DYNAMIC PROCESSES SHAPING THE GENE POOLS IN THE NATURAL POPULATIONS OF DROSOPHILA MELANOGASTER

I. K. Zakharov, Yu. Yu. Ilinsky, O. V. Vaulin, Ya. Ya. Sinyansky, A. M. Bocherikov, Yu. A. Koromyslov, A. V. Ivannikov, M. A. Voloshina, L. P. Zakharenko,

L. V. Kovalenko, S. V. Cheresiz, N. N. Yurchenko

Institute of Cytology and Genetics, Siberian Department of the RAS, Novosibirsk, Russia: zakharov@bionet. nsc. ru

A semi-centennial experience in the monitoring of processes that generate gene pools in the natural populations of Drosophila melanogaster testifies to the occurrence of mutation outbursts in the history of the species. The observed phenomenology of these events includes: 1) several genes or groups of genes with similar phenotypic expression, which can be involved in a particular outburst: 2) local or global geographical prevalence, the latter referring to a practically simultaneous process occurring in geographically remote populations; 3) outburst duration spanning ~7–11 years; 4) the recurrent mutation vogue phenomena involving particular gene/genes. Transposon invasion in a naïve species as well as recurrent activation of a mobile element were proposed to be the causal processes of the particular observed outbursts. Both the global singed mutation outburst, which involved the entire areal of D. melanogaster at the territory of the former Soviet Union (in 1973–1979), and the local yellow outburst (in 1982–1991), which caused an increase in concentration of mutation and mutability in that locus in a single separate population of Uman’ (Ukraine), are characterized by the transition of the involved genes into unstable condition. The latter event was caused by a single mobile element, hobo, while the former was related to the activation of several types of mobile elements. Transposable elements, as the facultative genomic components, co-evolve with the genome, and their role in the generation of genetic variability is logical to consider within the conceptual frame of co — adaptive genome — as both the important factors facilitating the ability of genomes to evolve and the major source and evolutionary tool generating the genetic variability in response to environmental changes.

Keywords: populations, gene pool, mutations, mutability, natural selection, Drosophila melanogaster, symbiosis, unstable genes, mobile elements.

Since the moment of its publication and for a period of already more than 150 years, the Darwinian theory has been repeatedly challenged by the revisionist attempts. Natural selection, as the cornerstone of the Darwinian evolutionary theory and, subsequently, the central point of the synthetic evolutionary theory as well, was most usually aimed at by the revisionists. Quite often the discoveries of the new biological phenomena or the origi — nal biological data obtained with the use of contemporary methods were employed by the Darwinian critic’s, however, all those biological “novelties” proved to be successfully incorporated into the modernized versions of the synthetic evolutionary theory.

The problem whether the mutability rate is permanent in the wild nature or it may fluctuate throughout the life time of species is crucial for the understanding of the genetic bases of evolution. At the beginning of the last century, Hugo de Vries came up with an idea of special mutational periods in the life time of species, when the hereditary factors are labile or unstable. For a long time these ideas were considered false and were not taken into account. However, along with the development of genetics, experimental data supporting Hugo de Vries’ hypothesis began to accumulate. In the 1920th M. Demerec

encountered the phenomenon of gene instability in the laboratory strains of Drosophila virilis (Demerec, 1937). Over the following decade, a great deal of communications re — porting the increased mutability in laboratory strains of different Drosophila species has been made. Mutator genes and highly mutable strains were discovered in the wild nature as well (for review, see Woodruff et al., 1983).

However, the recurrence and other specific traits of mutational outbursts were estab — lished only due to a longstanding research of geographically remote natural populations, commenced in the late 1920ties by Sergey S. Chetverikov and his followers and subse — quently actively pursued in Russia by several generations of geneticists (see reviews by Golubovsky, Kaidanov, 1995). As a result, the unique data on the dynamics of mutational process in natural populations of Drosophila melanogaster have been accumulated, with some Eurasian populations being monitored permanently since 1931 until now (Берг,

1948, 1961; Berg, 1966, 1982; Дубинин, 1966; Голубовский и др., 1974; Zakharov et al.,

2001; Захаров и др., 2008).

Here, the results of the four decades of research in this area carried out in our lab

are presented. Taken together with the previous research data obtained in the popula-tions of the same area, they evidence the regularity of mutation outbursts accompa-nied by unstable allele occurrence. Mutational outbursts may be local or may involve

remote populations in a short period of time; the latter phenomenon being referred to

as the “mutational vogue” (Голубовский и др., 1974; Golubovsky, 1980; Berg, 1982).

The mutational outbursts usually damp out within ~7–11 years. We were the first to

report the secondary outburst or the “recurrent mutational vogue” of the yellow gene

(y; 1–0.0) (Захаров, Голубовский, 1985).

