Cytogenetics of natural populations of Drosophila

D. bipectinata and D. malerkotliana differ from each other by three overlapping inversions in IIL, two included inversions in IIIL and two overlapping inversions in IIIR. These inversions were analysed on the basis of the salivary chromosome maps of D. malerkotliana. Bock's (1971) data revealed that the four members of the bipectinata species complex differ from each other with respect to overlapping inversions. The reason why the ancestral population which may have been heterozygous for common inversions split into at least four groups, each leading to the formation of a new species, and the possible mechanism of the origin of sexual isolation between the groups is discussed.     

Inversion polymorphism in Southeast Asian populations of the Drosophila nasuta subgroup

Heterozygosity for chromosomal arrangements was investigated in four species of the nasuta complex. D. sulfurigaster albostrigata, D. albomicans and D. kohkoa are highly polymorphic whereas D. pulaua is monomorphic. Inversions were identified with the aid of photographic chromosome maps. The geographic distribution and frequencies of inversions detected and their possible phylogenies were discussed. Most inversions in D.s. albostrigata and D. albomicans occur on chromosome IIL. In D. kohkoa there is marked preponderance of inversions on chromosome III. Non-random association of certain inversions was noted. Variation in frequencies of inversions is interpreted as a result of adaptation to local ecogeographic conditions. Shared extant polymorphisms indicate phylogenetic relationships between species.The contents of this paper were incorporated in a Ph.D. thesis accepted by the University of Queensland in 1978. The author's present address is: Unit Genetik, Universiti Kebangsaan Malaysia, Jalan Pantai Baru, Kuala Lumpur, Malaysia.     

Comparative polytene chromosome maps of <Emphasis Type="Italic">D. montana</Emphasis> and <Emphasis Type="Italic">D. virilis</Emphasis>

Chromosomal inversion polymorphism was characterized in Finnish Drosophila montana populations. A total of 14 polymorphic inversions were observed in Finnish D. montana of which nine had not been described before. The number of polymorphic inversions in each chromosome was not significantly different from that expected, assuming equal chance of occurrence in the euchromatic genome. There was, however, no correlation between the number of polymorphic inversions and that of fixed inversions in each chromosome. Therefore, a simple neutral model does not explain the evolutionary dynamics of inversions. Furthermore, in contrast to results obtained by others, no significant correlation was found between the two transposable elements (TEs) Penelope and Ulysses and inversion breakpoints in D. montana. This result suggests that these TEs were not involved in the creation of the polymorphic inversions seen in D. montana. A comparative analysis of D. montana and Drosophila virilis polytene chromosomes 4 and 5 was performed with D. virilis bacteriophage P1 clones, thus completing the comparative studies of the two species.     

Chromosomal Evolution of Sibling Species of the Drosophila willistoni Group. I. Chromosomal Arm IIR (Muller’s Element B)

The phylogenetic relationships among nine entities of Drosophila belonging to the D. willistoni subgroup were investigated by establishing the homologous chromosomal segments of IIR chromosome, Muller’s element B (equivalent to chromosome 2L of D. melanogaster). The sibling species of the D. willistoni group investigated include D. willistoni, D. tropicalis tropicalis, D. tropicalis cubana, D. equinoxialis, D. insularis and four semispecies of the D. paulistorum complex. The phylogenetic relationships were based on the existence of segments in different triads of species, which could only be produced by overlapping inversions. Polytene banding similarity maps and break points of inversions between species are presented. The implications of the chromosomal data for the phylogeny of the species and comparisons with molecular data are discussed. The aim of this study is to produce phylogenetic trees depicting accurately the sequence of natural events that have occurred in the evolution of these sibling species. Claudia Rohde, Ana Cristina Lauer Garcia: These authors contributed equally to this work     

Recombination between heterozygous inversions in Drosophila ananassae

The rate of recombination between linked inversions of the third chromosome of Drosophila ananassae has been investigated by means of the salivary gland smear technique. Different homozygous strains of the species were utilised during the present investigation. The data show that the crossover rate between heterozygous inversions of the third chromosome of D. ananassae varies among different strains. This suggests that recombination between heterozygous inversions is influenced by genic (strain) factors.     

