INVERSION POLYMORPHISM,LONGEVITY, AND BODY SIZE IN A NATURAL POPULATION OF DROSOPHILA BUZZATII

In this study we present the results of an analysis of differential longevity associated with Drosophila buzzatii second chromosome inversion karyotypes based on the assessment of more than 1000 individuals collected in a natural population. Comparisons of inversion frequencies between emerged and bait-collected flies showed not only that inversion arrangements were associated with differential longevity, but also that selection was sex specific. Because each individual fly was scored for thorax length and karyotype, we were able to show that longevity selection favoring larger flies coupled with the average effect of inversions on thorax length can account for the change of inversion frequencies due to longevity in females. The observed genotypic-by-sex interaction could be an important mechanism involved in the maintenance of the polymorphism. Arrangement 2Jz³, which was shown to impaired fecundity in two independent previous studies, exhibited a positive effect on longevity. This pattern of negative pleiotropy may be another plausible mechanism accounting for the maintenance of the polymorphism.     

The adaptive significance of chromosomal inversion polymorphisms in Drosophila melanogaster

Chromosomal inversions, structural mutations that reverse a segment of a chromosome, cause suppression of recombination in the heterozygous state. Several studies have shown that inversion polymorphisms can form clines or fluctuate predictably in frequency over seasonal time spans. These observations prompted the hypothesis that chromosomal rearrangements might be subject to spatially and/or temporally varying selection. Here, we review what has been learned about the adaptive significance of inversion polymorphisms in the vinegar fly Drosophila melanogaster, the species in which they were first discovered by Sturtevant in 1917. A large body of work provides compelling evidence that several inversions in this system are adaptive; however, the precise selective mechanisms that maintain them polymorphic in natural populations remain poorly understood. Recent advances in population genomics, modelling and functional genetics promise to greatly improve our understanding of this long‐standing and fundamental problem in the near future.     

Individual inversions or their combinations: which is the main selective target in a natural population of Drosophila subobscura?

It is generally accepted that chromosomal inversions have been key elements in adaptation and speciation processes. In this context, Drosophila subobscura has been, and still is, an excellent model species due to its rich chromosomal polymorphism. In this species, many analyses from natural populations have demonstrated the adaptive potential of individual inversions (and their overlapped combinations, the so‐called arrangements). However, little information is available on the evolutionary role of combinations generated by inversions located in homologous and nonhomologous chromosomes. The aim of this research was to ascertain whether these combinations are also a target for natural selection. For this objective, we have studied the inversion composition of homologous and nonhomologous chromosomes from a D. subobscura sample collected in a well‐studied population, Mount Avala (Serbia). No significant deviation from H‐W expectations was detected, and when comparing particular karyotypic combinations, likelihood ratios close to 1 were obtained. Thus, it seems that for each pair of homologous chromosomes inversions no deviation from randomness was detected. Finally, no linkage disequilibrium was observed between inversions located in different chromosomes of the karyotype. For all these reasons, it can be assumed that, at the cytological level, the individual inversions rather than their combinations in different chromosomes are the main target of selection.     

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.     

A negative association between horn length and survival in a weakly dimorphic ungulate

While all models of sexual selection assume that the development and expression of enlarged secondary sexual traits are costly, males with larger ornaments or weapons generally show greater survival or longevity. These studies have mostly been performed in species with high sexual size dimorphism, subject to intense sexual selection. Here, we examined the relationships between horn growth and several survival metrics in the weakly dimorphic Pyrenean chamois (Rupicapra pyrenaica). In this unhunted population living at high density, males and females were able to grow long horns without any apparent costs in terms of longevity. However, we found a negative relationship between horn growth and survival during prime age in males. This association reduces the potential evolutionary consequences of trophy hunting in male chamois. We also found that females with long horns tended to have lower survival at old ages. Our results illustrate the contrasting conclusions that may be drawn when different survival metrics are used in analyses. The ability to detect trade‐off between the expression of male secondary sexual traits and survival may depend more on environmental conditions experienced by the population than on the strength of sexual selection.     

