natural populations, in which the inverted segment may be selected for if its load of deleterious mutations is smaller than the average load of the noninverted segment in the population, is tested for Drosophila subobscura. The results show that for new inversions, originally with no deleterious alleles, the expected cumulative distribution of inversion lengths fits fairly well with the observed one. Therefore, genic selection may be an important cause of the establishment of newly arisen inversions in natural populations of D. subobscura. The applicability of the model to the maintenance of the inversion polymorphism present in this species; is discussed.