Inversion polymorphism in malaria mosquito Anopheles messeae. Part X. Resistance of larvae with different genotypes to toxins of crystal-forming bacteria Bacillus thuringiensis subsp. israelensis (serovar H14)

Insensibility of larvae with different chromosomal inversions to the toxins of Bacillus thuringiensis subsp. israelensis (Bti) was examined. It has been shown that larvae with inversion combinations XL0(XL1)2R0-3R0-3L0 had greater variability after treatment with Bti than larvae with inversions XL1(XL2)2R1-3R1-3L1(3L0). The former inversion combinations were previously shown to dominate in the south of the species area and to be supported by K-selection. The latter inversion combinations form "northest" karyotypes and are supported by r-selection. It is obvious that genetic effects of treatments with Bti depend on the population's structure and the directions of natural selection. The decrease in the level of heterozygotes after treatment of larvae with Bti reflects destruction of the system of genetic homeostasis in the natural populations of A. messeae.     

Inversion polymorphism of the malarial mosquito Anopheles messeae. IV. The stability of the frequency distribution of the inversions by species area

Distribution of the frequencies of inversions XL1, 2R1, 3R1, 3L1, from geographically widely separated 8 populations had been studied during a long period of time. The geographical inclines of distribution of inversions XL1, 3R1 (a longitudinal) and 2R1 (a latitudinal) are stable in time. Stationarity of inversional polymorphism is not connected with superdominance of heterozygotes. It is supposed that the stable equilibrium of the frequencies of inversions is supported by variable selection.     

Inversion polymorphism in malarial mosquito Anopheles messeae natural populations from the north-eastern region of the range

A cytogenetic study of eight natural populations of Anopheles messeae from the north-eastern part of the species areal was conducted. Complete predominance of homozygotes XL11 and 3R11 in the northern populations was observed. Change in the chromosome 2 inversion frequencies from south northwards was shown. The 2R11 variant, which was not observed in the southern region, was found in the northern populations. These results indicate the maintenance of chromosome frequency of the distribution of inversions XL1 and 3R (in longitude) and 2R1 (in latitude). The inversion frequency distribution in the examined part of the areal have been preserved for a long time.     

Chromosomal polymorphism in the populations of malaria mosquito <Emphasis Type="Italic">Anopheles messeae</Emphasis> (Diptera,Culicidae) in the Volga region

We studied the species composition and chromosomal variability of malaria mosquitoes in the Volga Basin (Upper, Middle, and Lower Volga regions). We investigated larvae karyotypes of sibling species of the Anopheles maculipennis group. We calculated the frequencies of chromosomal inversions in the local populations of the dominant species An. messeae. We discovered that karyotypic structure of An. messeae populations depends on landscape-climatic zones. Populations of the Upper, Middle and Lower Volga differ in frequency of chromosome inversions XL, 2R, 3R, and 3L.     

Inversion polymorphism of the malaria mosquito Anopheles messeae. VIII. Distribution of larvae in biotopes under conditions of co-habitation with Anopheles beklemishevi

The role of chromosomal variability was studied in the process of biotopical distribution of larvae of the sibling species Anopheles messeae and A. beklemishevi. It is shown that frequency of the inversions XL1, XL2, 2R1, 3R1 of A. messeae was changed in the lakes with different larval quantity of the sibling species. Mosquito of A. beklemishevi were developed in the suboptimal biotops having low larwal quantity of A. messeae with the analogous chromosomal arrangement 2R1. The larvae with "northeast" genocomplexes of A. messeae prevailed over A. beklemishevi in the lakes with high larval quantity and this prevalence determined dominant state of A. messeae. It is noted that natural selection on the preimaginal stages of development acts in the direction of karyotypic divergence of the sibling species and promotes more effective utilisation of food resources by each species.     

