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John H Willis - One of the best experts on this subject based on the ideXlab platform.
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Dissecting the role of a large Chromosomal Inversion in life history divergence throughout the Mimulus guttatus species complex
Molecular Ecology, 2018Co-Authors: Jennifer M. Coughlan, John H WillisAbstract:: Chromosomal Inversions can play an important role in adaptation, but the mechanism of their action in many natural populations remains unclear. An Inversion could suppress recombination between locally beneficial alleles, thereby preventing maladaptive reshuffling with less-fit, migrant alleles. The recombination suppression hypothesis has gained much theoretical support but empirical tests are lacking. Here, we evaluated the evolutionary history and phenotypic effects of a Chromosomal Inversion which differentiates annual and perennial forms of Mimulus guttatus. We found that perennials likely possess the derived orientation of the Inversion. In addition, this perennial orientation occurs in a second perennial species, M. decorus, where it is strongly associated with life history differences between co-occurring M. decorus and annual M. guttatus. One prediction of the recombination suppression hypothesis is that loci contributing to local adaptation will predate the Inversion. To test whether the loci influencing perenniality pre-date this Inversion, we mapped QTLs for life history traits that differ between annual M. guttatus and a more distantly related, collinear perennial species, M. tilingii. Consistent with the recombination suppression hypothesis, we found that this region is associated with life history in the absence of the Inversion, and this association can be broken into at least two QTLs. However, the absolute phenotypic effect of the LG8 Inversion region on life history is weaker in M. tilingii than in perennials which possess the Inversion. Thus, while we find support for the recombination suppression hypothesis, the contribution of this Inversion to life history divergence in this group is likely complex.
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divergent population structure and climate associations of a Chromosomal Inversion polymorphism across the mimulus guttatus species complex
Molecular Ecology, 2014Co-Authors: Elen Oneal, David B. Lowry, Kevin M Wright, Zhirui Zhu, John H WillisAbstract:Chromosomal rearrangement polymorphisms are common and increasingly found to be associated with adaptive ecological divergence and speciation. Rearrangements, such as Inversions, reduce recombination in heterozygous individuals and thus can protect favourable allelic combinations at linked loci, facilitating their spread in the presence of gene flow. Recently, we identified a Chromosomal Inversion polymorphism that contributes to ecological adaptation and reproductive isolation between annual and perennial ecotypes of the yellow monkeyflower, Mimulus guttatus. Here we evaluate the population genetic structure of this inverted region in comparison with the collinear regions of the genome across the M. guttatus species complex. We tested whether annual and perennial M. guttatus exhibit different patterns of divergence for loci in the inverted and noninverted regions of the genome. We then evaluated whether there are contrasting climate associations with these genomic regions through redundancy analysis. We found that the Inversion exhibits broadly different patterns of divergence among annual and perennial M. guttatus and is associated with environmental variation across population accessions. This study is the first widespread population genetic survey of the diversity of the M. guttatus species complex. Our findings contribute to a greater understanding of morphological, ecological, and genetic evolutionary divergence across this highly diverse group of closely related ecotypes and species. Finally, understanding species relationships among M. guttatus sp. has hitherto been stymied by accumulated evidence of substantial gene flow among populations as well as designated species. Nevertheless, our results shed light on these relationships and provide insight into adaptation in life history traits within the complex.
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A widespread Chromosomal Inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation.
