Inversion Heterozygotes Research Articles

Apparent Incipient speciation in the midge Chironomus oppositus Walker (Diptera: Chironomidae)

Field collections of Chironomus oppositus from certain localities in Tasmania, in particular from Bellerive, consistently show distributions of inversions different to those found in the normal form, which is referred to as form A and occurs in mainland Australia and most other Tasmanian populations. These collections showed: (1) a marked deficiency of almost all inversion heterozygotes; (2) significant groups of associated sequences which can be used to define two additional forms, referred to as form B and form C. Since forms B and C have so far only been found together, it would appear that this represents an unusual situation in insect speciation. This karyotypic divergence must be maintained by some restriction on interbreeding, both between these two groups and also between them and form A, with which they appear to coexist in some localities.

Somatic pairing and meiotic nonrandom disjunction in a pericentric inversion of Hylemya antiqua (Meigen)

An asymmetrical pericentric inversion in the onion fly, Hylemya antiqua was studied. Somatic pairing was studied in young eggs from test-and sibcrossed inversion heterozygous females which gave four and seven distinguishable karyotypes respectively. From these seven, three are balanced: the normal type, the inversion heterozygote and homozygote, and four are unbalanced recombinant karyotypes descending from crossovers in the loop. In all types at all mitotic stages the centromeres are paired. The telomeres only show association during prophase but this decreases from mid to late prophase. Quantitative analysis of the four different crossover products as produced by inversion heterozygous females showed the presence of nonrandom disjunction. A significant disparity was observed, viz. the normal chromosome was taken up preferentially into the functional gamete compared to the inverted chromosome. Dragging of long chromatids in the asymmetric dyad during M I-A I is a possible explanation of this feature.

X-ray induced pericentric inversions in Anopheles albimanus.

Sixteen different pericentric inversions, ten on chromosome 2 and six on chromosome 3, have been isolated and characterized. The partial sterility in the inversion heterozygotes ranged from about 28 to 50%. Contrary to theoretical considerations, a curvilinear relationship exists between inversion length and partial sterility, whereby a reduction in sterility was noted for progressively longer inversions. The break-points are distributed randomly over the autosomes, but are observed more frequently in the areas of the salivary gland chromosomes where diffuse and broken bands of variable stainability are located.

ENZYME AND CHROMOSOME POLYMORPHISMS IN JAPANESE NATURAL POPULATIONS OF DROSOPHILA MELANOGASTER

Collections of D. melanogaster from Japanese populations were analyzed for enzyme and chromosomal polymorphisms. Allelic frequencies at the Adh and alphaGpd loci were compared with polymorphic inversion (In(2L)B, In(2R)C) frequencies in the second chromosome. There was a significant positive correlation between the frequencies of AdhS and In(2L)B, caused by linkage. On the other hand, inversion-free cage populations maintained in the laboratory for a long time showed considerably larger variation in the frequencies of these enzyme alleles, which seem very likely to be a consequence of random drift. Two fitness components of these enzyme and chromosomal variants were measured in two different environmental conditions; neither of the two loci showed heterozygote superiority in viability or productivity, while the inversion heterozygotes showed a superior productivity compared to the corresponding homozygotes in the fluctuating environment. These findings are compatible with the hypothesis that polymorphic isozyme genes are maintained by random drift of neutral genes in natural populations, and that association with linked inversions is a historical accident.

Direct correlation between a chromosome puff and the synthesis of a larval saliva protein in Drosophila melanogaster

