Chromosome Studies in Wild Populations of DROSOPHILA MELANOGASTER. II. Relationship of Inversion Frequencies to Latitude, Season, Wing-Loading and Flight Activity

In the midwestern and eastern U.S. populations of Drosophila melanogaster, the Standard gene arrangements show higher frequencies in the north than in the south. In a Missouri population, and to a lesser extent in a south Texas population, the frequencies of Standard chromosomes regularly rise during the cold season and drop during the warm season, thus paralleling the north-south frequency differences. In the Missouri population in 1976 and 1978, wild males were tested for their ability to fly to bait at different ambient temperatures. In both years, males flying in nature in the temperature range of 13° to 15° showed significantly higher frequencies of Standard chromosomes than did those flying in the 16° to 28° range. Wild males flying at 13° to 15° also have different thorax/wing proportions and significantly lower wing-loading indices than do those flying at 16° to 28°. Moreover, wild flies homozygous Standard in 2R and/or 3R have significantly lower wing-loading indices than flies carrying inversions in these arms. Thus, wild flies with high frequencies of Standard chromosomes are karyotypically northern, are selectively favored during the cold season, have a relatively low wing-load and are most capable of flying at critically low ambient temperatures.—In summary, in Missouri, presence or absence of the common cosmopolitan inversions is an important factor in low temperature adaptation, and at least part of the adaptive mechanism involves control of thorax/wing proportions and thus control of wing-loading.     

High Fitness of Heterokaryotypic Individuals Segregating Naturally within a Long-Standing Laboratory Population of Drosophila silvestris

Natural populations of Drosophila silvestris are polymorphic for inversions in one or more of four of the five major chromosome arms; laboratory stocks tend to retain this heterozygosity. A laboratory stock, U28T2, was started from a single naturally inseminated wild female caught at Kilauea Forest Reserve, Hawaii, in January 1977. Polytene analysis in 1980 showed the presence of three natural inversions in chromosome 4: k ² is distal, t is central and l² is proximal. The inversions are short but only short uncovered euchromatic sections exist at the distal and proximal ends. Periodic examinations through 1986 showed all three inversions to be persistent at moderately high frequencies. In 1984, a series of tests of mating performance of caged, mature males, taken at random as they eclosed from the stock, were followed by cytological testcrosses to females from a homokaryotypic stock. Only three of the eight possible haplotypes, k²/t/+ (A), +/+/l² ( a) and +/+/+ (a') were present. Tests of crossing over show none in males; in females, there is about 1% in each of the two regions between the inversions. Only one such apparent crossover haplotype was found among 1084 examined in samples from this stock. Thus, chromosome arrangements A, a and a' virtually behave as wholechromosome alleles in both sexes. Of 146 males marked and tested in cages, 61 produced progeny; the others failed to reproduce. Of 58 males and 80 females producing progeny and analyzed cytologically, there were, respectively, 49 and 59 heterokaryotypes. On the basis of frequencies calculated for fertilized eggs, 33.6 males and 46.3 females are expected. The facts suggest that individual males with the Aa karyotype are particularly successful in production of offspring. Adult females show an excess of Aa' as well as Aa. Such high fitness of heterokaryotypes in the effective breeding adults could be a major factor in the maintenance of stable chromosomal polymorphisms both in laboratory stocks and in nature. Although some of this heterosis is clearly ascribable to differential survival, the facts suggest that there is a substantial opportunity, indeed a likelihood, for a contribution from differential mating among surviving adults.     