Chromosome Studies in Wild Populations of D. MELANOGASTER

Chromosome studies of wild D. melanogaster populations from Missouri, Mississippi, Louisiana and Texas uncovered 58 inversions. Six were common and cosmopolitan; 52 were new, rare and generally endemic. In one of two Missouri populations tested, structurally heterozygous females carried significantly more sperm at capture than did the homozygotes. In both populations comparisons of wild sperms with the females carrying them indicated significant positive assortative mating and an excess production of homozygotes among the F₁ progeny. Wild females structurally heterozygous in up to three major autosomal arms showed no associated nondisjunctional egg lethality; those heterozygous in all four arms produced from 0% to 24% dead eggs, suggesting the presence of intrapopulational gene modifiers of meiosis. Texas populations supported on windfall citrus fruit showed a slight but significant difference in inversion frequencies between flies breeding on oranges and those breeding on grapefruit. Within these populations inversions were not distributed at random among individuals; rather there was an observed excess of individuals carrying intermediate numbers, and a deficiency of those carrying very few or very many inversions. While there was no significant linkage disequilibrium associated with this central tendency, there was a significant interchromosomal interaction: flies carrying inversions in chromosome 2 tended not to carry them in chromosome 3, and vice versa.     

Genetic analysis of female mating recognition between Drosophila ananassae and Drosophila pallidosa: application of interspecific mosaic genome lines

Drosophila ananassae and Drosophila pallidosa are closely related species that can produce viable and fertile hybrids of both sexes, although strong sexual isolation exists between the two species. Females are thought to discriminate conspecific from heterospecific males based on their courtship songs. The genetic basis of female discrimination behavior was analyzed using isogenic females from interspecific mosaic genome lines that carry homozygous recombinant chromosomes. Multiple regression analysis indicated a highly significant effect of the left arm of chromosome 2 (2L) on the willingness of females to mate with D. ananassae males. Not only 2L but also the left arm of chromosome X (XL) and the right arm of chromosome 3 (3R) had significant effects on the females' willingness to mate with D. pallidosa males. All regions with strong effects on mate choice have chromosome arrangements characterized by species-specific inversions. Heterospecific combinations of 2L and 3R have previously been suggested to cause postzygotic reproductive isolation. Thus, genes involved in premating as well as postmating isolation are located in or near chromosomal inversions. This conclusion is consistent with the recently proposed hypothesis that "speciation genes" accumulate at a higher rate in non-recombining genome regions when species divergence occurs in the presence of gene flow.     

Lack of Underdominance in a Naturally Occurring Pericentric Inversion in Drosophila Melanogaster and Its Implications for Chromosome Evolution

In(2LR)PL is a large pericentric inversion polymorphic in populations of Drosophila melanogaster on two Indian Ocean islands. This polymorphism is puzzling: because crossing over in female heterokaryotypes produces inviable zygotes, such inversions are thought to be underdominant and should be quickly eliminated from populations. The observed fixation for such inversions among related species has led to the idea that genetic drift can cause chromosome evolution in opposition to natural selection. We found, however, that In(2LR)PL is not underdominant for fertility, as heterokaryotypic females produce perfectly viable eggs. Genetic analysis shows that the lack of underdominance results from the nearly complete absence of crossing over in the inverted region. This phenomenon is probably caused by mechanical and not genetic factors, because crossing over is not suppressed in In(2LR)PL homokaryotypes. Our observations do not support the idea that the fixation of pericentric inversions among closely related species implies the action of genetic drift overcoming strong natural selection in very small populations. If chromosome arrangements vary in their underdominance, it is those with the least disadvantage as heterozygotes, like In(2LR)PL, that will be polymorphic or fixed in natural populations.     

Genomic Architecture of Rapid Parallel Adaptation to Fresh Water in a Wild Fish

Rapid adaptation to novel environments may drive changes in genomic regions through natural selection. However, the genetic architecture underlying these adaptive changes is still poorly understood. Using population genomic approaches, we investigated the genomic architecture that underlies rapid parallel adaptation of Coilia nasus to fresh water by comparing four freshwater-resident populations with their ancestral anadromous population. Linkage disequilibrium network analysis and population genetic analyses revealed two putative large chromosome inversions on LG6 and LG22, which were enriched for outlier loci and exhibited parallel association with freshwater adaptation. Drastic frequency shifts and elevated genetic differentiation were observed for the two chromosome inversions among populations, suggesting that both inversions would undergo divergent selection between anadromous and resident ecotypes. Enrichment analysis of genes within chromosome inversions showed significant enrichment of genes involved in metabolic process, immunoregulation, growth, maturation, osmoregulation, and so forth, which probably underlay differences in morphology, physiology and behavior between the anadromous and freshwater-resident forms. The availability of beneficial standing genetic variation, large optimum shift between marine and freshwater habitats, and high efficiency of selection with large population size could lead to the observed rapid parallel adaptive genomic change. We propose that chromosomal inversions might have played an important role during the evolution of rapid parallel ecological divergence in the face of environmental heterogeneity in C. nasus. Our study provides insights into the genomic basis of rapid adaptation of complex traits in novel habitats and highlights the importance of structural genomic variants in analyses of ecological adaptation.     