The structural gene Sgs-4 responsible for larval saliva protein 4 of Drosophila melanogaster was localized, with the help of Notch deficiencies, within the section between bands 3C10 and 3D1 of the X chromosome. In this chromosome section there is, very probably, only one fine band. In the third larval instar chromosome this section is transcriptionally active and forms a puff. When the ecdysone concentration increases, about 5 h before prepupa formation, it becomes inactive.--In section 3C of X chromosomes of third instar larvae of the stock Hikone-R no puff is formed. The saliva of these larvae lacks protein 4. However, female hybrids (H/B and H/O) from Hikone-R crossed with Berlin and Oregon respectively produce a Hikone-specific saliva protein 4h. The synthesis of protein 4h in the hybrids H/B and H/O is ascribed to an activation of the gene Sgs-4 in the Hikone chromosome.--In the saliva of heterozygotes (FM1/H) carrying one inversion chromosome In(1)FM1 and one X chromosome from Hikone, protein 4h could not be detected. In these inversion heterozygotes in 90% of all nuclei the homologues are not paired in 3C, and 3C is puffed only in the FM1 chromosome. This suggests that a precondition for the activation of Hikone gene Sgs-4 in heterozygotes may be intimate homologue pairing.--Intersexes with one of their X chromosomes from Hikone-R and the other from Berlin produce relatively more protein 4h than do diploid H/B females, indicating facilitated transcription as a result of dosage compensation.

The meiotic behaviour of inversions in polyploid aloineae

In addition to the four classical inversion phenomena, meiosis in tetraploid paracentric inversion heterozygotes produces multiple dicentric and complex tricentric bridges which were previously little understood. Also formed are open loop chromatids which can give rise to dicentric chromosomes in the progeny. A qualitative and quantitative study of the first and second meiotic division in Gasteria nigricans var. crassifolia (Liliaceae, Aloineae) agrees closely with theoretical considerations. Breakage of dicentric bridges results in the formation of chromosomes carrying large terminal deletions. These are shown to be viable in the diploid gametes produced by tetraploids because of the buffering effect of the second haploid set of chromosomes.

Geographical variability in the pericentric inversion system of the grasshopper Trimerotropis pseudofasciata.

Island and mainland populations of Trimerotropis pseudofasciata from California were compared with respect to the nature and extent of their percentric inversion systems. Island populations generally have more chromosomes polymorphic for centromere position than mainland populations and a considerably higher percentage of the genome in these island populations is in a structurally heterozygous state. Thus, although geographically peripheral, the islands provide habitats capable of supporting denser and more chromosomally polymorphic populations than the mainland. Chiasmata are generally localized to terminal positions in all classes of chromosomes and do not occur in the inverted regions of inversion heterozygotes. Chiasma frequency is highest in inversion homozygotes. It is hypothesized that the inversion system in T. pseudofasciata serves the dual synergistic function of preserving allelic sequences in the inversion region intact through inversion heterozygosity and limiting the generation of variability in regions outside the inversion by increasing terminal chiasmata. Additionally, it is argued that it is the gene sequence on only the inversion chromosome that is important in Trimerotropis. This condition contrasts with the "co-adapted" pattern seen in Drosophila where the gene sequences on both chromosomes in the inversion heterozygote are simultaneously important.

The mitotic, polytene, and meiotic chromosomes of Drosophila ananassae.

The mitotic chromosome complement of D. ananassae consists of four structurally distinguishable submetacentric pairs and all four have been identified with their linkage groups. For the polytene chromosome complement of six arms representing the X, second and third chromosomes, an improved reference map has been constructed and used to describe selected cytogenetically useful rearrangements. In meiotic prophase of spermatocytes, chromosomes 2 and 3 form pachytene-diplotene bivalents whose arms may be associated by chiasmata in postdiplotene stages, but the X, Y and fourth chromosomes participate in a complex multivalent. No correlation was detected between meiotic chromosome behavior and specific genes that regulate crossing over in males. In male inversion heterozygotes having high levels of genetically monitored crossing over, no unequivocal evidence was found for formation of either pachytene inversion loops or anaphase bridges and fragments.

Inversion heterozygosity and the origin of XO daughters of Bpa/+female mice.

THERE has long been an interest in developing mouse stocks carrying chromosome inversions for mutation testing. This interest stems from the fact that heterozygosity for a paracentric inversion, that is, a structural rearrangement in which a chromosome segment that does not include the centromere is rotated through 180°, results in suppression of recombination in the inversion region. This is caused by the failure of recovery of the products of single crossovers in this region, because dicentric chromatids and acentric fragments are produced that either fail to give functional meiotic products or result in the formation of unbalanced zygotes which are generally eliminated. Recombination between the pair of chromosomes concerned is, therefore, confined to any crossovers in the non-inverted regions and to the rare two-strand double crossovers which may occur within the inversion region if it is a long one. This property of inversion heterozygotes enables the recovery, in the progeny, of the structurally normal homologue largely intact and any recessive mutation located on it can be readily detected if suitable genetically marked stocks are used. In the simplest case, when the mutation is a recessive lethal and the inversion is located in the X chromosome, detection is either by the absence of half the males, or if the inversion itself is marked by a recessive lethal (as in the C1B method devised by Muller for Drosophila melanogaster), by the absence of all the males.

