Genetic load and coadaptation of chromosomal inversions. II. O-chromosomes in Drosophila subobscura populations

We have analysed the inversion polymorphism and genetic load of O-chromosomes in three populations of D. subobscura from southeastern Europe. As expected for a central populations the inversion polymorphism was extensive. In a like fashion, the genetic load, in particular the frequency of lethals, was heavy in all three populations. There were significant differences in the frequency of moderately deleterious genes. These differences in viability can be attributed to balancing selection. A comparison of these two kinds of genetic polymorphism indicates that there are differences in mean viability among different gene arrangements of O-chromosomes in the three populations. The differences observed are due to an unequal distribution of various viability classes among O-chromosome gene arrangements. We here show for the first time a specific distribution of lethal genes among these arrangements within the Palearctic distribution area of D. subobscura. The lethal allelism test showed lethals are non-randomly associated with the Ost gene arrangement. The amount of genetic load is heavy in gene arrangements with a high frequency, in comparison with the ones with a low frequency. Lethal genes may be protected in combinations of low and moderate frequency gene arrangements that harbor more lethal genes, as the Ost in the one population. Some arrangements that are less protected against recombination have a higher load than ones that are more protected against recombination. This can be taken as evidence for coadaptation.     

The lack of evidence for coadaptation in geographic populations of Drosophila ananassae

Crosses were made between geographic races of Drosophila ananassas from different localities in India. All these strains employed in the present experiments were polymorphic for the gene arrangements in the second chromosome due to the occurrence of alpha (subterminal) inversion. After ten generations it was observed that the heterozygotes were the most superior genotype and their frequencies remained above fifty percent in all these strains which served as controls and in the hybrid populations of mixed geographic origin. Thus it was found that interracial hybridization does not lead to breakdown of heterosis. The chief conclusion from these experiments is that evidence for coadaptation is lacking in D. ananassae. This finding apparently conflicts with what has been claimed for other species.     

Frequency of chromosome polymorphism for pericentric inversions and B-chromosomes in Spanish populations of Rattus rattus frugivorus

Inversion frequencies in chromosomes 16 and 18 and B-chromosome frequency have been studied in three populations of Rattus rattus frugivorus.In two of these, Cuenca and San Pedro del Pinatar, the frequencies of homozygous and heterozygous individuals do not differ significantly from the Hardy-Weinberg equilibrium for both chromosome pairs. By contrast, in the Vega de Granada population there are fewer heterozygous and more homozygous individuals than expected on the basis of the Hardy-Weinberg distribution, although the frequency distributions of karyotypes in these three populations are not significantly different.In relation to the B chromosome, the Cuenca and San Pedro populations have frequencies of B-carrying animals of 0.25 and 0.22 respectively, the Vega de Granada population of 0.80.     

Evidence for coadaptation in geographic populations of Drosophila bipectinata

In order to test whether there is genetic coadaptation in geographic populations of Drosophila bipectinata with respect to body size, reciprocal crosses were made among five strains derived from ecogeographically different localities in India. Wing length was used as an index of body size, and was measured in all the five strains, and their crosses in F and F₂ generations. The statistical analysis of the data show that there is significant interpopulation variation in body size and in all the crosses, there is an increase in body size in F₁ generation when compared with mid-parent value. Further, there is a decrease in body size in F₂ generation as compared to F₁ in most of the crosses with increased variability. These results provide evidence for genetic coadaptation in geographic populations of D. bipectinata .     

Genetic coadaptation in the chromosomal polymorphism of Drosophila subobscura II. Changes of gametic disequilibrium in experimental populations

Experimental populations were examined for temporal changes of gametic disequilibria between allozyme loci (Lap and Pept-1) and gene arrangements of the O chromosome of Drosophila subobscura (O _st and O ₃₊₄₊₇) under several environmental conditions. In the foundation of the experimental populations a genetic perturbation was carried out in order to test the relevance of the current hypotheses used to explain the allozyme-inversion associations observed in natural populations. Differential changes of gametic disequilibria were detected over generations under the different environmental conditions. Mere mechanical or stochastic factors cannot explain the results and natural selection is probably the major agent generating the detected gametic associations. The observations are interpreted as a proof of coadaptation of D. subobscura inversions.     