Polytene chromosome maps in four species of tsetse flies Glossina austeni, G. pallidipes, G. morsitans morsitans and G. m. submorsitans (Diptera: Glossinidae): a comparative analysis

Photographic polytene chromosome maps from pupal trichogen cells of four tsetse species, Glossina austeni, G. pallidipes, G. morsitans morsitans and G. m. submorsitans were constructed and compared. The homology of chromosomal elements between the species was achieved by comparing banding patterns. The telomeric and subtelomeric chromosome regions were found to be identical in all species. The pericentromeric regions were found to be similar in the X chromosome and the left arm of L1 chromosome (L1L) but different in L2 chromosome and the right arm of L1 chromosome (L1R). The L2 chromosome differs by a pericentric inversion that is fixed in the three species, G. pallidipes, G. morsitans morsitans and G. m. submorsitans. Moreover, the two morsitans subspecies appeared to be homosequential and differ only by two paracentric inversions on XL and L2L arm. Although a degree of similarity was observed across the homologous chromosomes in the four species, the relative position of specific chromosome regions was different due to chromosome inversions established during their phylogeny. However, there are regions that show no apparent homology between the species, an observation that may be attributed to the considerable intra—chromosomal rearrangements that have occurred following the species divergence. The results of this comparative analysis support the current phylogenetic relationships of the genus Glossina.     

Divergence with gene flow in Anopheles funestus from the Sudan Savanna of Burkina Faso, West Africa

Anopheles funestus is a major vector of malaria across Africa. Understanding its complex and nonequilibrium population genetic structure is an important challenge that must be overcome before vector populations can be successfully perturbed for malaria control. Here we examine the role of chromosomal inversions in structuring genetic variation and facilitating divergence in Burkina Faso, West Africa, where two incipient species (chromosomal forms) of A. funestus, defined principally by rearrangements of chromosome 3R, have been hypothesized. Sampling across an approximately 300-km east-west transect largely contained within the Sudan-Savanna ecoclimatic zone, we analyzed chromosomal inversions, 16 microsatellite loci distributed genomewide, and 834 bp of the mtDNA ND5 gene. Both molecular markers revealed high genetic diversity, nearly all of which was accounted for by within-population differences among individuals, owing to recent population expansion. Across the study area there was no correlation between genetic and geographic distance. Significant genetic differentiation found between chromosomal forms on the basis of microsatellites was not genomewide but could be explained by chromosome 3R alone on the basis of loci inside and near inversions. These data are not compatible with complete reproductive isolation but are consistent with differential introgression and sympatric divergence between the chromosomal forms, facilitated by chromosome 3R inversions.     

Chromosomal plasticity and evolutionary potential in the malaria vector <Emphasis Type="Italic">Anopheles gambiae</Emphasis> sensu stricto: insights from three decades of rare paracentric inversions

Background  

In the Anopheles gambiae complex, paracentric chromosomal inversions are non-randomly distributed along the complement: 18/31 (58%) of common polymorphic inversions are on chromosome arm 2R, which represents only ~30% of the complement. Moreover, in An. gambiae sensu stricto, 6/7 common polymorphic inversions occur on 2R. Most of these inversions are considered markers of ecological adaptation that increase the fitness of the carriers of alternative karyotypes in contrasting habitats. However, little is known about the evolutionary forces responsible for their origin and subsequent establishment in field populations.     