Enzymes and Reproduction in Natural Populations of DROSOPHILA EURONOTUS

Populations of Drosophila euronotus, one from southern Louisiana )3 samples), and one from Missouri (2 samples), were classified for allele frequencies at alkaline phosphatase (APH) and acid phosphatase (ACPH) loci. The two populations differed consistently in allele frequencies at both loci. The APH locus is on the inversion-free X chromosome; the chromosomal locus of the autosomal ACPH is unknown, and could involve inversion polymorphism. Wild females from Missouri and Louisiana populations heterozygous at the APH locus carried more sperm at capture than did the corresponding homozygotes. This heterotic association was significant for the combined samples, and whether it was the result of heterosis at the enzyme locus studied, or due to geographically widespread close linkage with other heterotic loci, it should help to maintain heterozygosity at the APH locus. In a Louisiana collection which included large numbers of sperm-free females, simultaneous homozygosity at both enzyme loci was significantly associated with lack of sperm. It is suggested that the latter association is the result of young heterozygous females achieving sexual maturity earlier than do the double homozygotes. The average effective sperm load for 225 wild females was only 29.4, suggesting the necessity for frequent repeat-mating in nature to maintain female fertility. A comparison of the sex-linked APH genotypes of wild females with those of their daughters indicated that among 295 wild-inseminated females from five populations, 35% had mated more than once, and of this 35%, six females had mated at least three times. Because of ascertainment difficulties, it is clear that the true frequency of multiple-mating in nature must have been much higher than the observed 35%. Laboratory studies indicate that multiple-mating in this species does not involve sperm displacement, possibly due to the small number of sperms transmitted per mating, and the fact that the sperm receptacles are only partially filled by a given mating.     

Darwinian fitness and adaptedness in experimental populations of Drosophila willistoni

Fifteen second chromosomes were extracted from Drosophila willistoni flies collected in four natural populations. The adaptedness of populations homozygous for each chromosome was measured by average population size and productivity. Six control populations were established with mixtures of the wild second chromosomes. The Darwinian fitness of flies homozygous for each wild second ehromosome, and of flies carrying random combinations of these chromosomes, was measured relative to the fitness of flies heterozygous for a wild and a marker chromosome. The Darwinian fitness of homozygotes for each second chromosome relative to the fitness of flies carrying random combinations of the natural chromosomes was then inferred. The estimated loss of fitness on making the natural second chromosomes homozygous was substantial, ranging from 39 to 83 pereent, with an average reduction in fitness of 66 percent. These results with D. willistoni are consistent with those from similar experiments with other drosophila species, and they are compatible with a significant role for heterosis in the maintenance of genetic variability.Populations homozygous for wild chromosomes differ in their adaptedness to the experimental environment. Population size and productivity are correlated, although the correlation is far from complete. Some populations have high productivity and low population size, or vice versa. The control populations, with greater genetic variability, were superior in adaptedness to the average of the single-chromosome populations. The Darwinian fitness and the adaptedness of the genotypes in this experiment were not significantly correlated. It follows that certain measures used by population geneticists, such as genetic load and average Darwinian fitness, cannot be taken as general indices of how well adapted a population is to its environment.This work was supported by U.S. Public Health Service Grant RO1-HDO5055, NSF grant GB-20694 (International Biological Program). AEC contract AT-(30-1) 3096, and PHS Career Development Award K3 GM 37265. The collection of the flies was supported by the Fundacão de Amparo a Pesquisa do Estado de São Paulo, Brazil. The senior author's stay in New York, where the experiments were conducted, was financed in part by Research Fellowship 2-12861 from the Panamerican Union.     

Homozygous and Hemizygous Viability Variation on the X Chromosome of DROSOPHILA MELANOGASTER

We report here a study of viability inbreeding depression associated with the X chromosome of Drosophila melanogaster. Fifty wild chromosomes from Mt. Sinai, New York, and 90 wild chromosomes from Death Valley, California, were extracted using the marked FM6 balancer chromosome and viabilities measured for homozygous and heterozygous females, and for hemizygous males, relative to FM6 males as a standard genotype. No statistically significant female genetic load was observed for either chromosome set, although a 95% confidence limit estimated the total load <0.046 for the samples pooled. About 10% of the Death Valley chromosomes appear to be "supervital" as homozygotes. There is little evidence for a pervasive sex-limited detrimental load on the X chromosome; the evidence indicates nearly identical viability effects in males and homozygous females excluding the supervital chromosomes. The average degree of dominance for viability polygenes is estimated between 0.23 to 0.36, which is consistent with autosomal variation and implies near additivity. We conclude that there is little genetic load associated with viability variation on the X chromosome and that the substantial reduction in total fitness observed for chromosome homozygosity in an earlier study may be due largely to sex-limited fertility in females.     