MARGINAL POPULATIONS OF CEPAEA NEMORALIS (L.) ON THE BRENDON HILLS, ENGLAND. II. VARIATION IN CHIASMA FREQUENCY.

In different species genetic recombination and the release of variation may be regulated in different ways and at different levels of organization since the components of the control system do not necessarily act in the same direction (e.g., Grant, 1958). For example, in herbaceous plants short generation times promote the release of variability and are often associated with low chromosome numbers: a restrictive device (Grant, 1958). The recombination system within a population may similarly be adjusted so that there is a balance between immediate fitness and long-term adaptability (Carson, 1955a). In populations of an outbreeding organism an important level of genetic control may be through the regulation of chiasma frequency since, given sufficient heterozygosity, a raised chiasma frequency will lead to an increase in the range of gametic genotypes. Differences in chiasma frequencies between populations are therefore possibly adaptive, perhaps reflecting differing ecological circumstances under which these populations exist. In Drosophila the frequency of inversion heterozygotes, in which crossing over is restricted, is important in determining the level of recombination within a population. In certain species, particularly D. robusta and D. willistoni, the amount of inversion heterozygosity decreases as the margins of the species' ranges are reached. In a series of papers (da Cunha et al., 1950; Townsend, 1952; da Cunha et al., 1959) the view was advanced that the degree of chromosomal polymorphism is a function of the variety of ecological niches in the territory which a population inhabits. Carson (1955a, b, 1956, 1964), however, suggested that greater chromosomal homozygosity at the margins serves to allow more recombination which is necessary to provide sufficient flexibility for adjustment to suboptimal conditions. He has also shown (Carson, 1958) that the response to selection in strains originating from marginal populations is greater than that in strains originating from central ones, perhaps reflecting the occurrence of more recombination in the former populations. A completely different situation occurs in the grasshopper Myrmeleotettix maculatus. The presence of B chromosomes has been shown to raise both the frequency and the variance of chiasmata in those individuals which contain them (Barker, 1960; Hewitt and John, 1967). The frequency of B-containing individuals varies between populations and it has been shown that this variation is related to climatic factors such as temperature and rainfall (e.g., Barker, 1966, Hewitt, 1973). Central populations in favorable (warm, dry) environments possess more B chromosomes and have higher chiasma frequencies than more marginal populations in stringent (colder, wetter) localities which have no B chromosomes. A comparable situation may occur in the grouse locust Tettigidea lateralis where Fontana and Vickery (1973) found that the effect of B chromosomes in a marginal population was to change chiasma position with the net effect of depressing recombination. Cepaea nemoralis (L.) has a haploid number of 22 chromosomes (Perrot, 1938). There is a large metacentric pair forming the A group, a medium sized pair, the B

Chiasma studies in structural hybrids IX. Crossing-over in pericentric inversion ofScilla scilloides

InScilla scilloides (Lindle) Druce, the heterozygotes for a pericentric inversion were found to be predominant in a small natural population consisting of cytogenetic type BB (2n=18). Pericentric inversion may include about half the length of the original subtelocentric chromosome, changing it to submetacentric. The 9II were always formed in these heterozygotes as well as in normal plants at MI in PMCs. A single chiasma was formed in the shorter one of two inverted segments divided by the kinetochore at MI, while one or two inversion chiasmata were observed in the longer segment. The AI separation was always regular. Since both arms of a normal chromosome and those of an inverted one were clearly distinguishable from one another at AI and AII, two kinds of crossover chromatids could be identified. Both sides of the single inversion chiasma always opened out reductionally. The frequency of bivalent without inversion chiasma agreed statistically with that of half-bivalent at AI or chromatid structure at AII, which resulted from non crossing-over within the inverted segment. Likewise, no statistical difference was found between the frequency of a single chiasma and that of a single crossing-over product in a longer inverted segment. These findings have clearly proved that the chiasma is a consequence of genetic crossing-over. The average proportion of good pollen grains in the inversion heterozygotes, 53.6%, amounted to about half that of normal plants, 97.7%.