Evaluation of the genomic extent of effects of fixed inversion differences on intraspecific variation and interspecific gene flow in Drosophila pseudoobscura and D. persimilis

There is increasing evidence that chromosomal inversions may facilitate the formation or persistence of new species by allowing genetic factors conferring species-specific adaptations or reproductive isolation to be inherited together and by reducing or eliminating introgression. However, the genomic domain of influence of the inverted regions on introgression has not been carefully studied. Here, we present a detailed study on the consequences that distance from inversion breakpoints has had on the inferred level of gene flow and divergence between Drosophila pseudoobscura and D. persimilis. We identified the locations of the inversion breakpoints distinguishing D. pseudoobscura and D. persimilis in chromosomes 2, XR, and XL. Population genetic data were collected at specific distances from the inversion breakpoints of the second chromosome and at two loci inside the XR and XL inverted regions. For loci outside the inverted regions, we found that distance from the nearest inversion breakpoint had a significant effect on several measures of divergence and gene flow between D. pseudoobscura and D. persimilis. The data fitted a logarithmic relationship, showing that the suppression of crossovers in inversion heterozygotes also extends to loci located outside the inversion but close to it (within 1-2 Mb). Further, we detected a significant reduction in nucleotide variation inside the inverted second chromosome region of D. persimilis and near one breakpoint, consistent with a scenario in which this inversion arose and was fixed in this species by natural selection.     

Inversion Clines in Populations of DROSOPHILA MELANOGASTER

Twenty different natural populations of Drosophila melanogaster were sampled to determine the frequencies of inversions. Based on their frequencies and geographical distributions, the inversions could be classified as follows: (1) Common cosmopolitan inversions that are present in many populations in frequencies exceeding five percent and that may exhibit frequency clines over large geographical regions; (2) Rare cosmopolitan inversions that occur throughout the species range but usually at frequencies below five percent and that may be absent in many populations; (3) Recurrent endemic inversions that are found in several adjacent populations in frequencies usually not exceeding one or two percent; and (4) Unique endemic inversions that are found only among the progeny of a single individual and that may represent one aspect of the syndrome termed "hybrid dysgenesis". Four common cosmopolitan inversions that exhibit highly significant clines in populations in the eastern United States are In(2L)t, In(2R)NS, In(3L)P and In(3R)P.     

Chromosomal inversion polymorphism of Anopheles funestus from forest villages of South Cameroon.

The polymorphism of paracentric inversions of Anopheles funestus polytene chromosomes was studied in three villages (Nkoteng, Obala, and Simbock) located in a forest area of South Cameroon in order to analyse the genetic structure of these populations. A total of 146-210 chromatids could be scored from specimens collected over about two years. A low degree of chromosomal polymorphism was observed with two floating inversions on chromosomal arm 2 (2h and 2d), and three fixed arrangements on arms 3 (3a and 3b), and 5 (5a). Such arrangement of inversions has never been recorded elsewhere so far. The chromosome analysis indicated that the population from Obala was in Hardy-Weinberg equilibrium, whereas the samples from Nkoteng and Simbock showed a significant excess and deficit of heterokaryotypes, respectively. Significant differences in inversion frequencies on chromosomal arm 2 among villages lying in contrasting eco-climatic settings suggested an adaptive role of these inversions.     

Gametic associations between inversion and allozyme polymorphisms in Drosophila buzzatii.

Gametic disequilibria between second chromosome polymorphic arrangements and seven linked allozyme loci were estimated in seven populations of Drosophila buzzatii from Argentina. Significant and consistent associations across populations were detected for Est-1, Est-2, Aldox, and XDH: Phenograms based on Nei's genetic distance showed that chromosomes carrying the 2ST arrangement were more similar to each other, irrespective of the population from which they were extracted, than to chromosomes carrying the derived 2J and 2JZ3.Restriction of recombination in heterokaryotypes seems to be the best explanation for the significant linkage disequilibria between inversions and the loci located inside the rearranged segments, for example, Est-1 and Aldox, or close to the break points, for example, Est-2. However, epistatic interactions between Xdh, which is outside the inversions and not near the break points, and loci tightly linked to the inversions, is the most likely explanation for the association between Xdh and chromosomal arrangements. Some of the associations detected in endemic Argentinean populations are coincident with data obtained in colonizing populations of the Old World and Australia. Thus historical processes that took place in the original area of the species' distribution can account for these linkage disequilibria in colonized populations of D. buzzatii.     

Further evidence for latitudinal inversion clines in natural populations of Drosophila melanogaster from India.