Genetic and molecular analysis of unstable alleles isolated from the wild indicated

at the insertional nature of their instability (Golubovbsky et al., 1977; Голубовский,

Беляева, 1985; Yurchenko et al., 1984; O’Hare et al., 1998; Грачева и др., 1998). Hence,

such mutation outbursts could have been caused by the sporadic activation/invasion of

genetic mobile elements, although the key events leading to such activation still remain

under question. However, one of the causative mechanisms underlying the periodical

mobile element activation should, obviously, be related to the biocenotic interaction of

populations with infective agents.

Long-standing observations enabled us and others to establish two types of abrupt

mutability fluctuations. The first is related to the fluctuation of the overall mutability

rate evaluated by the total frequency of lethal mutations in a given chromosome. This

sort of event is typical both for laboratory strains and the strains isolated from the nature

(Green, 1977; Golubovsky et al., 1977; Woodruff, 1983). This paper focuses on another

type of events associated with fluctuating concentration and mutability of particular

genes (Zakharov, 2001; Zakharov et al., 2001).

Mutational vogue of different genes phenotypically similar to abnormal abdomen mutation

In 1968, an increased frequency of anomalies similar to the previously known abnor — mal abdomen mutation was observed in all studied D. melanogaster populations (Berg,

1972 a, b, 1973, 1974; Голубовский и др., 1974). As a rule, anomalies had a semidomi — nant inheritance. These mutations differed in localization (sex-linked or autosomal), in penetration and expression. This variability is the source of a certain subjectivity

in discrimination between the wild-type phenotype and weakly expressed mutation. Despite that, an increased concentration of abnormal abdomen-like phenotypes as well as their stronger expression in females are evident (Berg, 1974; Golubovsky, 1980).

Two outbursts in yellow — the global and the local one

Beginning in 1937, in numerous remote populations of D. melanogaster of the former Soviet Union, an increased concentration of yellow body mutation (y; 1–0.0) was detect — ed. An increase in mutation concentration was accompanied with (or resulted from) the increased mutability rate of phenotypically wild-type yellow alleles (Гершензон, 1941;

Дусеева, 1948). The frequency of mutation of those alleles from phenotypically yellow+

to yellow peaked to the values of 0.02–0.08 %. In other words, phenotypically wild-type

alleles of the yellow locus were highly unstable. Unfortunately, the reversion frequency of

mutant derivatives has not been studied at that period.

Mutational outburst of yellow gene in 1930–1940-ties is referred to as a global one as

it involved 35 populations studied over this period in the European and Asian parts of the

Soviet Union. The concentration of mutant yellow chromosomes reached 0.2 %; and the mutability of some y+-alleles was up to 0.4 % (Дусеева, 1948). This outburst lasted for at least a decade. In 1946, an acute drop in mutability of yellow locus (as compared to 1937), was found in two populations of Tiraspol (Moldavia) and Uman (Ukraine), although yel — low allele concentration in Uman still stood high (Берг, 1948).

In the same period, an increased mutational activity in other sex-linked genes was observed as well. Increased mutability in white, singed and forked bristles loci was found in two populations of Voronezh (Central Russia) and Dushanbe (Central Asia) (Дусеева,

1948; Berg, 1966).

In the subsequent to this outburst decades, the concentration and frequency of yel-low mutations lied background (0.04 % and below) (Берг, 1961, Berg, 1966).

A remarkable exception is the D. melanogaster population in Uman, where we ob-served a strong rise in the concentration of yellow-X-chromosome beginning from 1981

(Захаров, Голубовский, 1985; Голубовский и др., 1987; Zakharov, Skibitsky, 1995;

Захаров и др., 1995; Грачёва и др., 1998). Year by year, we monitored the dynamics

of the Uman’ population outburst. In the period of 1981–1991, an increased concentra-tion of yellow-X-chromosome observed in the males averaged the frequency of 0.9 %

(N=11,139), while the frequency of heterozygous females carrying yellow-X-chromosome

averaged to 1.7 % (N=3,217), and in females inseminated in nature by yellow-mutant

males the average frequency of yellow-X-chromosome was 0.8 % (N=2,609). Thus, the

mean concentration of yellow X-chromosomes in Uman over the studied period equaled

to 0.9 % (N=20,182), which is a 30-fold increase compared to the background concentra-tion of yellow mutations (0.03 %) (N=198,210).