PLoS biology, 2010Co-Authors: David B. Lowry, John H WillisAbstract:The role of Chromosomal Inversions in adaptation and speciation is controversial. Historically, Inversions were thought to contribute to these processes either by directly causing hybrid sterility or by facilitating the maintenance of co-adapted gene complexes. Because Inversions suppress recombination when heterozygous, a recently proposed local adaptation mechanism predicts that they will spread if they capture alleles at multiple loci involved in divergent adaptation to contrasting environments. Many empirical studies have found Inversion polymorphisms linked to putatively adaptive phenotypes or distributed along environmental clines. However, direct involvement of an Inversion in local adaptation and consequent ecological reproductive isolation has not to our knowledge been demonstrated in nature. In this study, we discovered that a Chromosomal Inversion polymorphism is geographically widespread, and we test the extent to which it contributes to adaptation and reproductive isolation under natural field conditions. Replicated crosses between the prezygotically reproductively isolated annual and perennial ecotypes of the yellow monkeyflower, Mimulus guttatus, revealed that alternative Chromosomal Inversion arrangements are associated with life-history divergence over thousands of kilometers across North America. The Inversion polymorphism affected adaptive flowering time divergence and other morphological traits in all replicated crosses between four pairs of annual and perennial populations. To determine if the Inversion contributes to adaptation and reproductive isolation in natural populations, we conducted a novel reciprocal transplant experiment involving outbred lines, where alternative arrangements of the Inversion were reciprocally introgressed into the genetic backgrounds of each ecotype. Our results demonstrate for the first time in nature the contribution of an Inversion to adaptation, an annual/perennial life-history shift, and multiple reproductive isolating barriers. These results are consistent with the local adaptation mechanism being responsible for the distribution of the two Inversion arrangements across the geographic range of M. guttatus and that locally adaptive Inversion effects contribute directly to reproductive isolation. Such a mechanism may be partially responsible for the observation that closely related species often differ by multiple Chromosomal rearrangements.
Mauro Santos - One of the best experts on this subject based on the ideXlab platform.
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vanishing Chromosomal Inversion clines in drosophila subobscura from chile is behavioral thermoregulation to blame
The American Naturalist, 2013Co-Authors: Luis E Castaneda, Joan Balanya, Enrico L Rezende, Mauro SantosAbstract:AbstractChromosomal Inversion clines paralleling the long-standing ones in native Palearctic populations of Drosophila subobscura evolved swiftly after this species invaded the Americas in the late 1970s and early 1980s. However, the new clines did not consistently continue to converge on the Old World baseline. Our recent survey of Chilean populations of D. subobscura shows that Inversion clines have faded or even changed sign with latitude. Here, we investigate the hypothesis that this fading of Inversion clines might be due to the Bogert effect, namely, that flies’ thermoregulatory behavior has eventually compensated for environmental variation in temperature, thus buffering selection on thermal-related traits. We show that latitudinal divergence in thermal preference (Tp) has evolved in Chile for females, with higher-latitude flies having a lower mean Tp. Plastic responses in Tp also lessen latitudinal thermal variation because flies developed at colder temperatures prefer warmer microclimates. Our re...
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Climate change and Chromosomal Inversions in Drosophila subobscura
Climate Research, 2010Co-Authors: Enrico L Rezende, Joan Balanya, Luis Serra, Francisco Rodríguez-trelles, Carla Rego, Inês Fragata, Margarida Gaspar De Matos, Mauro SantosAbstract:In natural populations, the large changes in Chromosomal structure occurring through Chromosomal Inversions show pronounced variations in frequency that often correspond to temporal and spatial climatic trends, which suggests that they may be employed to monitor the impact of global warming. Here we review and update the evidence on the association between Chromosomal Inversions and climate in D. subobscura, which provides one of the best studied models in this con- text. Chromosomal Inversion frequencies of D. subobscura populations vary predictably with lati- tude, and this association has evolved independently in Europe and South and North America. They also exhibit clear seasonal trends that are consistent with temperature fluctuations. More importantly, latitudinal clines in Chromosomal Inversion frequencies seem to be responding to the global rise in mean temperatures in all continents. We analyze the relevance of these results in the light of climate change, and discuss how a better understanding of the mechanisms underlying these patterns may contribute to our knowledge on the impacts of global warming in biological systems.
