Molecular Population Genetics of Inversion Breakpoint Regions inDrosophila pseudoobscura

Andre G Wallace,Don Detweiler,Stephen W Schaeffer

doi:10.1534/g3.113.006122

Andre G Wallace, Don Detweiler + Show 1 more

Open Access

https://doi.org/10.1534/g3.113.006122

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Abstract

Paracentric inversions in populations can have a profound effect on the pattern and organization of nucleotide variability along a chromosome. Regions near inversion breakpoints are expected to have greater levels of differentiation because of reduced genetic exchange between different gene arrangements whereas central regions in the inverted segments are predicted to have lower levels of nucleotide differentiation due to greater levels of genetic flux among different karyotypes. We used the inversion polymorphism on the third chromosome of Drosophila pseudoobscura to test these predictions with an analysis of nucleotide diversity of 18 genetic markers near and away from inversion breakpoints. We tested hypotheses about how the presence of different chromosomal arrangements affects the pattern and organization of nucleotide variation. Overall, markers in the distal segment of the chromosome had greater levels of nucleotide heterozygosity than markers within the proximal segment of the chromosome. In addition, our results rejected the hypothesis that the breakpoints of derived inversions will have lower levels of nucleotide variability than breakpoints of ancestral inversions, even when strains with gene conversion events were removed. High levels of linkage disequilibrium were observed within all 11 breakpoint regions as well as between the ends of most proximal and distal breakpoints. The central region of the chromosome had the greatest levels of linkage disequilibrium compared with the proximal and distal regions because this is the region that experiences the highest level of recombination suppression. These data do not fully support the idea that genetic exchange is the sole force that influences genetic variation on inverted chromosomes.

Highlights

Paracentric inversions in populations can have a profound effect on the pattern and organization of nucleotide variability along a chromosome
To better test how genetic exchange on inverted chromosomes affects the pattern and organization of nucleotide diversity, we developed ten new genetic markers for the third chromosome that map near the proximal and distal inversion breakpoints of gene arrangements with high frequency and wide geographical distributions
Tests of the impact of heterogeneous recombination rates on nucleotide polymorphism and divergence on inverted chromosomes in D. pseudoobscura The history of the gene arrangements of the third chromosome of D. pseudoobscura reflect a complex history that is written in the observed pattern of nucleotide variation

Summary

MATERIALS AND METHODS

Fly strains and DNA extraction Strains of D. pseudoobscura were collected in 1998 from four different populations in the southwestern United States by S. We used eight gene regions that were previously sequenced by Schaeffer et al (2003)), engrailed (en), exuperantia 1 (exu 1), Myocyte enhancing factor 2 (Mef 2), even skipped (eve), amylase 1 (Amy 1), vestigial (vg), F6, and Ecdysone Receptor (EcR), and we used the primers and PCR conditions described in the study. These eight loci are evenly distributed across the D. pseudoobscura third chromosome. We designed PCR primers to amplify additional gene regions to be near the breakpoints of six polymorphic inversions using the third chromosome nucleotide sequence and cytogenetic map (Dobzhansky and Sturtevant 1938; Schaeffer et al 2008). The number of strains sequenced for any of the 18 genetic markers varied from 86 to 144

Nucleotide sequence alignment

Type of variation

RESULTS AND DISCUSSION

TL S Obs