Geographical variation of chromosomal structure in Drosophila gasici

Summary Drosophila gasici Brncic 1957, is a neotropical species found in several parts of the Andes Mountain System. By means of the analysis of their external characteristics, chromosomes and hybridization test they have been included in the mesophragmatica group of species of the sub-genus Drosophila.The present paper describes the mitotic and polytene chromosomes of D. gasici from samples of natural populations collected at Bogotá (Colombia), Cochabamba (Bolivia), Arica (Chile) and San Luis (Argentina). The comparative study of all these populations has disclosed that the species has split in well defined geographic races. The Colombian and Chilean flies differ from those living in Bolivia and Argentina by three independent inversions in chromosome I (the sexual pair). The only polymorphic populations seem to be the Chilean ones which exhibit two inversions in the second chromosome, besides the Standard gene arrangement. All the other populations are homozygous for all their chromosomal sequences. Studies on reproductive isolation have demonstrated that there is some sexual discrimination between the Colombian and Chilean flies in respect to the Bolivian and Argentinean ones.The populational structure of D. gasici is in contrast to that observed in the other six species belonging to the mesophragmatica group in which there are no good evidences of geographical variations at the chromosomal level.This article is dedicated to Professor Hans Bauer on the occasion of his 60th birthday.     

Chromosomal structure of populations of drosophila flavopilosa studied in larvae collected in their natural breeding sites

Summary D. flavopilosa Frey, is a neotropical species of Drosophila living in Chile that, together with 13 other species, has been included by Wheeler, Takada und Brncic (1962) in the flavopilosa species group. Despite the fact that it has not been possible to breed this species in the laboratory, the circumstance that its habitat is well known, has allowed the study of the chromosomal structure of some natural populations of this species, analyzing larvae directly taken to the laboratory from their natural breeding sites: the flowers of the solanacean Cestrum parqui L'Héritier.The present paper describes the mitetic and salivary gland chromosomes of D. flavopilosa, and gives a composite map of the Standard gene arrangement. In central Chile, natural populations of this species are polymorphic with respect to the gene orders in their chromosomes, due to the presence of four independent inversions, all located in one of the six chromosomes (the right arm of the V-chromosome). Quantitative data on the distribution of the inversions shows that there is an altitudinal gradient in the frequencies of two of the four inversions. Heterozygotes for Inversion A, are more frequent at high altitudes than at sea level. On the contrary, heterozygotes for inversion B, are abundant at sea level, but practically disappear at high altitudes. These altitudinal clines have been observed in two valleys near Santiago, Chile, which run from the Andes mountains to the Pacific coast.The work reported in this article has been carried out under Contract AT (30-1) 2465 US Atomic Energy Commission, and partially supported by Grants from the University of Chile, Faculty of Medicine and the Rockefeller Foundation under a joint program.     

Inversion polymorphism in Drosophila obscura

The inversion polymorphism of Drosophila obscura Fallen, a European species of the obscura group of the subgenus Sophophora, is described. A total of 21 inversions have been recorded; they are located in the five large chromosomes of the species (a dot chromosome is also present) and form 25 gene arrangements present in the species' natural populations. Strains from five different countries were studied. Two of these inversions were found to be pericentric, and the remaining were paracentric. The presence of "hot" points (multibreaks) was noticed. The distribution of the relative lengths of inversions conformed to the Van Valen-Levins distribution, contrary to what happens in D. subobscura. Observations also showed that there is no crossover inhibition between nonoverlapping inversions. The phylogeny of chromosome C was reconstructed; the existence of several arrangements not found was postulated; and the primitive gene arrangement, linking D. obscura to its closely related species was identified, as well as the primitive gene arrangements of the other chromosomes. Photographic maps of the chromosomes of D. obscura are provided here.     

Chromosomal variation in natural populations of Drosophila guaramunu

Summary Brazilian populations of D. guaramunu (Dobzhansky and Pavan, 1943) exhibit a high degree of chromosomal polymorphism. At least 19 inversions are known.These inversions have been found in the four long autosomes, while the X chromosome and the dot-shaped chromosomes do not show any variation in the gene sequences. Among the autosomes, the fourth chromosome seems to be the most variable one, 13 out of 19 inversions here reported being localized in it.With the aid of crosses to a homozygous Standard strain, it has been possible to establish schematically the phylogenetic relationships between the different gene arrangements.With 7 figures in the text and 1 plate.Research Fellow of the University of São Paulo, Brazil, in 1951.     