Mutation Load in Sunflower Inversions Is Negatively Correlated with Inversion Heterozygosity

Recombination is critical both for accelerating adaptation and purging deleterious mutations. Chromosomal inversions can act as recombination modifiers that suppress local recombination in heterozygotes and thus, under some conditions, are predicted to accumulate such mutations. In this study, we investigated patterns of recombination, transposable element abundance, and coding sequence evolution across the genomes of 1,445 individuals from three sunflower species, as well as within nine inversions segregating within species. We also analyzed the effects of inversion genotypes on 87 phenotypic traits to test for overdominance. We found significant negative correlations of long terminal repeat retrotransposon abundance and deleterious mutations with recombination rates across the genome in all three species. However, we failed to detect an increase in these features in the inversions, except for a modest increase in the proportion of stop codon mutations in several very large or rare inversions. Consistent with this finding, there was little evidence of overdominance of inversions in phenotypes that may relate to fitness. On the other hand, significantly greater load was observed for inversions in populations polymorphic for a given inversion compared to populations monomorphic for one of the arrangements, suggesting that the local state of inversion polymorphism affects deleterious load. These seemingly contradictory results can be explained by the low frequency of inversion heterozygotes in wild sunflower populations, apparently due to divergent selection and associated geographic structure. Inversions contributing to local adaptation represent ideal recombination modifiers, acting to facilitate adaptive divergence with gene flow, while largely escaping the accumulation of deleterious mutations.     

Sex differences in ageing in natural populations of vertebrates

In many long-lived vertebrates (including humans), adult males have shorter lifespans than adult females, partly as a result of higher annual rates of mortality in males and partly owing to sex differences in the rate of ageing. A probable explanation of the evolution of sex differences in ageing is that, in polygynous species, intense intrasexual competition between males restricts the number of seasons for which individual males are able to breed successfully, weakening selection pressures favouring adult longevity in males relative to females. If this is the case, sex differences in adult longevity and in the onset and rate of senescence should be greater in polygynous species than in monogamous ones and their magnitude should be related to the duration of effective breeding males compared with females. Here, we use data from longitudinal studies of vertebrates to show that reduced longevity in adult males (relative to females) is commonly associated with a more rapid decline in male than female survival with increasing age and is largely confined to polygynous species. The magnitude of sex differences in adult longevity in different species is consistently related to the magnitude of sex differences in the duration of effective breeding, calculated across surviving adults. Our results are consistent with the suggestion that sex differences in senescence in polygynous species are a consequence of weaker selection for longevity in males than females.     

INVERSION LENGTH AND BREAKPOINT DISTRIBUTION IN THE DROSOPHILA BUZZATII SPECIES COMPLEX: IS INVERSION LENGTH A SELECTED TRAIT?

Length and position of breakpoints are characteristics of inversions that can be precisely determined on the polytene chromosomes of Drosophila species, and they provide crucial information about the processes that govern the origin and evolution of inversions. Eighty-six paracentric inversions described in the Drosophila buzzatii species complex and 18 inversions induced by introgressive hybridization in D. buzzatii were analyzed. In contrast to previous studies, inversion length and breakpoint distribution have been considered simultaneously. We conclude that: (1) inversion length is a selected trait; rare inversions are predominantly small while evolutionarily successful inversions, polymorphic and fixed, are predominantly intermediate in length; a nearly continuous variation in length, from small to medium sized, is found between less and more successful inversions; (2) there exists a significant negative correlation between length and number of polymorphic inversions per species which explains 39% of the inversion length variance; (3) natural selection on inversion length seems the main factor determining the relative position of breakpoints along the chromosomes; (4) the distribution of breakpoints according to their band location is non-random, with chromosomal segments that accumulate up to eight breakpoints.     

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.     