The phenomenon of increased mutability (10-2–10-4) of phenotypically mutant and

wild-type yellow alleles in Uman, discovered in 1980th, can be explained by recurrent in-versions and reinversions of the regulatory region of yellow gene flanked by the copies of

hobo transposon. Most of the molecular events accompanying this process occur with no

visible phenotypical changes. The fly strains from Uman and their derivatives seem to re-main phenotypically stable, however, following several generations of lab culturing they

can change the molecular-genetic characteristics of the yellow locus. Thus, the level of

instability in yellow locus, as evaluated by the phenotypical changes, is, in fact, underesti-

mated. Phenotypical instability in D. melanogaster strains from Uman can be lost during their lab maintenance. In some strains, however, it can be induced by the series of crosses with laboratory stocks carrying the attached X-chromosomes. Therefore, the saturating crosses with laboratory stock can induce genetic instability. In our work, the major mech — anism generating genetic heterogeneity in the yellow locus of D. melanogaster is shown to be mediated by hobo element. An increased frequency of recessive lethal mutations in у2-717-Х-chromosome from Uman is, possibly, due to the reinsertions of mobile elements, which are the major cause of spontaneous mutations in Drosophila melanogaster.

Global mutation outburst of singed gene

In 1973, some researchers have independently found the sharp increase in mutational frequency of singed gene (sn; 1–21.0) in the populations of Caucasus and Central Asia (Berg,

1974; Иванов, Голубовский, 1977). Subsequently, starting from 1975, phenotypically and genetically different alleles of singed (mutant males and sn/+ heterozygous females) were isolated from different remote populations (Golubovsky, 1980; Захаров, 1984; Захаров, Голубовский, 1984; Захаров и др., 1995). A hundred-fold increase in mutability level of singed has been observed. For example, in 1974–1977, the observed mutability was equal to 0.2–0.5 × 10-3 and the concentration of heterozygous females averaged to 0.1 % in North Caucasian and Trans Caucasian D. melanogaster populations. Starting from 1980, both the frequency and concentration of singed mutations began to decrease. This outburst of singed, thus, lasted for 7 years and was related to the activation of hobo and other mobile elements. For example, insertion of hobo element caused the genetical instability of singed-49 X-chro — mosome, the derivative alleles of which were studied in details by molecular-genetic meth — ods (Yurchenko et al., 1984; O’Hare et al., 1998). Singed-49 X-chromosome was remarkable due to the fact that it was carrying the sn49: : Tn-clw transposon, the naturally occurring in the wild genetically engineered construct. In this system, all mutational transitions fall into 4 clusters, characteristic for the phenotypical expression of their unstable singed- derivatives, the directions and frequencies of mutation transitions of the latter, as well as the character of expression of club-wing mutation.

Male Recombination class of mutators and the lethal mutations in chromosome 2 in the natural populations of D. melanogaster

We study the MR-class of mutator genes detected by their ability to induce recom — bination in the progeny of D. melanogaster males and their effects on the viability of ho — mozygotes for chromosome 2 obtained from the different Eurasian natural populations. In 1988 and 1990, as much as 201 chromosomes isolated from Dushanbe population were studied for MR-activity yielding 54 chromosomes (26.9 %) MR-positive, one of which (0.5%) was classified as a strong MR-factor with recombination frequency over 0.5 %. In 1993, in Uman population, fifteen chromosomes 2 out of 83 studied (18.1 %) carried MR factors, one of which (1.2 %) was strong. Populations of Pospelikha, Zmeinogorsk, and Gorno-Altaisk studied in year 1992 yielded 25 MR-chromosomes out of 85 chro — mosomes studied (29.4 %), with one of them (1.2 %) being a strong MR factor. In 2001, we studied the MR-activity of 55 chromosomes from Bishkek and Tashkent populations and detected 39 MR-chromosomes (70.9 %), 25 out of which (45.5 %) being the strong MR factors. These data show that the frequency of MR-chromosomes found in Central

Asian populations in 2001 (70.9 %) was twice as high as the MR-frequency observed in the period of 1988–1992 in the different populations of Northern Eurasia (see also: Ivan — nikov et al., 1995). Noteworthy, the fraction of strong MR-chromosomes in Central Asia in 2001 (45.5 %), is also considerably higher than previously (1.2 %).

MR factors are known to induce a wide range of mutations. It seems logical to assume that the high concentration of MR-chromosomes in populations and a high fraction of strong MR factors among them would increase the concentration of the lethal mutations in those populations. In 1990, we studied 240 chromosomes 2 from Dushanbe population and detected 41 lethal chromosomes (17.1 %). As much as 25 chromosomes 2 out of 136 studied (18.4 %) in 1991 in Uman population were carrying lethal mutations. In popu — lations of Bishkek and Tashkent, as much as 17.5 % of chromosomes 2 (58 out of 332) collected in year 2001 were also carrying lethal mutations (the combined data for both populations). Obviously, the concentrations of the lethal mutations in Dushanbe (1990) and Uman (1991), 17.1 % and 18.4 %, respectively, do not differ much from those in Bish — kek and Tashkent (2001), 17.5 % (Иванников и др., 2008).