Inversion polymorphism in a two-locus genetic system.

SUMMARYThe types of equilibria possible with an inversion in a two-locus system are considered, and their stability properties investigated. With complete suppression of crossing-over in inversion heterozygotes, there are three possible types of stable equilibria; which of these is reached by a new inversion depends on the fitness effects of the two loci concerned. With one of these equilibria, basically involving cumulative overdominance of the selected loci, the inverted and standard sequences are genetically homogeneous and differ with respect to both loci. With the other types of equilibrium, the standard sequence remains heterogeneous for one or both loci. It is shown that this situation may lead to variations in karyotypic fitnesses when the inversion is changing in frequency. It is also found that, with certain fitness relationships, two alternative stable equilibria may coexist; the final frequency reached by an inversion may therefore depend on the population's history.The effects of double crossing-over in inversion heterozygotes were also investigated, and it was shown that the equilibria with double crossing-over are closely related to the corresponding equilibria without it, except that both sequences are more heterogeneous genetically. Within each sequence there is almost complete linkage equilibrium between the selected loci, although both are in linkage disequilibrium with the inversion itself. It was also found that, with double crossing-over, the population tends to remain for many thousands of generations in a state of quasi-equilibrium. In this state, the inversion tends not to return to its original frequency after a perturbation; also, it may remain for a long time relatively homogeneous genetically, especially when rare.These results were compared with those from experiments and observations on inversion polymorphisms.

Exchange within heterozygous inversions in Drosophila melanogaster.

The exchange behavior of non-attached, whole arm, X chromosome inversions was reexamined using nondisjunction in XXY females as an indirect measure of the frequency of nonexchange tetrads. Crossing over is quite normal in these inversion heterozygotes and is independent of the arrangement of the basal heterochromatin.

The genetic structure of natural populations of Drosophila melanogaster. XI. Genetic variability in a local population.

Six hundred and ninety-one second chromosomes were extracted from a Raleigh, North Carolina population, and the following experimental results were obtained: (1) Salivary gland chromosomes of all lines were observed and the number of inversion-carrying chromosomes was 130, among which 76 carried In(2R)NS, 36 carried In(2L)t, 4 carried In(2L)t and In(2R)NS, and 14 carried different kinds of rare inversions. (2) Viabilities of homozygotes and heterozygotes were examined. The frequency of lethal-carrying chromosomes was 275/691 (or 0.398):70/130 (or 0.538) in inversion-carrying chromosomes and 205/561 (or 0.365) in inversion-free chromosomes. The former is significantly higher than the latter. The average homozygote viability was 0.4342 including lethal lines and 0.7163 excluding those, the average heterozygote viability being 1.0000. The detrimental load to lethal load ratio (D:L ratio) was 0.334/0.501 = 0.67. The average viability of lethal heterozygotes was less than that of lethal-free heterozygotes, significantly in inversion-free individuals but not significantly so in inversion-carrying individuals. Inversion heterozygotes seem to have slightly better viability than the inversion-free heterozygotes on the average, but not significantly so. (3) The average degree of dominance of viability polygenes was estimated to be 0.293 +/- 0.071 for all heterozygotes whose component chromosomes had better viabilities than 0.6 of the average heterozygote viability, 0.177 +/- 0.077 for inversion-free heterozygotes and 0.489 +/- 0.082 for inversion heterozygotes. (4) Mutation rates of viability polygenes and lethal genes were estimated on the basis of genetic loads and average degrees of dominance of lethal genes and viability polygenes. Estimates were very close to those obtained by direct estimation. (5) Possible overdominance and epistasis were detected, but the magnitude must be very small. (6) The effective size of the population was estimated to be much greater than 10,000 by using the allelism rate of lethal-carrying chromosomes (0.0040) and their frequency.-On the basis of these findings and the comparison with the predicted result (Mukai and Maruyama 1971), the mechanisms of the maintenance of genetic variability in the population are discussed.