Intra- and interspecific chromosomal inversions in the Drosophila bipectinata species complex

Twenty autosomal inversions were detected in the polytene chromosomes of larvae obtained by hybridizing inversion-free strains of the species of the bipectinata complex (D. bipectinata, D. parabipectinata, D. malerkotliana and D. pseudoananassae). Twenty autosomal inversions are also known as extant polymorphisms in these species; fifteen (possibly sixteen) of these inversions are different from those detected in the interspecific hybrids. The available evidence permits reconstruction of chromosome phylogenies deriving malerkotliana, pseudoananassae and a population ancestral to both bipectinata and parabipectinata directly from a common ancestral population. The results of the study support the Carson hypothesis of transitional homoselection during the processes of speciation.Part of this study was incorporated in a section of a thesis submitted for the degree of Doctor of Philosophy in the University of Queensland, Australia; the work was continued under support by a U.S. Public Health Service Research Grant No. GM-11609 from the National Institute of General Medical Sciences to Prof. M. R. Wheeler, University of Texas.     

Distribution of genetic diversity in relation to chromosomal inversions in the malaria mosquito Anopheles gambiae

The epidemiology of malaria in Africa is complicated by the fact that its principal vector, the mosquito Anopheles gambiae, constitutes a complex of six sibling species. Each species is characterized by a unique array of paracentric inversions, as deduced by karyotypic analysis. In addition, most of the species carry a number of polymorphic inversions. In order to develop an understanding of the evolutionary histories of different parts of the genome, we compared the genetic variation of areas inside and outside inversions in two distinct inversion karyotypes of A. gambiae. Thirty-five cDNA clones were mapped on the five arms of the A. gambiae chromosomes with divisional probes. Sixteen of these clones, localized both inside and outside inversions of chromosome 2, were used as probes in order to determine the nucleotide diversity of different parts of the genome in the two inversion karyotypes. We observed that the sequence diversity inside the inversion is more than threefold lower than in areas outside the inversion and that the degree of divergence increases gradually at loci at increasing distance from the inversion. To interpret the data we present a selectionist and a stochastic model, both of which point to a relatively recent origin of the studied inversion and may suggest differences between the evolutionary history of inversions in Anopheles and Drosophila species.Correspondence to: K.D. Mathiopoulos     

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.     

A comparative study of the chromosomal polymorphs in the incipient species of the Drosophila paulistorum complex

Ninety-six geographical strains distributed among the incipient species of the Drosophila paulistorum complex were examined cytologically, and the results obtained were correlated with available data on hybridization tests and chromosomal analysis. The complex was found to contain more than sixty-three different inversions, out of which thirty-two were 3rd chromosome configurations. This placed Drosophila paulistorum among the most chromosomally polymorphic species in the genus. The species differs from D. willistoni, in that a great number of inversions is concentrated in one of the chromosomes, as opposed to approximately equal distribution of inversions in the chromosomes of willistoni. — The data obtained in the course of this investigation seem to support the idea that either massive populations become isolated and then form new species, or that the newly forming species tend to retain some of their ancestral polymorphs which might present them with heterotic effects, gradually replacing them with more successful combinations as speciation progresses.The work reported in this article has been carried under Contract No. AT (30-1)-3096, U. S. Atomic Energy Commission.     

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.     

Genome‐wide tests for introgression between cactophilic Drosophila implicate a role of inversions during speciation

Models of speciation‐with‐gene‐flow have shown that the reduction in recombination between alternative chromosome arrangements can facilitate the fixation of locally adaptive genes in the face of gene flow and contribute to speciation. However, it has proven frustratingly difficult to show empirically that inversions have reduced gene flow and arose during or shortly after the onset of species divergence rather than represent ancestral polymorphisms. Here, we present an analysis of whole genome data from a pair of cactophilic fruit flies, Drosophila mojavensis and D. arizonae, which are reproductively isolated in the wild and differ by several large inversions on three chromosomes. We found an increase in divergence at rearranged compared to colinear chromosomes. Using the density of divergent sites in short sequence blocks we fit a series of explicit models of species divergence in which gene flow is restricted to an initial period after divergence and may differ between colinear and rearranged parts of the genome. These analyses show that D. mojavensis and D. arizonae have experienced postdivergence gene flow that ceased around 270 KY ago and was significantly reduced in chromosomes with fixed inversions. Moreover, we show that these inversions most likely originated around the time of species divergence which is compatible with theoretical models that posit a role of inversions in speciation with gene flow.     