Genetic Load and Viability Distribution in Central and Marginal Populations of DROSOPHILA SUBOBSCURA

Relative viabilities of individuals homozygous or randomly heterozygous for wild O chromosomes derived from a marginal (Norwegian) and a central (Greek) population of D. subobscura were obtained by means of a newly prepared marker strain. In the central and marginal populations 20.8 and 28.8 percent of all chromosomes proved lethal or semilethal in homozygous condition. Mean viability was higher for +/+ random heterozygotes than for +/+ homozygotes. This remained the case for the marginal, but not for the central populations, after exclusion of the detrimental chromosomes from the calculations. The variances of viabilities were higher for homozygotes than for heterozygotes, but the test crosses with chromosomes from the marginal population had generally higher variances than those with chromosomes from the central population. No correlation was found in either populations between the action of a chromosome in homozygous condition with its action in heterozygous condition. This is interpreted as complete recessiveness of genetic load. The results are discussed in terms of the observed reduction of the inversion polymorphism which is not paralleled by a reduction in enzyme and, as shown here, by reduction in viability variation. It is thought that the heterotic effect of inversions is due to their homeostatic action, which depends less on structural genes than on higher orders of organization due to gene interaction or regulation. Whatever the causes, it is very likely that marginal populations differ from central populations with respect to their genetic system.     

On the degree of genetic divergence in Drosophila ananassae populations transferred to laboratory conditions

Twelve natural populations of Drosophila ananassae were sampled and laboratory populations were derived. All the populations were maintained in food bottles in the laboratory for ten generations by transferring fifty flies (females and males in equal number) in each generation. After ten generations they were analysed chromosomally to determine the frequency of different chromosome arrangements. The results show that there is significant variation in the frequencies of chromosome arrangements and in the level of inversion heterozygosity. Although some of the populations became mo-nomorphic for certain inversions, in general all populations remained polymorphic even after ten generations. The degree of genetic differentiation in the populations after they were transferred to laboratory conditions has been estimated by calculating genetic identity and distance between the initial and final populations based on the differences in chromosome arrangement frequencies. The estimates of I and D suggest that there is considerable variation in the degree of genetic divergence in D. ananassae populations. Some populations have remained unchanged while others have diverged to a considerable extent.     

The effect of X chromosome heterozygosity on the structure of the ribosomal genes in Drosophila melanogaster.

Sucrose gradient analysis of DNA isolated from detergent-pronase lysates of adult flies has been used to look for ribosomal genes not integrated into the DNA of the chromosome in genotypes containing various combinations of inversions having breakpoints in the proximal heterochromatin of the X chromosome. Unintegrated genes are found in females heterozygous for inversions which have one breakpoint between the nucleolus organizer and the centromere. Homozygotes and males do not have unintegrated genes. The results suggest that unintegrated ribosomal genes result from an interaction between homologues having different arrangements of the proximal heterochromatin. In addition, data from a series of stocks carrying duplications of the X heterochromatin provide independent evidence for the size of the DNA on our gradients.     

Fitness of a translocation homozygote in cage experiments with the onion fly,Hylemya antiqua (meigen)

Summary In Hylemya antiqua, a stock homozygous for an autosomal reciprocal translocation was isolated using egg-hatch reduction and karyotype analysis. Sibling translocation homozygous (TT) and heterozygous (T+) females were compared in respect to egg production and longevity. In one full-sib (5 TT and 8 T+ females) significantly higher values for both parameters for T+ than for TT females were scored, in four others (a total of 35 TT and 28 T+ females) no significant differences were found. Cage experiments were started with populations composed of equal numbers of wild type flies (++) and translocation homozygotes. The frequencies of the different karyotypes in three successive, non-overlapping generations, did not suggest substantial differences in fitness between ++ and TT flies. Possible causes of a surplus of T+ individuals found in these experiments are discussed together with the usefulness of the translocation for genetic control of H. antiqua.     

A polymorphism for heterochromatic supernumerary segments in Chorthippus parallelus

Supernumerary heterochromatic segments have been found in the S₈ bivalent of two populations of Chorthippus parallelus. These segments occur both in the heterozygous and the homozygous states. In both populations the frequencies of basic homozygotes, structural heterozygotes and structural homozygotes conform to a Hardy-Weinberg distribution. In the structurally heterozygous and homozygous states there is a significant increase in the chiasma frequency of the bivalents other than the S₈ itself. It is suggested that the adaptive role of these supernumerary segments can be explained in terms of this interchromosomal effect.To Professor J. Seiler in commemoration both of his 80th birthday and his many distinguished years of cytological service.     