Our data, therefore, suggest that the two-fold increase in concentration of MR-chro — mosomes accompanied by a manifold increase in the fraction of strong MR factors, ob- served in the last decade, obviously, did not effect the concentration of lethal mutations in the natural populations of D. melanogaster.

Wolbachia, an endosymbiont in natural populations of D. melanogaster

An endosymbiotic alpha-proteobacteria, Wolbachia, is prevalent among arthropod and filarial nematode hosts and is characterized by vertical transmission. Wolbachia causes repro — ductive abnormalities in the host species, which represent the mechanism of spread of in — fected cytoplasm in the population (Hilgenboecker et al., 2008). Here, isofemale lines estab — lished from fly collections from the Eurasian populations of D. melanogaster were screened for Wolbachia infection. Wolbachia were genotyped by the use of 5 variable markers: insertion of IS5 sequence into two loci, number of repeats of two mini-satellites, and an inversion. In this study, 665 isofemale lines isolated from the natural populations of D. melanogaster from the Ukraine, Belarus, Moldavia, the Caucasus, Central Asia, the Urals, Udmurtia, Altai, Western and Eastern Siberia, and the Russian Far East since 1974 were screened (Илинский, Захаров,

2007, 2009; Ilinsky, Zakharov, 2007). Drosophila populations of the Caucasus, Cental Asia, and Altai were found to be heterogenic in the genotypes of prevalent cytoplasmic Wolbachia infection. wMel is the most widespread Wolbachia genotype found in all of the studied popu — lations. wMelCS2 genotype was sporadically occurring in the Eastern European populations while regularly found in the Asian and Altai populations. wMelCS was sporadically found only in the latter populations. The interaction of genes and genomes of the host species and its symbiont plays an important part in structuring the ecological relation between the two species (Воронин и др., 2009; Илинский, Захаров, 2009).

Genetic variability in populations, insertion mutagenesis and natural selection

The data accumulated during 5 decades of monitoring over the mutation process in natural populations of D. melanogaster allow the conclusion that mutational outbursts are regular events in the life of the species. The population phenomenology of these events

is as follows: 1) The outbursts may involve a particular genome locus or a group of genes with similar phenotypic expression; 2) The outbursts may be local or global, the latter breferring to an almost synchronous spread across numerous remote populations; 3) Life span of a particular outburst may last for ~7–11 years; 4) The mutational vogue of a par — ticular gene can be recurrent.

The mutation outbursts are accompanied by transition of particular genes into unsta — ble state. This statement is clearly demonstrated by the example of the global outburst of singed. In this case, for the first time a set of mutant unstable alleles was isolated from na — ture; and the instability was dissected by genetic analysis. Alleles were found differing both in phenotype as well as in the direction and mutation frequency in germ and somatic cells.

On the basis of genetic data obtained from natural populations, and prior to the dis — covery of mobile elements in Drosophila, a conclusion was made that unstable sn-alleles in the wild were generated by insertional mechanism (Green, 1977; Golubovsky et al.,

1977). This conclusion was supported by molecular genetic data, as well as by in situ hybridization to salivary gland polythenic chromosomes (Голубовский, Беляева, 1985). Although the sn locus is a “hot spot” for P element insertion, the global outburst of singed locus was found to be associated with activation of other mobile elements, as well. Be — sides, these elements were activated in one and the same population. In such a way, in two X chromosomes from Far East population studied in 1975, the unstable mutations occurred. One of them was caused by P-element insertion, whereas the other — by mdg3. In the sn49 allele, a large inserted sequence of hobo-element origin was detected in the first intron of singed gene, and dissected in detail by molecular genetic methods (O’Hare et al., 1998).

The origin of many alleles of the yellow-2 type are related to the insertion of the mdg4 or gypsy mobile element (Biessman, 1985; Geyer et al., 1988). The outburst in yellow-2 is caused by hobo-mobile element insertion (Грачева и др., 1998).

Thus, the stable and unstable mutations that appear during the outburst period are related to the activation of different mobile elements, which are capable to site-specific insertion mutagenesis.

Let us consider abnormal abdomen mutation. In this case, we observe the abrupt in — crease of mutability and population concentration of phenotypically similar mutations in different loci. The phenomenon of this kind is referred to as “heterogeneity of similar phen”. Heterogeneity of similar phen in Drosophila was observed in the cases of inser — tional and viral mutagenesis (Gazaryan et al., 1987).

We will illustrate the situation by the example of singed loci, which is better studied by the methods of molecular and population genetics. This locus is a target for P-element insertion both under the action of MR-like mutators and as a result of their activation in the system of hybrid dysgenesis (Green, 1977; Brookfield, Mitchell, 1985; Roiha et al.,

1988; Engels, 1989; Ладвищенко и др., 1990). Two facts are in a good agreement with these data. First, Male Recombination factors are of widespread occurrence throughout the studied populations (Ivannikov et al., 1995). Second, a predominance of P-insertions amongst the samples isolated from nature during the singed-allele burst.