Behavioral genetics of Drosophila ananassae

Drosophila ananassae has a unique status among Drosophila species because of certain peculiarities in its genetic behavior. The most unusual feature of this species is its relatively high frequency of spontaneous male recombination. The results of studies on non-sexual behavior, such as phototactic responses, eclosion rhythm, and preferences for oviposition and pupation sites, lead us to suggest that this behavior is under polygenic control, with a substantial amount of additive genetic variation. Sexual isolation has been reported in D. ananassae with the degree of such isolation being stronger in isofemale lines than in natural populations. The significant variations seen in the mating propensity of several isofemale strains, inversion karyotypes and wild type strains, the diminishing effects of certain mutations on the sexual activity of males, and the positive responses to selection for high and low mating propensity point to a genetic control of sexual behavior in D. ananassae. Males contribute more to variation and thus are more subject to intrasexual selection than females. There is a positive correlation between sternopleural bristle number, mating propensity and fertility in D. ananassae. This correlation between morphometric traits and mating success suggests that larger flies are more successful in mating than smaller ones. There is also evidence for adaptive plasticity and a trade-off between longevity and productivity in D. ananassae. Rare, specific courtship song parameters that provide males with a mating advantage have also been reported in different geographic strains of D. ananassae. The remating behavior of males and females, sperm displacement, and the bi-directional selection for female remating speed indicate that post-mating behavior in this species may also be under genetic control. The occurrence of size assortative mating further indicates that there is size-dependent sexual selection in D. ananassae.     

Chromosomal inversions effect body size and shape in different breeding resources in Drosophila buzzatii

The cactophilic Drosophila buzzatii provides an excellent model for the study of reaction norms across discrete environments because it breeds on rotting tissues (rots) of very different cactus species. Here we test the possible effects of second chromosome inversions on body size and shape (wing loading) across suitable natural breeding substrates. Using homokaryotypic stocks derived from several lines homozygous for four naturally occurring chromosomal inversions, we show that arrangements significantly affect size-related traits and wing loading. In addition, karyotypes show differing effects, across natural breeding resources, for wing loading. The 2st and 2jz(3) arrangements decrease and the 2j arrangement increases wing loading. For thorax length and wing loading, karyotypic correlations across host plants are slightly lower in females than in males. These results support the hypothesis that these traits have a genetic basis associated with the inversion polymorphism.     

The role of genic selection in the establishment of inversion polymorphism in Drosophila subobscura

A model for explaining the establishment of newly arisen inversions in natural populations, in which the inverted segment may be selected for if its load of deleterious mutations is smaller than the average load of the noninverted segment in the population, is tested for Drosophila subobscura. The results show that for new inversions, originally with no deleterious alleles, the expected cumulative distribution of inversion lengths fits fairly well with the observed one. Therefore, genic selection may be an important cause of the establishment of newly arisen inversions in natural populations of D. subobscura. The applicability of the model to the maintenance of the inversion polymorphism present in this species; is discussed.     

Population and behaviour genetics of Drosophila ananassae

Drosophila ananassae is a cosmopolitan and domestic species. It occupies a nuique status among the Drosophila species due to certain peculiarities in its genetic behaviour. The most unusual feature of this species is spontaneous male recombination in appreciable frequency. The present review summarises the work done on population and behaviour genetics of D. ananassae from India. Population dynamics of three cosmopolitan inversions has been studied in Indian population of D. ananassae and it is evident from the results that there is a considerable degree of genetic divergence at the level of inversion polymorphism. In general, the populations from south India show more differentiation than those from the north. These three cosmopolitan inversions, which are coextensive with the species, exhibit heterosis. Interracial hybridization does not lead to beaakdown of heterosis, which suggests that evidence for coadaptation is lacking in geographic populations of D. ananassae. Heterosis appears to be simple luxuriance rather than populational heterosis (coadaptation). Unlinked inversions occur in random associations, indicating no interchromosomal interactions. However, two inversions of the third chromosome often show strong linkage disequilibrium in laboratory populations, which is due to epistatic gene interaction and suppression of crossing-over. Genetic variations for certain allozyme polymorphism and sternoleural bristle phenotypes in Indian populations of D. ananassae have also been observed.A number of investigations have also been carried out on certain aspects of behaviour genetics of Indian D. ananassae. There is evidence for sexual isolation within D. ananassae. Significant variations in mating propensity of several isofemale strains, inversion karyotypes, the diminishing effects of certain mutations on sexual activity of males and positive response to selection for high and low mating propensity provide evidence for genetic control of sexual behaviour in D. ananassae. Males contribute more to variation and thus are more subject to intra-sexual selection than females. Evidence for rare male mating advantage has also been presented. Geographic strains of D. ananassae show variation with respect to oviposition site preference. The results of studies on pupation site preference, which is an important component of larval behaviour, suggest that larval pupation behaviour in D. ananassae is under polygenic control with a substantial amount of additive genetic variation.     