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Contrasting patterns of phenotypic variation linked to Chromosomal Inversions in native and colonizing populations of Drosophila subobscura
Journal of Evolutionary Biology, 2009Co-Authors: Inês Fragata, Joan Balanya, Enrico L Rezende, Carla Rego, Margarida Gaspar De Matos, Mauro SantosAbstract:In fewer than two decades after invading the Americas, the fly Drosophila subobscura evolved latitudinal clines for Chromosomal Inversion frequencies and wing size that are parallel to the long-standing ones in native Palearctic populations. By sharp contrast, wing shape clines also evolved in the New World, but the relationship with latitude was opposite to that in the Old World. Previous work has suggested that wing trait differences among individuals are partially due to the association between Chromosomal Inversions and particular alleles which influence the trait under consideration. Furthermore, it is well documented that a few number of effective individuals founded the New World populations, which might have modified the biometrical effect of Inversions on quantitative traits. Here we evaluate the relative contribution of Chromosomal Inversion clines in shaping the parallel clines in wing size and contrasting clines in wing shape in native and colonizing populations of the species. Our results reveal that Inversion-size and Inversion-shape associations in native and colonizing (South America) populations are generally different, probably due to the bottleneck effect. Contingent, unpredictable evolution was suggested as an explanation for the different details involved in the otherwise parallel wing size clines between Old and New World populations of D. subobscura. We challenge this assertion and conclude that contrasting wing shape clines came out as a correlated response of Inversion clines that might have been predicted considering the genetic background of colonizers.
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recombination load in a Chromosomal Inversion polymorphism of drosophila subobscura
Genetics, 2009Co-Authors: Mauro SantosAbstract:Chromosomal Inversions suppress recombination in heterokaryotypes and may help to maintain positive epistatic interactions among groups of alleles at loci contained in the Inversion. Here I evaluate the protective effect of Inversions on recombination when different Chromosomal segments, or even the whole chromosome O of Drosophila subobscura, can be effectively prevented from undergoing recombination in several naturally occurring heterokaryotypes. The fitness of flies made homozygous for recombinant chromosomes was generally lower when compared to their nonrecombinant counterparts, thus suggesting that segregating gene arrangements in this species hold together favorable combinations of alleles that interact epistatically.
Nora J. Besansky - One of the best experts on this subject based on the ideXlab platform.
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2la Chromosomal Inversion enhances thermal tolerance of anopheles gambiae larvae
Malaria Journal, 2009Co-Authors: Kyle A C Rocca, Carlo Costantini, Emilie M Gray, Nora J. BesanskyAbstract:The mosquito Anopheles gambiae is broadly distributed throughout sub-Saharan Africa and this contributes to making it the most efficient vector of malaria on the continent. The pervasiveness of this species is hypothesized to originate in local adaptations facilitated by Inversion polymorphisms. One Inversion, named 2La, is strongly associated with aridity clines in West and Central Africa: while 2La is fixed in arid savannas, the 2L+a arrangement is predominantly found in the rainforest. Ability to survive high temperature exposure is an essential component of aridity tolerance, particularly in immature stages that are restricted to shallow puddles. Toward deciphering the role of the 2La Inversion in local adaptation, the present investigation focused on variation in larval and pupal thermo-tolerance in two populations dissimilar solely in 2La arrangement. A laboratory colony of A. gambiae that is polymorphic for 2La but standard for all other known Inversions was used to create 2 homokaryotypic populations (2L+a and 2La). The survival of 4th instar larvae and pupae from both populations was then tested following exposure to thermal stress with and without prior heat hardening. Larvae responded identically to a 40°C heat stress, with about 50% of larvae dying after 1.5–2 h and few larvae surviving a 3 h stress. When heat hardened prior to the thermal stress, thermo-tolerance of both larval populations increased, with 2La 24 h survival significantly exceeding that of 2L+a. Pupae were generally more thermo-tolerant than larvae, although 2La pupae were less so than 2L+a. Heat hardening had no positive effect on pupal thermo-tolerance. The increased thermo-tolerance observed in 2La larvae following heat hardening suggests higher responsiveness (i.e., thermal sensitivity) of the inverted karyotype. By responding more drastically to the heat shock, 2La larvae are better equipped to resist the potentially lethal temperatures that occur in arid habitats. The lower survival of 2La pupae compared with 2L+a may reflect the cost of this sensitivity, whereby the thermal resistance mechanisms prevent successful completion of metamorphosis. The costs and benefits of thermal resistance are discussed in light of the climates characterizing either end of the 2La frequency cline.