Chromosomal Polymorphism in Korean Natural Populations of Drosophila immigrans

ABSTRACT To analyze chromosome inversions of Drosophila immigrans , wild flies were captured from large vineyards located in the suburbs of Yecheon and Gyeongsan from October 1999 to 2001. With the egg samples obtained singly at each of the 799 females of D. immigrans , cytological examinations were carried out for the type and frequency of inversions. Two types of different inversions were found only in the second chromosome. The inversions detected were known to be the cosmopolitan inversion "A" and "B". The mean frequency of inversion A was estimated to be 0.074 in Yecheon and 0.066 in Gyeongsan and that of B was to be 0.026 in Yecheon and 0.021 in Gyeongsan, respectively. In the frequency ratio, inversion A was significantly higher than that of B. The present populations of D. immigrans showed subtle differences from other Korean populations in inversion frequencies. To account for the local variations observed in inversion frequencies, several hypotheses are discussed such as founding event or selective force.     

Lack of correlation between crossing-over and chromosome distance between inversions in Drosophila ananassae

Two linked inversions, AL and ZE, located in the opposite limbs of the second chromosome of Drosophila ananassae are separated from each other by nearly 32% of the total length of the second chromosome. Crossing-over between these inversions when heterozygous was studied in females and males by the salivary-gland smear technique using karyotypically homozygous stocks. The results of recombination experiments show that there is a strong suppression of recombination between inversions when heterozygous, in spite of a large euchromatic distance available for crossing-over between them. Thus there is no correlation between chromosome distance and crossing-over between heterozygous inversions in the second chromosome of D. ananassae when studied cytologically.     

Latitudinal variation in wing size in Drosophila subobscura and its dependence on polygenes of chromosome O

The genetic variability of natural populations of Drosophila subobscura derived from localities situated approximately along a north-to-south diameter through the distribution area of the species was studied. The polygenic and adaptive trait ‘wing size’ shows a continuous clinal reduction from north to south. The comparison between flies homozygous or randomly heterozygous for wild chromosomes showed that heterozygous flies are on an average bigger than homozygous flies and that overdominance exists for increased wing size. The genetic variance proved lower in central than in ecologically marginal populations. From the analysis of left-right asymmetry it could be shown that heterozygous flies are more homeostatic than homozygous flies but no differences appeared between populations. Therefore, lower phenotypic variability in central populations must be due to lower genetic variation. An hypothesis was put forward that normalizing selection eliminates + and-alleles in the central populations; in marginal populations, on the other hand, either + (north) or-(south) alleles are favoured and the genetic variability is augmented.     

The behavioural response of Great Tits to novel environment and handling is affected by the DRD4 gene

Studies have provided inconsistent evidence regarding the effects on behaviour of nucleotide polymorphism at the DRD4 gene. For instance, the DRD4 gene affects exploratory behaviour in some bird species and populations but not in others. Our earlier experiment with a wild Great Tit Parus major population revealed an important impact of the DRD4 gene on behavioural variation during the breeding season. The aim of this study was to clarify these results by measuring individual behavioural differences (exploration and anxiety) in Great Tits under controlled conditions before the beginning of egg‐laying in order to exclude the potential impacts of breeding (egg‐laying, motivation to feed nestlings, the potential effect of a partner) and the natural environment (e.g. the presence of predators). Birds were caught from their natural habitat and their behaviour was tested in a trial room the following morning. Individuals with the CT heterozygous genotype (SNP830) performed more actively in different contexts (visiting a novel object in the trial room and vocal behaviour during handling) compared with homozygotes, and the relationships were consistent in males and females. In light of the results from our previous study (heterozygous males, but not females, had a shorter latency to feed nestlings than CC homozygotes), we conclude that the same DRD4 gene variants affect behavioural responses in a controlled environment and wild contexts in the same directions, but that these relationships are not sex‐specific under standardized conditions.     