Chromosomal analysis of eight Indian natural populations (six from north India and two from south India) of Drosophila melanogaster revealed the presence of 13 paracentric inversions, including one in the X chromosome. All four types of inversions--common cosmopolitan (4), rare cosmopolitan (3), recurrent endemic (2), and unique endemic (4)--were detected. The frequency of commonly occurring inversions and the level of inversion heterozygosity were found to be higher in the two southern populations. The south Indian populations are genetically more differentiated than those from the north. Also, latitudinal clines in the frequencies of the four common cosmopolitan inversions were detected. These results provide further evidence for the existence of inversion clines in Indian populations of D. melanogaster.     

Spatial and temporal variations of the chromosomal inversion frequencies across the range of malaria mosquito <Emphasis Type="Italic">Anopheles messeae</Emphasis> Fall. (Culicidae) during the 40-year monitoring period

The analysis of personal and published data on the frequency dynamics of chromosomal inversions within the range of Anopheles messeae obtained during the period from 1974 through 2014 is presented. The results showed that, in general, across the species range, during the 40 years of genetic monitoring, there was a steady (stationary) clinal distribution of inversions in the first decade (1974–1985). Then, over the period of five years (1986–1990), there was a considerable change in the inversion frequencies in favor of southwestern chromosomal variants (particularly strongly fixed in the Tomsk population), and from 1992 to the present time, these changes remained and were relatively stably reproduced in most parts of the range. It was noted that the jump in warming during the winter of 1981–1982 led to a correlated jump of the southwestern chromosomes in the Tomsk population. In connection with the general tendency toward the increase in average winter temperatures, a sharp decrease in the 2R₁ chromosome frequency in the Siberian region and Syktyvkar in the period from 1992 to the present time was observed. There is reason to assume that, over the past decade, the northern boundary of the An. messeae range moved northward to the tundra zone.     

Inversion frequencies in Drosophila serrata along an eastern Australian transect.

Clinal patterns over broad geographic regions provide a way of identifying characteristics of species under selection and are increasingly being used in quantitative trait locus mapping of adaptive genetic variation in Drosophila. However, interpretations of clinal patterns can be complicated by inversions that also vary clinally and reduce recombination in some parts of the genome. Drosophila serrata (Malloch) is an Australian endemic species being used to investigate the genetic basis of geographic variation in climatic adaptation and mate recognition. Here we describe inversions in D. serrata populations from the east coast of Australia, covering tropical and temperate regions. Seven autosomal paracentric inversions and 1 apparently complex X chromosome arrangement were identified from these populations. All inverted arrangements were relatively more common in tropical populations; 2 common inversions showed clinal patterns over part of the range of D. serrata. Inversion polymorphism was relatively higher in tropical populations and almost absent in populations near the cooler southern border, in agreement with findings on other Drosophila species. While these patterns will complicate mapping of adaptive variation in D. serrata, they suggest that this species will be useful in investigatingthe dynamics of inversion-trait associations in natural populations.     

The Fertility Effects of Pericentric Inversions in Drosophila Melanogaster

Heterozygotes for pericentric inversions are expected to be semisterile because recombination in the inverted region produces aneuploid gametes. Newly arising pericentric inversions should therefore be quickly eliminated from populations by natural selection. The occasional polymorphism for such inversions and their fixation among closely related species have supported the idea that genetic drift in very small populations can overcome natural selection in the wild. We studied the effect of 7 second-chromosome and 30 third-chromosome pericentric inversions on the fertility of heterokaryotypic Drosophila melanogaster females. Surprisingly, fertility was not significantly reduced in many cases, even when the inversion was quite large. This lack of underdominance is almost certainly due to suppressed recombination in inversion heterozygotes, a phenomenon previously observed in Drosophila. In the large sample of third-chromosome inversions, the degree of underdominance depends far more on the position of breakpoints than on the inversion's length. Analysis of these positions shows that this chromosome has a pair of ``sensitive sites' near cytological divisions 68 and 92: these sites appear to reduce recombination in a heterozygous inversion whose breakpoints are nearby. There may also be ``sensitive sites' near divisions 31 and 49 on the second chromosome. Such sites may be important in initiating synapsis. Because many pericentric inversions do not reduce the fertility of heterozyotes, we conclude that the observed fixation or polymorphism of such rearrangements in nature does not imply genetic drift in very small populations.