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Breakpoint structure reveals the unique origin of an interspecific Chromosomal Inversion (2La) in the Anopheles gambiae complex.
Proceedings of the National Academy of Sciences of the United States of America, 2006Co-Authors: Igor V. Sharakhov, Bradley J. White, Maria V. Sharakhova, Jonathan K. Kayondo, Neil F. Lobo, Federica Santolamazza, Alessandra Della Torre, Frédéric Simard, Frank H. Collins, Nora J. BesanskyAbstract:Paracentric Chromosomal Inversions are major architects of organismal evolution and have been associated with adaptations relevant to malaria transmission in anopheline mosquitoes. The processes responsible for their origin and maintenance, still poorly understood, can be illuminated by analysis of Inversion breakpoint sequences. Here, we report the breakpoint structure of Chromosomal Inversion 2La from the principal malaria vector Anopheles gambiae and its relatives in the A. gambiae complex. The distal and proximal breakpoints of the standard (2L+a) arrangement contain gene duplications: full-length genes and their truncated copies at opposite ends. Intact genes without pseudogene copies in the alternative arrangement (2La) imply that 2L+a is derived and was viable despite damage to genes, because duplication preserved gene function. A unique origin for the interspecific 2La Inversion was challenged previously by indirect genetic evidence, but breakpoint sequences determined from members of the A. gambiae complex strongly suggest their descent from a single event. The derived position of 2L+a, long considered ancestral in this medically important group, has significant implications for the phylogenetic history and the evolution of vectorial capacity in the A. gambiae complex.
Carlo Costantini - One of the best experts on this subject based on the ideXlab platform.
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breakpoint structure of the anopheles gambiae 2rb Chromosomal Inversion
Malaria Journal, 2010Co-Authors: Neil F. Lobo, Maria V. Sharakhova, Djibril Sangare, Allison A Regier, Kyanne R Reidenbach, David Bretz, Scott J Emrich, Sekou F Traore, Carlo CostantiniAbstract:Alternative arrangements of chromosome 2 Inversions in Anopheles gambiae are important sources of population structure, and are associated with adaptation to environmental heterogeneity. The forces responsible for their origin and maintenance are incompletely understood. Molecular characterization of Inversion breakpoints provides insight into how they arose, and provides the basis for development of molecular karyotyping methods useful in future studies. Sequence comparison of regions near the cytological breakpoints of 2Rb allowed the molecular delineation of breakpoint boundaries. Comparisons were made between the standard 2R+ b arrangement in the An. gambiae PEST reference genome and the inverted 2Rb arrangements in the An. gambiae M and S genome assemblies. Sequence differences between alternative 2Rb arrangements were exploited in the design of a PCR diagnostic assay, which was evaluated against the known Chromosomal banding pattern of laboratory colonies and field-collected samples from Mali and Cameroon. The breakpoints of the 7.55 Mb 2Rb Inversion are flanked by extensive runs of the same short (72 bp) tandemly organized sequence, which was likely responsible for Chromosomal breakage and rearrangement. Application of the molecular diagnostic assay suggested that 2Rb has a single common origin in An. gambiae and its sibling species, Anopheles arabiensis, and also that the standard arrangement (2R+ b ) may have arisen twice through breakpoint reuse. The molecular diagnostic was reliable when applied to laboratory colonies, but its accuracy was lower in natural populations. The complex repetitive sequence flanking the 2Rb breakpoint region may be prone to structural and sequence-level instability. The 2Rb molecular diagnostic has immediate application in studies based on laboratory colonies, but its usefulness in natural populations awaits development of complementary molecular tools.