On the other hand, P-DNA replicas began to spread in Eurasian populations of D. mel — anogaster (as in the case of populations studied by us) only in 1960ties (Anxolabehere et al., 1988; Kidwell, 1994), whereas the increase of singed mutability was registered even in

1930-1940ties. Besides, the individuals from natural populations characterized by singed

gene burst, according to our data, fall in the M-cytotype. Moreover, these individuals carry

deleted variants of the P element. These variants were denoted as KP and were found first in the Krasnodar population (Black et al., 1987). They turn out to be dispersed throughout the whole species areal (Read, Gibson, 1993). The action of KP leads to suppression of full — sized replicas transposition, although the presence of KP replicas in genome is not always necessary for P-mediated instability to be suppressed (Otori et al., 1994).

Thus, the relation between P-element replicas distribution at the end of 1960ties in Eurasian populations and singed gene mutability outburst in 1973 does exist, but the former is not the direct and the only cause of mutability outburst in this locus. All the more difficult is to explain the reason of the other types of outbursts registered more than half of a century ago. To our opinion, the common biological approach is required for the search of the factors and key events that shape the population and genetic regular pattern of mutational bursts.

Stable and unstable mutations occurring during the outburst period are therefore as- sociated with the activation of different mobile elements capable of site-specific insertion.

This brings up the questions: how can mobile elements be activated in nature? Which processes trigger activation? How are these processes synchronized in geographically re — mote populations? Why this activation demonstrates wave-like pattern? Why insertion of mobile elements is site specific? Only tentative answers to such questions can be given (Kidwell, Lish, 2001).

Investigation of insertion mutagenesis, in case of insertion alleles isolated from natu — ral populations of D. melanogaster, allows us to understand the complex pattern of ge — netic events caused by insertion mutations at different levels and to gain more knowledge about the nature of genetic variability in natural populations (Golubovsky, Kaidanov,

1995; Захаров и др., 2008).

The mechanism of action/manifestation of transposable elements lies in induction of

mutations and recombinations, which increase the mutability rate and expand the poten-tial of combinatorial variability. Still, even on this background, the role of the selection

remains the same.

Transposable elements, as the facultative elements of the genome, co-evolve with the

genome, and their role in the generation of genetic variability is logical to consider within

the concept of co-adaptive genome. Transposable elements are being currently consid-ered as both the important factors facilitating the ability of genomes to evolve and the

major source and evolutionary tool generating genetic variability in response to environ-mental changes.

All the species in biocenosis are subjected to infections with microorganisms (most

often, of viral origin). The temporal dynamics of this interaction may be of pulse, wave-like mode. It may cause synchronized alteration of gene pool in populations because the

transmission of infections agent is incomparably higher rather than usual migration of the

individuals of the host species. This may cause both local and global bursts of infections

(Andrewes, 1967).

In conclusion, the results of the analysis given in the present paper and some other

data give evidence that facultative genetic elements of the combined nuclear/cytoplasmic

genome (including different classes of mobile elements, microorganisms, and viruses) play

a significant role in spontaneous mutagenesis and in structuring the natural population

gene pools (Temin, Engels, 1984; Smith, Corces, 1991; Golubovsky, 1995). Spontaneous

mutagenesis can be considered as a two-stage process. At the first stage, the facultative

genome elements are activated by some currently non-identified weak, non-mutagenic

environmental factors. They cause inherited genotypic alterations, which, as a rule, do not exceed the limits of morphophysiological norm. Such alterations may be considered as pre-mutational. Only at the second stage of mutagenesis, the classical gene or chromo — somal mutations appear under the influence of facultative genome elements.

Thus, the modern genetics carries on the description and characterization of the mu — tations, describes novel mechanisms of mutagenesis as well as differential expression of particular gene systems, thus expanding the described field of the raw material for evolu — tionary changes, the substrate, with which the selection works.

This work was supported partly by Russian Foundation for Basic Research No. 99-04-00872-a, and by Program of Basic Research of the Presidium Russian Academy of

Sciences “Biological diversity” № 23.30.

References

Берг Р. Л. О взаимоотношении между мутабильностью и отбором в природных популяциях

Drosophila melanogaster // Журнал общей биологии. 1948. Т. 9. № 4. С. 299–313.

Берг Р. Л. Мутация «желтая» (yellow) в популяции Drosophila melanogaster г. Умани // Вест — ник Ленинградского университета. 1961. № 3. Сер. Биол. Вып. 1. С. 77–89.

Воронин Д. А., Бочериков А. М., Баричева Э. М. и др. Влияние генотипического окружения хо — зяина — Drosophila melanogaster — на биологические эффекты эндосимбионта Wolbachia (штамм wMelPop) // Цитология. 2009. Т. 51. № 4. С. 335–345.