The coadaptation of parental supply and offspring demand

The evolution of parent-offspring interactions for the provisioning of care is usually explained as the phenotypic outcome of resolved conflicting selection pressures. However, parental care and offspring solicitation are expected to have complex patterns of inheritance. Here we present a quantitative genetic model of parent-offspring interactions that allows us to investigate the evolutionary maintenance of a state of resolved conflict. We show that offspring solicitation and parental provisioning are expected to become genetically correlated through coadaptation and that their genetic architecture is dictated by an interaction between patterns of selection and the proximate mechanisms regulating supply and demand. When selection is predominately on offspring solicitation, our model suggests that the genetic correlations between provisioning and solicitation are usually positive if provisioning reduces solicitation. Conversely, when selection is predominately on parental provisioning, the correlations are mostly negative as long as parents show a positive response to offspring demand. Empirical estimates of the genetic architecture of traits involved in family interactions fit these predictions. Our model demonstrates how the evolutionary maintenance of parent-offspring interactions can result in variable patterns of coadaptation, and it provides an explanation for the diversity of family interactions within and among species.     

The interchromosomal effect of inversions in maize

Summary The interchromosomal effect of inversions in maize along the short arm of chromosome 9 yields results which are distinctly different from those which are reported with Drosophila melanogaster. Recombination was increased in the c ₁-sh₁ region of chromosome 9 while the sh ₁-wx region was unaffected. This increased frequency of recombination appears to be due to an increase in single exchange events as multiple events were unchanged. Increases in recombination were accompanied by either an increase in chromosome interference or normal interference levels. The magnitude of increase in recombination was much smaller than that seen in interchromosomal effects in Drosophila and is consistent with other observations made in maize. When two inversions were present in the same nucleus simultaneously, the effect on recombination was of the same magnitude as the effect of a single inversion. All inversions tested, regardless of size or position with respect to the centromere showed the same magnitude of increase.     

A maternal-offspring coadaptation theory for the evolution of genomic imprinting

Imprinted genes are expressed either from the maternally or paternally inherited copy only, and they play a key role in regulating complex biological processes, including offspring development and mother–offspring interactions. There are several competing theories attempting to explain the evolutionary origin of this monoallelic pattern of gene expression, but a prevailing view has emerged that holds that genomic imprinting is a consequence of conflict between maternal and paternal gene copies over maternal investment. However, many imprinting patterns and the apparent overabundance of maternally expressed genes remain unexplained and may be incompatible with current theory. Here we demonstrate that sole expression of maternal gene copies is favored by natural selection because it increases the adaptive integration of offspring and maternal genomes, leading to higher offspring fitness. This novel coadaptation theory for the evolution of genomic imprinting is consistent with results of recent studies on epigenetic effects, and it provides a testable hypothesis for the origin of previously unexplained major imprinting patterns across different taxa. In conjunction with existing hypotheses, our results suggest that imprinting may have evolved due to different selective pressures at different loci.     

The meiotic behaviour of inversions in polyploid aloineae

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

Evolution of coadaptation in a subdivided population

The interplay between population subdivision and epistasis is investigated by studying the fixation probability of a coadapted haplotype in a subdivided population. Analytical and simulation models are developed to study the evolutionary fate of two conditionally neutral mutations that interact epistatically to enhance fitness. We find that the fixation probability of a coadapted haplotype shows a marked increase when the population is genetically subdivided and subpopulations are loosely connected by migration. Moderate migration and isolation allow the propagation of the mutant alleles across subpopulations, while at the same time preserving the favorable allelic combination established within each subpopulation. Together they create the condition most favorable for the ultimate fixation of the coadapted haplotype. On the basis of the analytical and simulation results, we discuss the fundamental role of population subdivision and restricted gene flow in promoting the evolution of functionally integrated systems, with some implications for the shifting-balance theory of evolution.     

Chromosomal inversions and genetic control revisited: the use of inversions in sexing systems for higher Diptera

Summary Genetic sexing systems based on sex-linked translocations and deleterious mutations are subject to breakdown from genetic recombination in males. Including inversions in these strains may provide a solution to this problem, by ensuring selective elimination of recombinant products. Inversions could be used either in coupling to or in repulsion to the translocation. The latter system, requiring homozygous-viable inversions, would be more difficult to construct, but would offer several advantages not available with coupled translocation/inversion systems. A system proposed for the blowfly Lucilia cuprina is outlined, which combines homozygous-viable pericentric inversions in repulsion to existing sex-linked translocations. This system should both stabilize the genetic sexing system and increase the suppressive potential of such strains.     