Recombination rate predicts inversion size in Diptera.

Most species of the Drosophila genus and other Diptera are polymorphic for paracentric inversions. A common observation is that successful inversions are of intermediate size. We test here the hypothesis that the selected property is the recombination length of inversions, not their physical length. If so, physical length of successful inversions should be negatively correlated with recombination rate across species. This prediction was tested by a comprehensive statistical analysis of inversion size and recombination map length in 12 Diptera species for which appropriate data are available. We found that (1) there is a wide variation in recombination map length among species; (2) physical length of successful inversions varies greatly among species and is inversely correlated with the species recombination map length; and (3) neither the among-species variation in inversion length nor the correlation are observed in unsuccessful inversions. The clear differences between successful and unsuccessful inversions point to natural selection as the most likely explanation for our results. Presumably the selective advantage of an inversion increases with its length, but so does its detrimental effect on fertility due to double crossovers. Our analysis provides the strongest and most extensive evidence in favor of the notion that the adaptive value of inversions stems from their effect on recombination.     

Investigating latitudinal clines for life history and stress resistance traits in Drosophila simulans from eastern Australia

Latitudinal clines have been demonstrated for many quantitative traits in Drosophila and are assumed to be due to climatic selection. However, clinal studies are often performed in species of Drosophila that contain common cosmopolitan inversion polymorphisms that also show clinal patterns. These inversion polymorphisms may be responsible for much of the observed clinal variation. Here, we consider latitudinal clines for quantitative traits in Drosophila simulans from eastern Australia. Drosophila simulans does not contain cosmopolitan inversion polymorphisms, so allows the study of clinal selection on quantitative traits that are not confounded by associations with inversions. Body size showed a strong linear cline for both females and males. Starvation resistance exhibited a weak linear cline in females, whereas chill-coma recovery exhibited a significant nonlinear cline in females only. No clinal pattern was evident for development time, male chill-coma recovery, desiccation or heat resistance. We discuss these results with reference to the role inversion polymorphisms play in generating clines in quantitative traits of Drosophila.     

THE EVOLUTIONARY HISTORY OF DROSOPHILA BUZZATII. VIII. EVIDENCE FOR ENDOCYCLIC SELECTION ACTING ON THE INVERSION POLYMORPHISM IN A NATURAL POPULATION

The pattern of selection acting in nature on the chromosomal polymorphism of the cactophilic species Drosophila buzzatii was investigated by comparing inversion and karyotypic frequencies through four different life-cycle stages: adult males, eggs, third-instar larvae, and immature adults. All population samples were obtained in June 1981 at an old Opuntia ficus-indica plantation near Carboneras, Spain. The analysis rests on several assumptions which are explicitly set forth and discussed. The results, if these assumptions prove true, indicate strong directional selection for larval viability acting on the second-chromosome karyotypes and also suggest selective differences in fecundity and longevity. Heterotic selection, however, cannot be ruled out for other fitness components such as male mating success. This kind of selection could be operating on the fourth-chromosome polymorphism as well. Some gene arrangements showed significant and opposite changes in frequency at different parts of the life cycle, thus demonstrating endocyclic selection.     

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.     

Evolutionary genetics of Drosophila ananassae. I. Effect of selection on body size and inversion frequencies

Adaptive importance of inversion polymorphism has been discussed in Drosophila species at several levels but no study has been carried out demonstrating the individual and combined effects of polymorphic inversions on the fitness of flies through bi‐directional selection. Therefore, artificial bi‐directional selection for thorax length in Drosophila ananassae was carried out for 10 generations. Both, Tukey test for selection difference and regression coefficients of offspring on mid‐parent are highly significant. The realized heritability (h²) in males of both high and low selection lines is more or less similar but is more pronounced in low line females, which suggests the asymmetrical response. This asymmetry in selection is discussed in the light of evidence provided by the study of chromosome inversion frequencies in different selection lines at different generations of selection. Interestingly, chromosome inversion frequency changes towards homozygosity for different gene arrangements in different selection lines. Tests of correlations at G₆ and G₁₀ among different gene arrangements as well as with mean thorax length suggest that 2L‐ST gene arrangement is negatively correlated, while 3L‐ST gene arrangement is positively correlated with thorax length. Furthermore, the present study shows the significant effects of 3L‐ST and 2L + 3L (positive correlation) on thorax length, while 3R‐ST and 2L + 3R show significant effect (negative correlation) on thorax length, which was not evident in the previous study. Present results also suggest how polymorphic inversions and their combinations affect the body size differently in different selection lines. These results suggest that thorax length in D. ananassae is under polygenic control and inversion polymorphism plays crucial role in maintaining body size by modifying genotypic frequency under various selection pressures.     