Гершензон С. М. Новые данные по генетике природных популяций Drosophila melanogaster // Статьи по генетике. Институт зоологии Академии наук УССР. 1941. № 4–5. С. 13–39.

Голубовский М. Д., Беляева Е. С. Вспышка мутаций в природе и мобильные генетические эле — менты: изучение серии аллелей локуса singed у Drosophila melanogaster // Генетика. 1985. Т. 21. № 10. С. 1662–1670.

Голубовский М. Д., Захаров И. К., Соколова О. А. Анализ нестабильности аллелей гена yellow, выделенных из природной популяции дрозофил в период вспышки мутабильности // Генетика. 1987. Т. 23. № 9. С. 1595–1603.

Голубовский М. Д., Иванов Ю. Н., Захаров И. К., Берг Р. Л. Исследование синхронных и па — раллельных изменений генофондов в природных популяциях плодовых мух Drosophila melanogaster // Генетика. 1974. Т. 10. № 4. C. 72–83.

Грачева Е. М., Захаров И. К., Волошина М. А. и др. Вспышки мутаций гена yellow в природной популяции Drosophila melanogaster связаны с инсерцией транспозона hobo // Генетика.

1998. Т. 34. № 4. С. 462–468.

Дубинин Н. П. Эволюция популяций и радиация. М. : Атомиздат, 1966. 744 с.

Дусеева Н. Д. Распространение высокой мутабильности в yellow в природных популяциях

Drosophila melanogaster // Доклады Академии наук СССР. 1948. Т. 59. № 1. С. 151–153.

Захаров И. К. Генетика природных популяций Drosophila melanogaster: колебание мутабиль — ности и концентрации аллелей гена singed в природных популяциях // Генетика. 1984. Т. 20. № 8. С. 1295–1304.

Захаров И. К., Голубовский М. Д. Cерия нестабильных аллелей гена singed, выделенных из природных популяций Drosophila melanogaster: закономерности мутирования // Генети- ка. 1984. Т. 20. № 7. С. 1117–1124.

Захаров И. К., Голубовский М. Д. Возвращение моды на мутацию yellow в природной популя — ции Drosophila melanogaster г. Умани // Генетика. 1985. Т. 21. № 8. С. 1298–1305.

Захаров И. К., Ваулин О. В., Илинский Ю. Ю. и др. Источники генетической изменчивости в природных популяциях Drosophila melanogaster // Информационный вестник ВОГиС.

2008. Т. 12. № 1/2. С. 112–126.

Захаров И. К., Иванников А. В., Скибицкий Е. Э. и др. Генетические свойства аллелей генов Х-хромосомы, выделенных из природных популяций Drosophila melanogaster в период вспышки мутаций // Доклады Академии наук. 1995. Т. 341. №1. C. 126–129.

Иванников А. В., Синянский Я. Я., Юрченко Н. Н. и др. Летальные мутации в популяциях Drosophila melanogaster Северной Евразии // Информационный вестник ВОГиС. 2008. Т. 12. № 3. С. 392–398.

Иванов Ю. Н., Голубовский М. Д. Повышение мутабильности и появление мутационно — нестабильных аллелей локуса singed в популяциях Drosophila melanogaster // Генетика.

1977. Т. 13. № 4. С. 655–666.

Илинский Ю. Ю., Захаров И. К. Характеристика инфицированности цитоплазматическим эн-досимбионтом Wolbachia популяции Drosophila melanogaster Умани // Доклады Акаде-мии наук. 2007. Т. 413. № 4. С. 561–563.

Илинский Ю. Ю., Захаров И. К. Цитоплазматическая несовместимость у Drosophila melanogaster,

обусловленная различными генотипами Wolbachia // Экологическая генетика. 2009. Т. 7.

№ 2. С. 11–18.

Ладвищенко А. Б., Могила В. А., Георгиев П. Г. и др. Супернестабильные системы у Dro-sophila melanogaster. Анализ мутаций локусов singed и cut // Генетика. 1990. Т. 26. № 7.

С. 1133–1143.

Andrewes C. H. The Natural History of Viruses. L. : Weidenfeld and Nicolson. 1967. VIII, 237 p.

Anxolabehere D., Kidwell M. D., Perique G. Molecular characteristics of diverse populations are

consistent with the hypothesis of recent invasion of Drosophila melanogaster by mobile

P elements // Molecular Biology and Evolution 1988. Vol. 5. P. 252–269.

Berg R. L. Studies on mutability in geographically isolated populations of Drosophila melanogaster //

Mutations in Populations / ed. by R. Yoncariv. Prague : Czechoslovak Academy of Sciences,

1966. P. 61–74.

Berg R. L. The inheritance of abnormal abdomen in the offspring of wild males of Drosophila mela-nogaster // Drosophila Information Service. 1972a. Vol. 48. P. 67.