A Genetic Analysis of Phototactic Behavior in DROSOPHILA MELANOGASTER I. Selection in the Presence of Inversions

The effectiveness of selection for positive and negative phototactic behavior in populations of Drosophila melanogaster heterozygous for various multiple inversions was compared using the method of realized heritability. Selection in the presence of FM6, SM1 or TM3 alone was as effective as in populations carrying no inversions. However, the presence of FM6 and TM3 together reduced the effectiveness of selection for photopositive behavior and FM6 and SM1 and TM3 restricted the response to selection for negative phototactic behavior. The results are discussed in terms of the organization of genes influencing phototactic behavior in this species.     

Analysis of male recombination in third chromosomes of Drosophila melanogaster

Data on male recombination in twenty third-chromosomal lines of Drosophila melanogaster are presented. Frequencies of female and male recombination have been calculated in seven intervals along the third chromosome. The influence on male recombination (M.R.) exercised by different factors such as population origin (cellar, vineyard), the presence of heterozygous inversions and recessive lethal chromosomes, is analyzed. The results obtained lead to the main conclusion that M.R. is not affected by the presence of heterozygous inversions which reduce female recombination in the same lines. In the light of this effect, the possible mechanism operating on male recombination is discussed. Lethal chromosomes reduce significantly the number of male recombination events as compared with wild chromosomes. We have not obtained significant differences in male recombination frequencies between the cellar and the vineyard lines.     

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.     

An Analysis of Regional Constraints on Exchange in DROSOPHILA MELANOGASTER Using Recombination-Defective Meiotic Mutants

The frequency of crossing over per unit of physical distance varies systematically along the chromosomes of Drosophila melanogaster . The regional distribution of crossovers in a series of X chromosomes of the same genetic constitution, but having different sequences, was compared in the presence and absence of normal genetically mediated regional constraints on exchange. Recombination was examined in Drosophila melanogaster females homozygous for either normal sequence X chromosomes or any of a series of X chromosome inversions. Autosomally, these females were either (1) wild type, (2) homozygous for one of several recombination-defective meiotic mutations that attenuate the normal regional constraints on exchange or (3) heterozygous for the multiply inverted chromosome TM2. The results show that the centromere, the telomeres, the heterochromatin and the euchromatic-heterochromatic junction do not serve as elements that respond to genic determinants of the regional distribution of exchanges. Instead, the results suggest that there are several elements sparsely distributed in the X chromosome euchromatin. Together with the controlling system affected by recombination-defective meiotic mutations, these elements specify the regional distribution of exchanges. The results also demonstrate that the alteration in the distribution of crossovers caused by inversion heterozygosity (the interchromosomal effect) results from the response of a normal controlling system to an overall increase in the frequency of crossing over, rather than from a disruption of the system of regional constraints on exchange that is disrupted by meiotic mutations. The mechanisms by which regional constraints on exchange might be established are discussed, as is the possible evolutionary significance of this system.     

Homozygous-viable pericentric inversions for genetic control of Lucilia Cuprina

Summary The isolation of homozygous-viable pericentric inversions for inclusion in field-female killing (FK) systems in Lucilia cuprina is described. From 7,236 irradiated chromosomes screened, 16 pericentric inversions were isolated. Four of these were viable as homozygotes. One of these, In (3LR) 14, possesses the properties required for inclusion in FK systems (tight linkage of one inversion break-point to the white-eye gene and substantial genetic exchange within the inversion in heterozygous females).     

Somatic synapsis of eu- and heterochromatic regions of Drosophila melanogaster chromosomes

Quantitative cytogenetical analysis has been used to study the synapsis of D. melanogaster neuroblast mitotic chromosomes from normal females, flies with heterozygous deletions, duplications or inversions in the heterochromatic regions of chromosome 2 and in triploid females. In all these genotypes chromocentric fusion of heterochromatic regions of heterologous chromosomes is observed. Eu- and heterochromatic regions of homologous chromosomes are intimately paired at the same time during the cell cycle. The structural rearrangements lead to reduced frequencies of chromocentric association as well as of homologous synapsis compared with the frequencies in the wild-type. The results obtained are discussed with respect to the general problem of the homologous interaction of chromosomes and the significance of heterochromatin for these processes.