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The role of natural selection in genetic differentiation of worldwide populations of Drosophila ananassae.

ABSTRACT: The main evolutionary forces leading to genetic differentiation between populations are generally considered to be natural selection, random genetic drift, and limited migration. However, little empirical evidence exists to help explain the extent, mechanism, and relative role of these forces. In this study, we make use of the differential migration behavior of genes located in regions of low and high recombination to infer the role and demographic distribution of natural selection in Drosophila ananassae. Sequence data were obtained from 13 populations, representing almost the entire range of cosmopolitan D. ananassae. The pattern of variation at a 5.1-kb fragment of the furrowed gene, located in a region of very low recombination, appears strikingly different from that of 10 noncoding DNA fragments (introns) in regions of normal to high recombination. Most interestingly, two main haplotypes are present at furrowed, one being fixed in northern populations and the other being fixed or in high frequency in more southern populations. A cline in the frequency of one of these haplotypes occurs in parallel latitudinal transects. Taken together, significant clinal variation and a test against alternative models of natural selection provide evidence of two independent selective sweeps restricted to specific regions of the species range.

SUBMITTER: Baines JF

PROVIDER: S-EPMC1448739 | biostudies-literature | 2004 Dec

REPOSITORIES: biostudies-literature

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The role of natural selection in genetic differentiation of worldwide populations of Drosophila ananassae.

Baines John F JF Das Aparup A Mousset Sylvain S Stephan Wolfgang W

Genetics 20041201 4

The main evolutionary forces leading to genetic differentiation between populations are generally considered to be natural selection, random genetic drift, and limited migration. However, little empirical evidence exists to help explain the extent, mechanism, and relative role of these forces. In this study, we make use of the differential migration behavior of genes located in regions of low and high recombination to infer the role and demographic distribution of natural selection in Drosophila ...[more]

PMID: 15611169

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Project description:Several allozyme-coding genes in Drosophila melanogaster show patterns suggesting that polymorphisms at these loci are targets of balancing selection. An important question is whether these genes have similar distributions of underlying DNA sequence variation which would indicate similar evolutionary processes occurring in this class of loci. One such locus, 6-phosphogluconate dehydrogenase (Pgd), has previously been shown to exhibit clinal variation for Fast/Slow electromorph variation in the United States and Australia, unusually large electromorph frequency differences between the United States and Africa, and other patterns indicative of selection. We measured four-cutter DNA restriction site and allozyme variation at Pgd among 142 D. melanogaster X chromosomes collected from several geographic regions including North Carolina, California, and Zimbabwe (Africa). We also sequenced a representative sample of 13 D. melanogaster Pgd genes collected in North Carolina and a single copy of Pgd from the sibling species, Drosophila simulans. While some population genetic models predict excess DNA polymorphism in genes which are targets of balancing selection, the D. melanogaster samples from the United States had significantly reduced levels of DNA polymorphism and extraordinarily high levels of linkage disequilibrium, providing evidence of hitchhiking effects of advantageous mutants at Pgd or at linked sites. Therefore, while selection has probably influenced the distribution of DNA variation at Pgd, the precise nature of these selective events remains obscure. Since the Pgd region appears to have low rates of crossing over, the reduced level of variation at this locus supports the idea that recombination rates are important determinants of levels of DNA polymorphism in natural populations. Furthermore, while patterns of allozyme variation are very similar at Pgd and Adh, the DNA data show that the evolutionary histories of these genes are dramatically different. We observed extensive differences in the amount and distribution of variation in D. melanogaster Pgd samples from the United States and Zimbabwe which cannot be explained by differential selection on the Fast/Slow polymorphism in these two geographic regions. Thus, genetic drift among partially isolated populations has also been an important factor in determining the distribution of variation at Pgd in D. melanogaster. Finally, we assayed four-cutter variation at Pgd in a sample of 19 D. simulans X chromosomes and observed reduced levels of DNA variability and high levels of linkage disequilibrium. These patterns are consistent with predictions of some hitchhiking models.

Project description:Background The Mediterranean fruit fly, Ceratitis capitata, is a cosmopolitan agricultural pest of worldwide economic importance and a model for the development of the Sterile Insect Technique (SIT) for fruit flies of the Tephritidae family (Diptera). SIT relies on the effective mating of laboratory-reared strains and natural populations, and therefore requires an efficient mass-rearing system that will allow for the production of high-quality males. Adaptation of wild flies to an artificial laboratory environment can be accompanied by negative effects on several life history traits through changes in their genetic diversity and symbiotic communities. Such changes may lead to reduced biological quality and mating competitiveness in respect to the wild populations. Profiling wild populations can help understand, and maybe reverse, deleterious effects accompanying laboratory domestication thus providing insects that can efficiently and effectively support SIT application. Results In the present study, we analyzed both the genetic structure and gut symbiotic communities of natural medfly populations of worldwide distribution, including Europe, Africa, Australia, and the Americas. The genetic structure of 408 individuals from 15 distinct populations was analyzed with a set of commonly used microsatellite markers. The symbiotic communities of a subset of 265 individuals from 11 populations were analyzed using the 16S rRNA gene-based amplicon sequencing of single individuals (adults). Genetic differentiation was detected among geographically distant populations while adults originated from neighboring areas were genetically closer. Alpha and beta diversity of bacterial communities pointed to an overall reduced symbiotic diversity and the influence of the geographic location on the bacterial profile. Conclusions Our analysis revealed differences both in the genetic profile and the structure of gut symbiotic communities of medfly natural populations. The genetic analysis expanded our knowledge to populations not analyzed before and our results were in accordance with the existing scenarios regarding this species expansion and colonization pathways. At the same time, the bacterial communities from different natural medfly populations have been characterized, thus broadening our knowledge on the microbiota of the species across its range. Genetic and symbiotic differences between natural and laboratory populations must be considered when designing AW-IPM approaches with a SIT component, since they may impact mating compatibility and mating competitiveness of the laboratory-reared males. In parallel, enrichment from wild populations and/or symbiotic supplementation could increase rearing productivity, biological quality, and mating competitiveness of SIT-important laboratory strains. Supplementary Information The online version contains supplementary material available at 10.1186/s12863-020-00946-z.

Dataset Information

The role of natural selection in genetic differentiation of worldwide populations of Drosophila ananassae.

Publications

The role of natural selection in genetic differentiation of worldwide populations of Drosophila ananassae.

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