Berg R. L. A sudden and synchroneous increase in the frequency of abnormal abdomen in the geo-graphically isolated populations of Drosophila melanogaster // Drosophila Information Ser-vice. 1972b. Vol. 48. P. 94.

Berg R. L. A further study of the rate of abnormal abdomen (aa) in geographically isolated D. mela-nogaster population // Drosophila Information Service. 1973. Vol. 50. P. 92.

Berg R. L. A simultaneous mutability rise at the singed locus in two out three Drosophila melano-gaster populations studied in 1973 // Drosophila Information Service. 1974. Vol. 51. P. 100.

Berg R. L. Mutability changes in Drosophila melanogaster populations of Europe, Asia and North

America and probable mutability changes in human populations of the USSR // Japanese

Journal of Genetics. 1982. Vol. 57. P. 171–183.

Biessman H. Molecular analysis of yellow gene (y) region of Drosophila melanogaster // Proceedings

of the National Academy of Sciences of the USA. 1985. Vol. singed и cut // Генетика. 1990. Т. 26. № 7.

С. 1133–1143.

Andrewes C. H. The Natural History of Viruses. L. : Weidenfeld and Nicolson. 1967. VIII, 237 p.

Anxolabehere D., Kidwell M. D., Perique G. Molecular characteristics of diverse populations are

consistent with the hypothesis of recent invasion of Drosophila melanogaster by mobile

P elements // Molecular Biology and Evolution 1988. Vol. 5. P. 252–269.

Berg R. L. Studies on mutability in geographically isolated populations of Drosophila melanogaster //

Mutations in Populations / ed. by R. Yoncariv. Prague : Czechoslovak Academy of Sciences,

1966. P. 61–74.

Berg R. L. The inheritance of abnormal abdomen in the offspring of wild males of Drosophila mela-nogaster // Drosophila Information Service. 1972a. Vol. 48. P. 67.

Berg R. L. A sudden and synchroneous increase in the frequency of abnormal abdomen in the geo-graphically isolated populations of Drosophila melanogaster // Drosophila Information Ser-vice. 1972b. Vol. 48. P. 94.

Berg R. L. A further study of the rate of abnormal abdomen (aa) in geographically isolated D. mela-nogaster population // Drosophila Information Service. 1973. Vol. 50. P. 92.

Berg R. L. A simultaneous mutability rise at the singed locus in two out three Drosophila melano-gaster populations studied in 1973 // Drosophila Information Service. 1974. Vol. 51. P. 100.

Berg R. L. Mutability changes in Drosophila melanogaster populations of Europe, Asia and North

America and probable mutability changes in human populations of the USSR // Japanese

Journal of Genetics. 1982. Vol. 57. P. 171–183.

Biessman H. Molecular analysis of yellow gene (y) region of Drosophila melanogaster // Proceedings

of the National Academy of Sciences of the USA. 1985. Vol. 82. P. 7369–7373.

Black D. N., Jackson M. S., Kidwell M. G., Dover G. A. KP elements repress P-induced hybrid

dysgenesis in Drosophila melanogaster // The EMBO Journal. 1987. Vol. 6. P. 4125–4135.

Brookfield J. F. Y., Mitchell S. F. P-M hybrid dysgenesis using geographically separated P-strains of

Drosophila melanogaster // Heredity. 1985. Vol. 55. P. 163–165.

Demerec M. Frequency of spontaneous mutations in certain stocks of Drosophila melanogaster //

Genetics. 1937. Vol. 22. P. 469–478.

Engels W. R. P elements in Drosophila melanogaster // Mobile DNA / eds. D. E. Berg, M. M. Howe.

Washington DC : American Society of Microbiology, 1989. P. 437–484.

Gazaryan K. G., Nabirochkin S. D., Shibanova E. N. et al. Unstable visible mutations induced in

Drosophila melanogaster by injection of oncogenic virus DNA into polar plasm of early

embryos // Molecular and General Genetics. 1987. Vol. 207. P. 130–141.

Geyer P. K., Green M. M., Corces V. G. Reversion of gypsy-induced mutation at the yellow (y) locus

of Drosophila melanogaster is associated with the insertion of a newly defined transposable

element // Proceedings of the National Academy of Sciences of the USA. 1988. Vol. 85. P. 3938–3942.

Golubovsky M. D. Mutational process and microevolution // Genetica. 1980. Vol. 52/53. P. 139–149.

Golubovsky M. D. Mobile genetics and forms of heritable changes in eukaryotes // Биополимеры и клетка. 1995. Т. 11. № 2. С. 29–38.