Chromosomal polymorphism in two species of the guarani group of drosophila

Summary Studies of chromosomal polymorphism in natural populations of D. guaramunu and D. griseolineata in Rio Grande do Sul, Brazil, confirmed and extended previous findings in these species. The more common D. guaramunu is much more polymorphic than its closest but less common relative D. griseolineata. In the former species, the frequencies of four inversions showed differences from locality to locality, and five inversions of the same species showed temporal changes in the population of Bexiga. It was not possible to correlate the differences with any particular factor in the environment, though the temporal changes were perhaps due to seasonal climatic cycles.Inversion heterosis was not evident in either species — instead, inversion Ee of D. guaramunu was found to be less frequent than expected on the basis of the Hardy-Weinberg equilibrium in the localities of Emboaba, Bexiga and Feliz. The implications of these findings are discussed.Fellow of the Conselho Nacional de Pesquisas.     

Inversion polymorphism in species of the Drosophila nasuta subgroup from Thailand

Thailand populations of three species of the D. nasuta complex have been analysed for the presence of paracentric inversions. D. albomicans and D. sulfurigaster albostrigata were collected from Phuket, Chiang Mai and the River Kwai, whilst D. kohkoa was found only in Phuket and the River Kwai. Chromosomal polymorphism was studied in respect to geographical distribution. The Phuket populations of all three species proved to be highly polymorphic by comparison with the River Kwai and Chiang Mai populations. The heterozygosity frequencies of inversions were calculated and the variations interpreted as a result of adaptation to local ecogeographical conditions. Shared polymorphisms revealed that D. kohkoa and D. s. albostrigata are more closely related to D. albomicans than they are to each other.Based on a thesis submitted for the degree of Ph.D. in the University of Queensland.     

Pervasive gene conversion in chromosomal inversion heterozygotes

Chromosomal inversions shape recombination landscapes, and species differing by inversions may exhibit reduced gene flow in these regions of the genome. Though single crossovers within inversions are not usually recovered from inversion heterozygotes, the recombination barrier imposed by inversions is nuanced by noncrossover gene conversion. Here, we provide a genomewide empirical analysis of gene conversion rates both within species and in species hybrids. We estimate that gene conversion occurs at a rate of 1 × 10^–5 to 2.5 × 10^–5 converted sites per bp per generation in experimental crosses within Drosophila pseudoobscura and between D. pseudoobscura and its naturally hybridizing sister species D. persimilis. This analysis is the first direct empirical assessment of gene conversion rates within inversions of a species hybrid. Our data show that gene conversion rates in interspecies hybrids are at least as high as within‐species estimates of gene conversion rates, and gene conversion occurs regularly within and around inverted regions of species hybrids, even near inversion breakpoints. We also found that several gene conversion events appeared to be mitotic rather than meiotic in origin. Finally, we observed that gene conversion rates are higher in regions of lower local sequence divergence, yet our observed gene conversion rates in more divergent inverted regions were at least as high as in less divergent collinear regions. Given our observed high rates of gene conversion despite the sequence differentiation between species, especially in inverted regions, gene conversion has the potential to reduce the efficacy of inversions as barriers to recombination over evolutionary time.     

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.     

Individual inversions or their combinations: which is the main selective target in a natural population of Drosophila subobscura?

It is generally accepted that chromosomal inversions have been key elements in adaptation and speciation processes. In this context, Drosophila subobscura has been, and still is, an excellent model species due to its rich chromosomal polymorphism. In this species, many analyses from natural populations have demonstrated the adaptive potential of individual inversions (and their overlapped combinations, the so‐called arrangements). However, little information is available on the evolutionary role of combinations generated by inversions located in homologous and nonhomologous chromosomes. The aim of this research was to ascertain whether these combinations are also a target for natural selection. For this objective, we have studied the inversion composition of homologous and nonhomologous chromosomes from a D. subobscura sample collected in a well‐studied population, Mount Avala (Serbia). No significant deviation from H‐W expectations was detected, and when comparing particular karyotypic combinations, likelihood ratios close to 1 were obtained. Thus, it seems that for each pair of homologous chromosomes inversions no deviation from randomness was detected. Finally, no linkage disequilibrium was observed between inversions located in different chromosomes of the karyotype. For all these reasons, it can be assumed that, at the cytological level, the individual inversions rather than their combinations in different chromosomes are the main target of selection.     