Genome‐wide tests for introgression between cactophilic Drosophila implicate a role of inversions during speciation

Models of speciation‐with‐gene‐flow have shown that the reduction in recombination between alternative chromosome arrangements can facilitate the fixation of locally adaptive genes in the face of gene flow and contribute to speciation. However, it has proven frustratingly difficult to show empirically that inversions have reduced gene flow and arose during or shortly after the onset of species divergence rather than represent ancestral polymorphisms. Here, we present an analysis of whole genome data from a pair of cactophilic fruit flies, Drosophila mojavensis and D. arizonae, which are reproductively isolated in the wild and differ by several large inversions on three chromosomes. We found an increase in divergence at rearranged compared to colinear chromosomes. Using the density of divergent sites in short sequence blocks we fit a series of explicit models of species divergence in which gene flow is restricted to an initial period after divergence and may differ between colinear and rearranged parts of the genome. These analyses show that D. mojavensis and D. arizonae have experienced postdivergence gene flow that ceased around 270 KY ago and was significantly reduced in chromosomes with fixed inversions. Moreover, we show that these inversions most likely originated around the time of species divergence which is compatible with theoretical models that posit a role of inversions in speciation with gene flow.     

How chromosomal rearrangements shape adaptation and speciation: Case studies in Drosophila pseudoobscura and its sibling species Drosophila persimilis

The gene arrangements of Drosophila have played a prominent role in the history of evolutionary biology from the original quantification of genetic diversity to current studies of the mechanisms for the origin and establishment of new inversion mutations within populations and their subsequent fixation between species supporting reproductive barriers. This review examines the genetic causes and consequences of inversions as recombination suppressors and the role that recombination suppression plays in establishing inversions in populations as they are involved in adaptation within heterogeneous environments. This often results in the formation of clines of gene arrangement frequencies among populations. Recombination suppression leads to the differentiation of the gene arrangements which may accelerate the accumulation of fixed genetic differences among populations. If these fixed mutations cause incompatibilities, then inversions pose important reproductive barriers between species. This review uses the evolution of inversions in Drosophila pseudoobscura and D. persimilis as a case study for how inversions originate, establish and contribute to the evolution of reproductive isolation.     

Genomics of natural populations: Evolutionary forces that establish and maintain gene arrangements in Drosophila pseudoobscura

The evolution of complex traits in heterogeneous environments may shape the order of genes within chromosomes. Drosophila pseudoobscura has a rich gene arrangement polymorphism that allows one to test evolutionary genetic hypotheses about how chromosomal inversions are established in populations. D. pseudoobscura has >30 gene arrangements on a single chromosome that were generated through a series of overlapping inversion mutations with >10 inversions with appreciable frequencies and wide geographic distributions. This study analyses the genomic sequences of 54 strains of Drosophila pseudoobscura that carry one of six different chromosomal arrangements to test whether (i) genetic drift, (ii) hitchhiking with an adaptive allele, (iii) direct effects of inversions to create gene disruptions caused by breakpoints, or (iv) indirect effects of inversions in limiting the formation of recombinant gametes are responsible for the establishment of new gene arrangements. We found that the inversion events do not disrupt the structure of protein coding genes at the breakpoints. Population genetic analyses of 2,669 protein coding genes identified 277 outlier loci harbouring elevated frequencies of arrangement‐specific derived alleles. Significant linkage disequilibrium occurs among distant loci interspersed between regions with low levels of association indicating that distant allelic combinations are held together despite shared polymorphism among arrangements. Outlier genes showing evidence of genetic differentiation between arrangements are enriched for sensory perception and detoxification genes. The data presented here support the indirect effect of inversion hypothesis where chromosomal inversions are favoured because they maintain linked associations among multilocus allelic combinations among different arrangements.     

Hybrid disadvantage in the larval foraging behaviour of the two neotropical species of <Emphasis Type="Italic">Drosophila pavani</Emphasis> and <Emphasis Type="Italic">Drosophila gaucha</Emphasis>

Flies from two populations of the Chilean endemic neotropical species Drosophila pavani and two populations of its sibling species Drosophila gaucha were crossed reciprocally to obtain intra- and interspecific hybrids. The developmental pathways of locomotor activity and feeding rate were analysed for eleven of twelve possible genotype groups. The hybrids showed reduced fitness indicated by a decrease in the measured traits. Hybrid disadvantage was strongest in interspecific hybrids, especially with respect to feeding behaviour. This evidence supports the contention that D. pavani and D. gaucha have evolved different coadapted gene pools controlling the developmental pathways for behavioural traits expressed during larval foraging; but genetic divergence affecting these behaviours has also taken place between locally adapted populations within each species.     