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2la Chromosomal Inversion enhances thermal tolerance of anopheles gambiae larvae
Malaria Journal, 2009Co-Authors: Kyle A C Rocca, Carlo Costantini, Emilie M Gray, Nora J. BesanskyAbstract:The mosquito Anopheles gambiae is broadly distributed throughout sub-Saharan Africa and this contributes to making it the most efficient vector of malaria on the continent. The pervasiveness of this species is hypothesized to originate in local adaptations facilitated by Inversion polymorphisms. One Inversion, named 2La, is strongly associated with aridity clines in West and Central Africa: while 2La is fixed in arid savannas, the 2L+a arrangement is predominantly found in the rainforest. Ability to survive high temperature exposure is an essential component of aridity tolerance, particularly in immature stages that are restricted to shallow puddles. Toward deciphering the role of the 2La Inversion in local adaptation, the present investigation focused on variation in larval and pupal thermo-tolerance in two populations dissimilar solely in 2La arrangement. A laboratory colony of A. gambiae that is polymorphic for 2La but standard for all other known Inversions was used to create 2 homokaryotypic populations (2L+a and 2La). The survival of 4th instar larvae and pupae from both populations was then tested following exposure to thermal stress with and without prior heat hardening. Larvae responded identically to a 40°C heat stress, with about 50% of larvae dying after 1.5–2 h and few larvae surviving a 3 h stress. When heat hardened prior to the thermal stress, thermo-tolerance of both larval populations increased, with 2La 24 h survival significantly exceeding that of 2L+a. Pupae were generally more thermo-tolerant than larvae, although 2La pupae were less so than 2L+a. Heat hardening had no positive effect on pupal thermo-tolerance. The increased thermo-tolerance observed in 2La larvae following heat hardening suggests higher responsiveness (i.e., thermal sensitivity) of the inverted karyotype. By responding more drastically to the heat shock, 2La larvae are better equipped to resist the potentially lethal temperatures that occur in arid habitats. The lower survival of 2La pupae compared with 2L+a may reflect the cost of this sensitivity, whereby the thermal resistance mechanisms prevent successful completion of metamorphosis. The costs and benefits of thermal resistance are discussed in light of the climates characterizing either end of the 2La frequency cline.
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Chromosomal Inversion polymorphism of Anopheles funestus from forest villages of South Cameroon.
Parassitologia, 2000Co-Authors: Daniela Boccolini, Christophe Antonio-nkondjio, Carlo Costantini, Didier FontenilleAbstract:: 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.
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spatial and temporal variations of the Chromosomal Inversion polymorphism of anopheles funestus in senegal
Parasite, 2000Co-Authors: Daniela Boccolini, Carlo Costantini, I. Dia, L. Lochouarn, Didier FontenilleAbstract:Le polymorphisme des Inversions paracentriques des chromosomes polytenes d'An. funestus a ete etudie le long d'un transect au Senegal dans le but d'estimer leurs variations spatio-temporelles. Un polymorphisme croissant a ete observe de l'ouest vers le sud-est. A l'echelle geographique, les variations des frequences des Inversions ont ete significatives quel que soit le bras chromosomique considere. Cependant ces variations n'ont ete liees ni a la saison ni a l'annee a l'exception de l'Inversion 3b dans le village de Dielmo. De telles variations des frequences des Inversions chromosomiques a l'interieur d'une aire limitee, associees a une stabilite temporelle, suggerent un flux genetique restreint entre les differentes populations etudiees du probablement aux discontinuites observees dans la distribution et la bioecologie d'An. funestus.
Carmen Segarra - One of the best experts on this subject based on the ideXlab platform.