Gene conversion and transfer of genetic information within the inverted region of inversion heterozygotes.

Prior studies of recombination which monitor exchange events in exceedingly short intervals (i.e., separable sites within a cistron) reveal that the basic event in recombination involves a non-reciprocal transfer of information, termed conversion. As a logical consequence of the model suggested by the work in Drosophila, the present investigation examined recombination between rosy mutant alleles (ry:3-52.0) in Drosophila melanogaster in a paracentric inversion (In(3R)P(18)) heterozygote, which placed the rosy region approximately at the center of the inverted region. Comparison of the results of this study with experiments carried out in standard chromosome homozygotes reveals a dramatic suppression of classical crossovers between the rosy mutant alleles in the inversion heterozygote. However, conversions continue to occur for all rosy mutant alleles in all heterozygous combinations in the inversion heterozygote. Moreover, the order of magnitude of conversion frequencies seen in the inversion heterozygote does not change from that seen in the standard chromosome homozygote study. The significance of these observations with reference to the role of rearrangements as barriers of information transfer is discussed. Particular attention is directed to the elaborate inversion polymorphisms seen in natural populations, and to notions concerning their role in the evolution of adaptive gene complexes.

FERTILITY GENES IN NATURAL POPULATIONS OF DROSOPHILA MELANOGASTER. III. SUPERIORITY OF INVERSION HETEROZYGOTES.

Chromosomal polymorphism in natural populations is largely maintained by the adaptive superiority of inversion heterozygotes. Dobzhansky and his co-workers have carried out many studies on heterosis in Drosophila pseudoobscura populations (summarized in Dobzhansky, 1970). The superior fitness of heterokaryotypes has also been reported in other Drosophila species: D. persimilis (Spiess, 1958; Spiess and Langer, 1964); D. robusta (Carson, 1958; Prakash, 1967); D. willistoni (da Cunha et al., 1950; Pavan et al., 1957); D. ananassae (Tobari, 1962) and D. pavani (Brncic et al., 1969). Extensive chromosomal polymorphism in Japanese populations of D. melanogaster was demonstrated by Watanabe (1967). Two inversions on the second chromosome and four inversions on the third chromosome which had been found all over the world were highly polymorphic in Japanese natural populations. The second chromosome inversion In(2L)B was maintained in the population year after year at a frequency of about 35%. A higher adaptive value of the inversion heterozygotes was expected from estimates of the pre-adult viability. However, superiority was found only when In(2L)B was combined with another inversion, In(2R)C. The viability of the heterozygotes for In(2L)B and standard chromosomes was the same as that of the standard heterozygotes (Watanabe et al., 1964). A significant superiority of this inversion heterozygote in female

MAINTENANCE OF CHROMOSOMAL POLYMORPHISM IN A POPULATION OF DROSOPHILA PSEUDOOBSCURA. II. FECUNDITY, LONGEVITY, VIABILITY AND COMPETITIVE FITNESS.

Superiority of inversion heterozygotes over corresponding homozygotes is generally believed to be a major mechanism for maintaining chromosomal polymorphism in populations of D. pseudoobscura. Differential egg-to-adult survival in favor of the inversion heterozygotes has been postulated as a key component of this heterozygote superiority (Dobzhansky, 1947). Chromosomal polymorphism involving AR and CH gene arrangements has persisted in a cage population (No. 173) at 25 C since 1957 (Beardmore et al., 1960; Dobzhansky and Pavlovsky, 1961; Levine and Van Valen, 1964; Druger, 1966; Druger and Nickerson, 1972). Two independent analyses of this population revealed no significant advantage of inversion heterozygotes over homozygotes in egg-to-adult viability (Druger, 1966; Druger and Nickerson, 1972). This finding does not exclude heterozygote superiority as a mechanism for maintaining the polymorphism, since such superiority may operate in other ways. To investigate this possibility, studies of fecundity, longevity, and viability were conducted on AR/AR, CH/CH and AR/CH flies derived from AR and CH strains that were re-isolated from population No. 173. In addition to evaluating these individual components of fitness, a comparison of the fitness of polymorphic (AR + CH) and monomorphic (AR/AR) and (CH/CH) populations was obtained through competition with a standard population of a non-interbreeding species (Claringbold and Barker, 1961; Barker, 1963). D. nebulosa was used as a competitor for D. pseudoobscura (Barker, 1965).