A comparative study of the chromosomes in the incipient species of the Drosophila paulistorum complex

Summary Drosophila paulistorum Dobzhansky et Pavan is a complex of six races or incipient species. The races are mostly allopatric, but they are reproductively isolated sufficiently to permit them to exist also sympatrically in some places. The gene arrangements in the chromosomes of the races have been compared by means of examination of the giant chromosomes in the larval salivary glands; 28 strains of all races, and about an equal number of interracial hybrids have been studied.Chromosomal inversion polymorphism has been discovered in all races, even in the Guianan race of which only a single strain is available. Inversion heterozygotes are found in every one of the five chromosomal strands which the species has. Interracial hybrids tend to be heterozygous for more inversions than are present in the strains of the parental races. The Transitional race has however much the same gene arrangements as the widespread Andean — South Brazilian race.With the exception of the Transitional race, and of three other possible exceptions, each race has a collection of its own race-specific inversion polymorphs, not found in the other races. This very striking finding is discussed in connection with the hypothesis which envisages the origin of new species from marginal colonies at the periphery of the geographic distribution area of the ancestral species.The work reported in this article has been carried under Contract No. AT-(30-1)-1151, U.S. Atomic Energy Commission, mostly at the Department of Zoology, Columbia University, New York.     

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 banding pattern of polytene chromosomes of Drosophila guanche compared with that of D. subobscura

A detailed map of the salivary gland chromosomes of Drosophila guanche is presented and compared to the standard gene arrangements of D. subobscura. Generally, the polytene chromosomc banding patterns of the two species show a high degrce of homology. Only Segment I of the sex chromosome (Chromosome A) shows marked differences. The banding pattern proposed for this segment in D. guanche could have originated from a cluster of overlapping inversions including A₁ arrangement.     

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.     

Chromosomal polymorphism in two species of the guarani group of drosophila

Summary Studies of chromosomal polymorphism in natural populations of D. guaramunu and D. griseolineata in Rio Grande do Sul, Brazil, confirmed and extended previous findings in these species. The more common D. guaramunu is much more polymorphic than its closest but less common relative D. griseolineata. In the former species, the frequencies of four inversions showed differences from locality to locality, and five inversions of the same species showed temporal changes in the population of Bexiga. It was not possible to correlate the differences with any particular factor in the environment, though the temporal changes were perhaps due to seasonal climatic cycles.Inversion heterosis was not evident in either species — instead, inversion Ee of D. guaramunu was found to be less frequent than expected on the basis of the Hardy-Weinberg equilibrium in the localities of Emboaba, Bexiga and Feliz. The implications of these findings are discussed.Fellow of the Conselho Nacional de Pesquisas.     

Chromosomal inversion polymorphism of Drosophila subobscura populations from Jastrebac Mountain shows temporal and habitat-related changes

Inversion polymorphism in populations of D. subobscura from a beech forest on Jastrebac mountain was studied in June 1990, 1993, and 1994, respectively. The same analysis was performed in 1990 for D. subobscura populations in a beech forest and an oak forest in the same region. Statistically significant differences in the frequencies of the gene arrangements of A₁, J and U chromosome were observed during the period of investigation. A tendency towards a decrease in the frequency of the standard gene arrangements was found for all chromosomes, but was particularly evident with chromosomes A and J. The frequency of the gene arrangements A₁ A₂, J₁ and U_1–2+6 increased at the same time. Differences in the frequency of the gene arrangements of A, J and U chromosomes were also observed when the populations from two ecologically different habitats (beech and oak forest) were compared in 1990.     

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.     

The role of the transposable element hobo in the origin of endemic inversions in wild populations of Drosophila melanogaster

Evidence from in situ hybridizations of DNA from the transposable element hobo to polytene salivary gland chromosome squashes reveals that hobo occupies both cytological breakpoints of three of four endemic inversions sampled from natural populations of Drosophila melanogaster in the Hawaiian islands. The fourth endemic inversion has a single hobo insert at one breakpoint. Cosmopolitan inversions on the same chromosomes do not show this association. Frequencies of both endemic and cosmopolitan inversions in Hawaiian populations fall in ranges typical for natural populations of D. melanogaster sampled worldwide, suggesting that these results may be typical of other regions besides Hawaii. This appears to be the first direct demonstration that transposable elements are responsible for causing specific rearrangements found in nature; consequently, it is also the first direct demonstration that chromosome rearrangements can arise in nature in a manner predicted by results of hybrid dysgenic crosses in the laboratory. Possible population genetic and evolutionary consequences are discussed.     

