Abstract
Drosophila pseudoobscura harbors a rich gene arrangement polymorphism on the third chromosome generated by a series of overlapping paracentric inversions. The arrangements suppress recombination in heterokaryotypic individuals, which allows for the selective maintenance of coadapted gene complexes. Previous mapping experiments used to determine the degree to which recombination is suppressed in gene arrangement heterozygotes produced non-recombinant progeny in non-Mendelian ratios. The deviations from Mendelian expectations could be the result of viability differences between wild and mutant chromosomes, meiotic drive because of achiasmate pairing of homologues in heterokaryotypic females during meiosis, or a combination of both mechanisms. The possibility that the frequencies of the chromosomal arrangements in natural populations are affected by mechanisms other than adaptive selection led us to consider these hypotheses. We performed reciprocal crosses involving both heterozygous males and females to determine if the frequency of the non-recombinant progeny deviates significantly from Mendelian expectations and if the frequencies deviate between reciprocal crosses. We failed to observe non-Mendelian ratios in multiple crosses, and the frequency of the non-recombinant classes differed in only one of five pairs of reciprocal crosses despite sufficient power to detect these differences in all crosses. Our results indicate that deviations from Mendelian expectations in recombination experiments involving the D. pseudoobscura inversion system are most likely due to fitness differences of gene arrangement karyotypes in different environments.
Highlights
Drosophila pseudoobscura harbors a rich gene arrangement polymorphism on the third chromosome generated by a series of overlapping inversions [1] (Figure 1); over thirty different arrangements segregate in natural populations
We mated single females heterozygous for a mutant marked chromosome on an AR background and a wild-type chromosome carrying either the AR, ST, Pikes Peak (PP), Santa Cruz (SC), or Tree Line (TL) arrangement to single males homozygous for chromosomes carrying some of the same mutant markers (Figure 2)
If meiotic drive were responsible for non-Mendelian ratios, the reciprocal crosses should differ in the frequency of individuals in each of the two non-recombinant classes
Summary
Drosophila pseudoobscura harbors a rich gene arrangement polymorphism on the third chromosome generated by a series of overlapping inversions [1] (Figure 1); over thirty different arrangements segregate in natural populations. Population cage experiments indicate that there are fitness differences between arrangement genotypes [7,8]. These laboratory crosses suggest that heterokaryotypic individuals within a population have a fitness advantage, but this advantage is lost when arrangements from different populations are combined. The coadaptation model was developed to explain the apparent fitness differences of karyotypes in natural populations and laboratory crosses.
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