A model for somatic pairing derived from somatic crossing over with third chromosome rearrangements in Drosophila melanogaster

X-ray induced crossing-over between the left arms of third chromosome pairs heterozygous for rearrangements was used to measure the somatic pairing of these arms. mwh spots were scored in the wing blades. A significantly reduced number of crossover spots is found in flies heterozygous for inversions or translocations located in the 3L arm. This decrease from control frequencies was experimentally demonstrated to be due to inviability of some crossover spots which are aneuploid as a result of crossing-over within the inverted sequence or between the translocation piece and its centromere. By the same token, some euploid crossover spots are produced by crossing-over outside of the inverted region or between the translocation breakpoint and the mwh locus. Thus, these results are evidence that the euchromatic non-centric portions of the 3L arms are somatically paired in the presence of rearrangements. A model of somatic pairing in which chromosomes are normally found in a “hair pin” configuration is proposed to account for these results and for some previous results with X-chromosomes which indicated that inversion heterozygotes did not pair somatically.

Are dicentric anaphase bridges formed by somatic recombination in X chromosome inversion heterozygotes of Drosophila melanogaster?

Mitotic recombination has been induced with X-rays in Drosophila melanogaster larvae and assayed later as twin mosaic spots on the adult tergites. With the use of the In(1)sc 4L sc 8R chromosome which lacks the nucleolar organizer and is marked with yellow (y) indirect evidence was obtained that mitotic recombination between ring and rod chromosomes results, in a majority of cases, in XO spots, bearing the rod-X only. This was concluded from the relative scarcity and small sizes of y NO- spots (uncovering the sc 4 sc 8 chromosome), compared to control sisters bearing an extra Y chromosome with its NO locus. Thus, dicentric chromatid bridges formed by mitotic recombination between the ring and rod chromosomes are probably eliminated at the next division. In In(1)sc 4 sc 8/f36a (rod/rod) females, no effect of the Y chromosome on the frequency and sizes of cross-over spots was observed. Either any dicentric chromatid bridges formed by recombination between inverted rod chromosomes fragment at division, with a centromeric piece going to each pole, or such bridges are not usually formed by recombination. The latter case would indicate that somatic pairing of homologues is not accurate in X chromosome inversion heterozygotes and consequently, that recombination yields aneuploid cells. Additional studies are cited which indicate that X chromosome heterozygotes for entire arm inversions may not pair in the typical loop at the time of mitotic recombination.

MAINTENANTE OF CHROMOSOMAL POLYMORPHISM IN A POPULATION OF DROSOPHILA PSEUDOOBSCURA: VIABILITY UNDER CROWDED AND UNCROWDED CONDITIONS.

Numerous studies have shown that stable equilibria are usually attained when Drosophila pseudoobscura flies of similar geographic origin but having different gene arrangements in their third chromosomes are bred in population cages at 25 C (Dobzhansky, 1947a; Levene et al., 1954). Superiority of inversion heterozygotes over corresponding homozygotes has been cited as a major factor in attainment of such equilibria. Dobzhansky (1 947b) analyzed several experimental populations at equilibrium to determine the stage of the life cycle when selection was occurring. He found a significant excess of inversion heterozygotes and a deficiency of homozygotes among adult flies that developed under crowded cage conditions compared to Hardy-Weinberg expectations. This result indicated differential mortality between egg and adult stages favoring inversion heterozygotes. Druger (1966) analyzed an experimental cage population (No. 173) in which polymorphism for Arrowhead (AR) and Chiricahua (CH) inversions had persisted for more than eight years. Significant differential mortality in favor of inversion heterozygotes was not observed. In the present study, this analysis was repeated when population No. 173 was more than ten years old, using a larger sample, and deliberately overcrowding food cups with eggs. This was part of an attempt to determine those factors contributing to the longterm maintenance of polymorphism.