How chromosomal rearrangements shape adaptation and speciation: Case studies in Drosophila pseudoobscura and its sibling species Drosophila persimilis

The gene arrangements of Drosophila have played a prominent role in the history of evolutionary biology from the original quantification of genetic diversity to current studies of the mechanisms for the origin and establishment of new inversion mutations within populations and their subsequent fixation between species supporting reproductive barriers. This review examines the genetic causes and consequences of inversions as recombination suppressors and the role that recombination suppression plays in establishing inversions in populations as they are involved in adaptation within heterogeneous environments. This often results in the formation of clines of gene arrangement frequencies among populations. Recombination suppression leads to the differentiation of the gene arrangements which may accelerate the accumulation of fixed genetic differences among populations. If these fixed mutations cause incompatibilities, then inversions pose important reproductive barriers between species. This review uses the evolution of inversions in Drosophila pseudoobscura and D. persimilis as a case study for how inversions originate, establish and contribute to the evolution of reproductive isolation.     

ANTAGONISTIC PLEIOTROPIC EFFECT OF SECOND-CHROMOSOME INVERSIONS ON BODY SIZE AND EARLY LIFE-HISTORY TRAITS IN DROSOPHILA BUZZATII

A simple way to think of evolutionary trade-offs is to suppose genetic effects of opposed direction that give rise to antagonistic pleiotropy. Maintenance of additive genetic variability for fitness related characters, in association with negative correlations between these characters, may result. In the cactophilic species Drosophila buzzatii, there is evidence that second-chromosome polymorphic inversions affect size-related traits. Because a trade-off between body size and larval developmental time has been reported in Drosophila, we study here whether or not these inversions also affect larva-adult viability and developmental time. In particular, we expect that polymorphic inversions make a statistically significant contribution to the genetic correlation between body size (as measured by thorax length) and larval developmental time. This contribution is expected to be in the direction predicted by the trade-off, namely, those flies whose karyotypes cause them to be genetically larger should also have a longer developmental time than flies with other karyotypes. Using two different experimental approaches, a statistically significant contribution of the second-chromosome inversions to the phenotypic variances of body size and developmental time in D. buzzatii was found. Further, these inversions make a positive contribution to the total genetic correlation between the traits, as expected by the suggested trade-off. The data do not provide evidence as to whether the genetic correlation is due to antagonistic pleiotropic gene action or to gametic disequilibrium of linked genes that affect one or both traits. The results do suggest, however, a possible explanation for the maintenance of inversion polymorphism in this species.     

Chromosome inversions in Indian Drosophila melanogaster

Ten laboratory stocks of Drosophila melanogaster initiated from females collected in different localities in India were analysed for chromosome inversions. Six inversions were found to be present, three in 2L, one in 2R, one in 3L and one in 3R. Out of these six inversions, three are new and are being reported for the first time. Furthermore, this is the first report of inversion polymorphism in Indian D. melanogaster. The persistence of inversion polymorphism in our laboratory stocks of D. melanogaster which were maintained for more than one year under laboratory conditions, suggests some heterotic advantage of inversion heterozygotes.     

Limits of the distal inversion in the t complex of the house mouse: Evidence from linkage disequilibria

The suppression of crossing-over and the consequent linkage disequilibrium of genetic markers within the t complex of the house mouse is caused by two large and two short inversions. The inversions encompass a region that is some 15 centiMorgans (cM) long in the homologous wild-type chromosome. The limits of the proximal inversions are reasonably welldefined, those of the distal inversions much less so. We have recently obtained seven new DNA markers (D17Tu) which in wild-type chromosomes map into the region presumably involved in the distal inversions of the t chromosomes. To find out whether the corresponding loci do indeed reside within the inversions, we have determined their variability among 26 complete and 12 partial t haplotypes. In addition, we also tested the same collection of t haplotypes for their variability at five D17Leh, Hba-ps4, Pim-1, and Crya-1 loci. The results suggest that the distal end of the most distal inversion lies between the loci D17Leh467 and D17Tu26. The proximal end of the large distal inversion was mapped to the region between the D17Tu43 and Hba-ps4 loci, but this assignment is rather ambiguous. The loci Pim-1, Crya-1, and the H-2 complex, which have been mapped between the Hba-sp4 and Grr within the large distal inversion, behave as if they recombine from time to time with their wildtype homologs.