Inversion polymorphism of the malarial mosquito Anopheles messeae. V. The interaction of different chromosomal inversions in the spatial area

The relations between inversions of chromosome XL, 2R, 3R, 3L from 8 populations of the central part and periphery of the species area were studied. 2-, 3- and 4-factor analysis was carried out. Interaction of inversions XL1, 2R1, 3R1 in central populations (Riga, Moscow, Tomsk) was observed. The nonrandom association of definite inversional genotypes was stationary in spatial - temporary. The phylogenetic initial sequences XL0, 2R0, 3R0 display "+" interaction. The 3-factor analysis of populations of Tomsk shows: 1) interaction of inversions is more essential in males than in females; 2) the statistically significant interaction of 3-4 inversions is not always determined by the effect of 2-factor analysis; 3) the chromosome 3R has a dominance influence on the pattern of association of the multiinversional complex. These data support the hypothesis that differential selection for chromosomes with certain combinations of arrangements is mainly responsible for this phenomenon. In peripheral area populations (Syctyvkar, Irkutsk, Chita), no associations were observed (2R and 3R). When they do take place, their character is changed (Kiev - XL and 3R). This phenomenon may be explained by the influence of frequency-dependent selection.     

Coalescent patterns for chromosomal inversions in divergent populations

Chromosomal inversions allow genetic divergence of locally adapted populations by reducing recombination between chromosomes with different arrangements. Divergence between populations (or hybridization between species) is expected to leave signatures in the neutral genetic diversity of the inverted region. Quantitative expectations for these patterns, however, have not been obtained. Here, we develop coalescent models of neutral sites linked to an inversion polymorphism in two locally adapted populations. We consider two scenarios of local adaptation: selection on the inversion breakpoints and selection on alleles inside the inversion. We find that ancient inversion polymorphisms cause genetic diversity to depart dramatically from neutral expectations. Other situations, however, lead to patterns that may be difficult to detect; important determinants are the age of the inversion and the rate of gene flux between arrangements. We also study inversions under genetic drift, finding that they produce patterns similar to locally adapted inversions of intermediate age. Our results are consistent with empirical observations, and provide the foundation for quantitative analyses of the roles that inversions have played in speciation.     

Paracentric inversions in man

Summary The Leuven cytogenetic center experience on paracentric inversions in man is discussed. From a total of 51,000 patients, referred for constitutional chromosome analysis during the period 1970–1985, paracentric inversions were found in 18 index patients. A puzzling finding is the high incidence (26%) of mental retardation and/or congenital malformation in the inversion carrier offspring of phenotypically normal parents with identical chromosomal rearrangements. There was also a high incidence of early fetal loss in the inversion carrier parents. This finding may be explained by an increase of chromosomally unbalanced gametes which result from crossing-over in the meiotic inversion loop. Finally, the possibility of an increased tendency to non-disjunction in paracentric inversion carrier parents is discussed. The most frequent paracentric inversion was inv(3)(p13p25); it was detected in seven unrelated index patients. According to the present experience and the literature data, the breakpoints in paracentric inversions seem to occur preferentially at 1p22, 1p36, 3p13, 3p25, 7q11, and 7q22 regions.     

Colour polymorphism in Drosophila mediopunctata: genetic (chromosomal) analysis and nonrandom association with chromosome inversions

The presence of three dark spots on the abdomen is typical of the tripunctata group of Drosophila, which is the second largest Neotropical group, with 56 species. In some species, such as D. mediopunctata, the colour pattern varies considerably: ranging from flies showing no spots up to flies with three dark spots. In this paper, we present a genetic (chromosomal) analysis of this character showing that this colour polymorphism is genetically determined mainly by the second chromosome. Since this chromosome is the most polymorphic for inversions in this species, we also examined the influence of the inversions on this character. We used strains in which different second chromosomes were placed on the same genetic background and the offspring between them. We found a nonrandom association between the number of spots and the inversions PA0 and PC0. Thus, our results are consistent with the idea that the factors or genes determining a conspicuous polymorphism are likely to be associated, forming a supergene, and this association would be most efficiently accomplished through a chromosome inversion. Moreover, this is the first time that an association between a conspicuous morphological polymorphism and chromosome inversions has been described.     

Evolution of coadaptation in a two-locus epistatic system

Although recent advances in genome biology have dramatically increased our understanding of the contribution of gene interactions to the development of complex phenotypes, we still lack general agreement on the process and mechanisms responsible for the evolution of epistatic systems. Even if genes in a species are indeed integrated into coadapted complexes of interacting components, simple additive evolution may eventually result in epistatic differentiation of populations. Consequently, the prevalence of epistatic gene action does not tell us anything about the role of epistatic selection in the history of population divergence. To elucidate the contribution of epistatic selection in the evolution of coadaptation, we investigate the fixation process of two mutations that interact synergistically to enhance fitness. We show by diffusion analysis and simulations that epistatic selection on cosegregating variants does not by itself promote the evolution of epistatic systems; rather, accumulation of neutral mutations may play a crucial role, creating an appropriate genetic milieu for adaptive evolution in the future generations.