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Inferring the demographic history of Drosophila subobscura from nucleotide variation at regions not affected by Chromosomal Inversions
Molecular Ecology, 2015Co-Authors: Roser Pratdesaba, Carmen Segarra, Montserrat AguadéAbstract:: Drosophila subobscura presents a rich and complex Chromosomal Inversion polymorphism. It can thus be considered a model system (i) to study the mechanisms originating Inversions and how Inversions affect the levels and patterns of variation in the inverted regions and (ii) to study adaptation at both the single-gene and Chromosomal Inversion levels. It is therefore important to infer its demographic history as previous information indicated that its nucleotide variation is not at mutation-drift equilibrium. For that purpose, we sequenced 16 noncoding regions distributed across those parts of the J chromosome not affected by Inversions in the studied population and possibly either by other selective events. The pattern of variation detected in these 16 regions is similar to that previously reported within different Chromosomal arrangements, suggesting that the latter results would, thus, mainly reflect recent demographic events rather than the partial selective sweep imposed by the origin and frequency increase of Inversions. Among the simple demographic models considered in our Approximate Bayesian Computation analysis of variation at the 16 regions, the model best supported by the data implies a population size expansion soon after the penultimate glacial period. This model constitutes a better null model, and it is therefore an important resource for subsequent studies aiming among others to uncover selective events across the species genome. Our results also highlight the importance of introducing the possibility of multiple hits in the coalescent simulations with an outgroup.
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genetic exchange versus genetic differentiation in a medium sized Inversion of drosophila the a2 ast arrangements of drosophila subobscura
Molecular Biology and Evolution, 2008Co-Authors: Clevio Nobrega, Montserrat Aguadé, Mahnaz Khadem, Carmen SegarraAbstract:Chromosomal Inversion polymorphism affects nucleotide variation at loci associated with Inversions. In Drosophila subobscura, a species with a rich Chromosomal Inversion polymorphism and the largest recombinational map so far reported in the Drosophila genus, extensive genetic structure of nucleotide variation was detected in the segment affected by the O(3) Inversion, a moderately sized Inversion at Muller's element E. Indeed, a strong genetic differentiation all over O(3) and no evidence of a higher genetic exchange in the center of the Inversion than at breakpoints were detected. In order to ascertain, whether other polymorphic and differently sized Inversions of D. subobscura also exhibited a strong genetic structure, nucleotide variation in 5 gene regions (P236, P275, P150, Sxl, and P125) located along the A(2) Inversion was analyzed in A(st) and A(2) chromosomes of D. subobscura. A(2) is a medium-sized Inversion at Muller's element A and forms a single Inversion loop in heterokaryotypes. The lower level of variation in A(2) relative to A(st) and the significant excess of low-frequency variants at polymorphic sites indicate that nucleotide variation at A(2) is not at mutation-drift equilibrium. The closest region to an Inversion breakpoint, P236, exhibits the highest level of genetic differentiation (F(ST)) and of linkage disequilibrium (LD) between arrangements and variants at nucleotide polymorphic sites. The remaining 4 regions show a higher level of genetic exchange between A(2) and A(st) chromosomes than P236, as revealed by F(ST) and LD estimates. However, significant genetic differentiation between the A(st) and A(2) arrangements was detected not only at P236 but also in the other 4 regions separated from the nearest breakpoint by 1.2-2.9 Mb. Therefore, the extent of genetic exchange between arrangements has not been high enough to homogenize nucleotide variation in the center of the A(2) Inversion. A(2) can be considered a typical successful Inversion of D. subobscura according to its relative length. Chromosomal Inversion polymorphism of D. subobscura might thus cause the genome of this species to be highly structured and to harbor different gene pools that might contribute to maintain adaptations to particular environments.
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Chromosomal Inversion Polymorphism Leads to Extensive Genetic Structure: A Multilocus Survey in Drosophila subobscura
Genetics, 2005Co-Authors: Agustí Munté, Montserrat Aguadé, Julio Rozas, Carmen SegarraAbstract:The adaptive character of Inversion polymorphism in Drosophila subobscura is well established. The OST and O3+4 Chromosomal arrangements of this species differ by two overlapping Inversions that arose independently on O3 chromosomes. Nucleotide variation in eight gene regions distributed along Inversion O3 was analyzed in 14 OST and 14 O3+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 ∼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 O3 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.