Genetic Exchange versus Genetic Differentiation in a Medium-Sized Inversion of Drosophila: The A2/Ast Arrangements of Drosophila subobscura

Abstract

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.

Molecular population genetics of the OBP83 genomic region in Drosophila subobscura and D. guanche: contrasting the effects of natural selection and gene arrangement expansion in the patterns of nucleotide variation

“…Actually, a number of studies (for example Aguadé, 1988;Aguadé, 1990, 1994;Aquadro et al, 1991;Benassi et al, 1993;Popadic et al, 1995;Babcock and Anderson, 1996;Hasson and Eanes, 1996;Rozas et al, 1999;Schaeffer et al, 2003;Nobrega et al, 2008;Kulathinal et al, 2009 and others) have shown extensive genetic differentiation between gene arrangements, a pattern that is consistent with the reduction of recombination levels expected in inversion heterozygotes (Roberts, 1976). Still, there is evidence of genetic exchange (either by gene conversion or double crossover) between gene arrangements Aguadé 1990, 1994;Rozas et al, 1999;Schaeffer and Anderson, 2005).…”

Effects of Inversions on Within- and Between-Species Recombination and Divergence

“…In comparison, the double-crossover rate across similar regions in homokaryotypes is approximately 5–10% (Gruneberg 1935; Spurway and Philip 1952; Novitski and Braver 1954; Robbins 1974; Pegueroles et al 2010), showing that double-recombination products are not produced as frequently as expected in inversion heterozygotes. Sequencing approaches have enhanced our understanding of differentiation within inverted regions by being able to detect double-crossover events or historical gene flux due to conversion within an inverted region (Rozas and Aguade 1994; Wesley and Eanes 1994; Hasson and Eanes 1996; Betran et al 1997; Laayouni et al 2003; Schaeffer and Anderson 2005; Nobrega et al 2008; White et al 2009). These studies confirm predictions by theoretical models for flux rates to be highest near the center of inverted regions (Navarro et al 1997; Kirkpatrick and Barton 2006; Feder and Nosil 2009).…”

Megabase-Scale Inversion Polymorphism in the Wild Ancestor of Maize

“…Inversion-induced LD has been reported in a variety of organisms, including humans (Bansal et al 2007), Drosophila subobscura (Munte et al 2005), and several other species (reviewed in Hoffmann and Rieseberg 2008). Strong differentiation between chromosomal arrangements (as measured by F ST ) has also been used as evidence of inversions in Drosophila (Andolfatto et al 1999;Depaulis et al 1999;Nóbrega et al 2008).A variety of circumstances can favor the maintenance or spread of an inversion polymorphism. The inversion may be 2010), an inversion is involved in local adaptation to Mediterranean habitats through several morphological and phenological traits, while the standard arrangement appears in a perennial ecotype from habitats with high year-round soil moisture.…”

“…Inversion-induced LD has been reported in a variety of organisms, including humans (Bansal et al 2007), Drosophila subobscura (Munte et al 2005), and several other species (reviewed in Hoffmann and Rieseberg 2008). Strong differentiation between chromosomal arrangements (as measured by F ST ) has also been used as evidence of inversions in Drosophila (Andolfatto et al 1999;Depaulis et al 1999;Nóbrega et al 2008).…”