Golubovsky M. D., Ivanov Yu. N., Green M. M. Genetic instability in Drosophila melanogaster: putative multiple insertion mutants at the singed bristle locus // Proceedings of the National Academy of Sciences of the USA. 1977. Vol. 74. №. 7. P. 2973–2975.

Golubovsky M. D., Kaidanov L. Z. Investigation of genetic variability in Drosophila populations // Genetics of natural populations: the continuing importance of Theodosius Dobzhansky. N. Y. : Columbia Univ. Press, 1995. P. 188–197.

Green M. M. Genetic instability in Drosophila melanogaster: de novo induction of putative insertion mutants // Proceedings of the National Academy of Sciences of the USA. 1977. Vol. 74. № 8. P. 3490–3493.

Hilgenboecker K., Hammerstein P., Schlattmann P. et al. How many species are infected with

Wolbachia? — A statistical analysis of current data // FEMS Microbiology Letter. 2008. Vol.

281. P. 215–220.

Ilinsky Yu. Yu., Zakharov I. K. The endosymbiont Wolbachia in Eurasian populations of Drosophila melanogaster // Russian Journal of Genetics. 2007. Vol. 43. №. 7. P. 905–915.

Ivannikov A. V., Golubovsky M. D., Koromyslov Yu. A., Zakharov I. K. MR chromosomes in Eurasian populations of Drosophila melanogaster // Russian Journal of Genetics. 1995. Vol. 31. №. 2. P. 178–180.

Kidwell M. G. The evolutionary history of the P family of transposable elements // Journal of

Heredity. 1994. Vol. 85. P. 339–346.

Kidwell M. G., Lish D. R. Perspective: Transposable

Zakharov I. K., Skibitsky E. E. Genetics of unstable alleles of the X chromosome genes isolated from natural populations of Drosophila melanogaster during the outburst of mutation уеllow in 1982 to 1991 in Uman’ // Russian Journal of Genetics. 1995. Vol. 31. №. 8. P. 920–924.

Zakharov I. K., Ivannikov A. V., Yurchenko N. N. Mutational process and gene pool of natural populations of Drosophila melanogaster // Modern Problems of Radiobiology, Radioecology and Evolution. Dubna : Joint Institute for Nuclear Research, 2001. P. 100–112.

Динамические процессы в генофондах природных популяций

Drosophila melanogaster

И. К. Захаров, Ю. Ю. Илинский, О. В. Ваулин, Я. Я. Синянский, А. М. Бочериков, Ю. А. Коромыслов, А. В. Иванников, М. А. Волошина, Л. П. Захаренко,

Л. В. Коваленко, С. В. Чересиз, Н. Н. Юрченко

Институт цитологии и генетики Сибирского отделения РАН Новосибирск, Россия; zakharov@bionet. nsc. ru

Полувековое наблюдение мутационного процесса в природных популяциях Dro — sophila melanogaster позволяет сделать вывод о существовании вспышек мутаций в жизни вида. Популяционная феноменология данного явления такова: 1) вспышки мутаций происходят по отдельным локусам генома (yellow или singed) или по группе генов со сходным фенотипическим проявлением (abnormal abdomen); 2) вспышки мутаций могут быть локальными или глобальными (последнее означает схожие гене — тические процессы, происходящие практически одновременно в удаленных генети — ческих популяциях); 3) определенная вспышка продолжается 7–11 лет; 4) возможно возвращение «моды» на мутации определенного гена. Реактивация мобильного эле — мента или инвазия нового для вида транспозона могут лежать в основе некоторых из наблюдавшихся вспышек мутаций. Как глобальная вспышка мутаций в локусе singed, охватившая весь ареал вида D. melanogaster на территории бывшего СССР в 1973–1979 гг., так и локальная вспышка мутаций в локусе yellow в 1982–1991 гг. в отдельной популяции Умани (Украина) характеризовались нестабильным состоя — нием соответствующих локусов, связанным с активностью мобильных элементов. Последняя вспышка в Уманской популяции связывается с активацией единствен — ного вида мобильных элементов, hobo. Мобильные элементы, как факультативные компоненты генома, коэволюционируют с геномом хозяина, и их роль в формиро — вании генетической изменчивости логичнее рассматривать в рамках концепции коа — даптированного генома. Мобильные элементы сегодня принято рассматривать как важные факторы, обеспечивающие способность генома эволюционировать, и равным образом как главный компонент эволюционного инструментария, генерирующего генетическую изменчивость в ответ на изменения окружающей среды.

Ключевые слова: популяции, генофонд, Drosophila melanogaster, симбиоз, мутации, мутабильность, естественный отбор, нестабильные гены, мобильные элементы.

Материал взят из: Чарльз Дарвин и современная биология. Труды Международной научной конференции (21–23 сентября 2009 г., Санкт — Петербург)