Drosophila bipectinata species complex

The Drosophila bipectinata species complex belongs to the ananassae subgroup of the melanogaster species group (Genus Drosophila, Subgenus Sophophora). The members of the complex are: D. bipectinata, D. parabipectinata, D. malerkotliana, and D. pseudoananassae. Of the four species, D. bipectinata is most widely distributed. Females are indistinguishable, but males are distinguishable by their sex-comb teeth number and pattern and by abdominal colouration. Chromosomal inversions have been detected in these species. In natural populations of D. bipectinata the frequency of inversions and the level of inversion heterozygosity were found to be very low but in laboratory stocks inversions persisted for more than 20 generations due to heterotic buffering. On an average 9.3 fixed interspecific inversions separate each species pair. Non-random association between linked inversions indicated epistatic interaction in natural populations of D. bipectinata. Certain spontaneous mutations were detected and mapped for the first time in D. bipectinata. Low frequency of spontaneous male recombination has also been reported in D. bipectinata. Sexual isolation study in the complex indicated strong preference for homogamic mating. The results also indicated incomplete sexual isolation among different members of this complex. The isolation estimate among six different geographic populations of D. bipectinata ranged from 0.54 - 0.92 representing positive assortative mating which is an evidence for incipient sexual isolation. Incipient sexual isolation was also found within D. malerkotliana and D. parabipectinata . Chromosomal, hybridization and allozyme studies revealed close phylogenetic relationship among the four species of the bipectinata complex. Mitochondrial DNA study revealed net nucleotide difference (delta) between these species to be very small (0.0002 +/- 0.0008) reflecting closeness. Evidence for genetic control of sexual activity and existence of sexual selection in D. bipectinata has been shown on the basis of mating propensity tests carried out on geographic strains, their hybrids and diallel crosses. Significant variation was found among the strains tested with respect to courtship time, duration of copulation and fertility. A positive correlation between duration of copulation and fertility in D. bipectinata was found. Evidence for rare-male mating advantage was also found in D. bipectinata. A positive response to selection for high and low mating activity provided evidence for polygenic control of this phenomenon in D. bipectinata. Bilateral outgrowths on thorax, a unique phenotype, reported for the first time in D. bipectinata has been shown to affect mate recognition ability. Results of the study on pupation site preference (larval behaviour) and oviposition site preference (non-sexual behaviour) have also been included.     

Effects of Chromosomal Inversion on Cell Fitness in Escherichia Coli K-12

In an effort to learn what factors might mitigate the establishment of Escherichia coli variants bearing major chromosomal rearrangements, we have examined the effects on cell growth of two inversions between rRNA operons. One of these inversions, IN(rrnD-rrnE), had been propagated in a commonly used subline of E. coli K-12 for approximately 30 yr before its discovery, a fact that illustrates the absence of obvious detrimental effects associated with the inversion. We found that culturing under conditions requiring repeated transition from stationary phase to rapid growth led to the replacement of IN(rrnD-rrnE) cells by cells that had undergone either of two types of additional chromosomal inversion: one type fully restored the wild-type order, while the other partially restored it. The partial reinversion was also between rrn operons, but it left a small transposition. The tendency for overgrowth by these revertants persisted through several rounds of periodic selection. In contrast, the other inversion, IN(rrnG-rrnE), was associated with severe, detrimental effects. The effects of IN(rrnG-rrnE) were also alleviated by full or partial reinversion. The probable relationship between the severity of the effects caused by the inversions and the degree of displacement of the replication origin is discussed. Spontaneous inversion events between rrn operons separated by 18% of the chromosome were estimated to occur at a frequency of roughly 10(-5). If extended to natural situations, the growth disadvantage together with the relatively high frequency of reinversion suggest that clones of cells with an inversion between these rrn operons would be readily overgrown by revertants.