Inversion polymorphism in species of the Drosophila nasuta subgroup from Thailand

Thailand populations of three species of the D. nasuta complex have been analysed for the presence of paracentric inversions. D. albomicans and D. sulfurigaster albostrigata were collected from Phuket, Chiang Mai and the River Kwai, whilst D. kohkoa was found only in Phuket and the River Kwai. Chromosomal polymorphism was studied in respect to geographical distribution. The Phuket populations of all three species proved to be highly polymorphic by comparison with the River Kwai and Chiang Mai populations. The heterozygosity frequencies of inversions were calculated and the variations interpreted as a result of adaptation to local ecogeographical conditions. Shared polymorphisms revealed that D. kohkoa and D. s. albostrigata are more closely related to D. albomicans than they are to each other.Based on a thesis submitted for the degree of Ph.D. in the University of Queensland.     

Chromosomal inversion polymorphism leads to extensive genetic structure: a multilocus survey in Drosophila subobscura

The adaptive character of inversion polymorphism in Drosophila subobscura is well established. The O(ST) and O(3+4) chromosomal arrangements of this species differ by two overlapping inversions that arose independently on O(3) chromosomes. Nucleotide variation in eight gene regions distributed along inversion O(3) was analyzed in 14 O(ST) and 14 O(3+4) lines. Levels of variation within arrangements were quite similar along the inversion. In addition, we detected (i) extensive genetic differentiation between arrangements in all regions, regardless of their distance to the inversion breakpoints; (ii) strong association between nucleotide variants and chromosomal arrangements; and (iii) high levels of linkage disequilibrium in intralocus and also in interlocus comparisons, extending over distances as great as approximately 4 Mb. These results are not consistent with the higher genetic exchange between chromosomal arrangements expected in the central part of an inversion from double-crossover events. Hence, double crossovers were not produced or, alternatively, recombinant chromosomes were eliminated by natural selection to maintain coadapted gene complexes. If the strong genetic differentiation detected along O(3) extends to other inversions, nucleotide variation would be highly structured not only in D. subobscura, but also in the genome of other species with a rich chromosomal polymorphism.     

An experimental study of evolution in progress: Clines for quantitative traits in colonizing and Palearctic populations ofDrosophila

Summary Drosophila subobscura has recently colonized the American continent and is an excellent model for studying evolution in action. Previous analyses have shown that these colonizing populations have significant latitudinal clines for the frequencies of some chromosomal arrangements that parallel those clines found in the Old World. These results strongly suggest that this polymorphism is adaptive. In the present study, significant latitudinal clines for continuous morphometric variables (flies are larger in the north) have been detected in Old World populations ofD. subobscura. The adaptive nature of these clines is reinforced by the fact that parallel latitudinal clines for body size have also been detected inDrosophila obscura, a closely related sympatric species, as well as previously in otherDrosophila. On the other hand, no significant latitudinal clines for continuous morphometric traits, not even when using an overall size index, have been detected in colonizing populations ofD. subobscura. This is a rather surprising result given the number of generations that have elapsed since the species was detected in America and given that significant clines in chromosomal inversions are already established. Thus, the adaptive response of quantitative morphometric variables is not as rapid as that found for chromosomal inversions. Nevertheless, canonical correlation analysis suggests that significant latitudinal clines for body size might soon be detected in the American continent. The results obtained here are included in a projected time series with the aim of documenting size evolution in action.     

Evolution of Chilean colonizing populations of <Emphasis Type="Italic">Drosophila subobscura</Emphasis>: lethal genes and chromosomal arrangements

Knowledge of the frequency, distribution, and fate of lethal genes in chromosomal inversions helps to illuminate the evolution of recently founded populations. We analyze the relationship between lethal genes and inversions in two colonizing populations of D. subobscura in Chile. In the ancestral Palearctic populations of this species, lethal genes seem distributed at random on chromosomes. But in colonizing American populations, some lethal genes are associated with specific chromosomal arrangements. Some of these associated lethals were detected only during the first stages of the colonization (O ₃₊₄₊₂ ), and never thereafter, whereas others have persisted (O ₃₊₄₊₇ and O₅). However, most lethal genes in American populations have been observed only once: they have arisen by novel mutation and soon disappear. Finally, recombination between different inversions has been observed in America. However, the persistence of lethal genes associated with the heterotic inversions O ₃₊₄₊₇ and O₅ could indicate that recombination inside these inversions is rare. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.