Absence of linkage disequilibria between chromosomal arrangements and mtDNA haplotypes in natural populations ofDrosophila subobscurafrom the Balkan Peninsula

Abstract

The genetic structure of Drosophila subobscura from the Balkan Peninsula was studied with respect to restriction site polymorphism of mitochondrial DNA in populations from the Derventa River Gorge and Sicevo Gorge (Serbia). To investigate the role of cytonuclear interactions in shaping mitochondrial DNA variability in natural populations of this species, the study was complemented with the analysis of linkage disequilibria between mitochondrial haplotypes and chromosomal inversion arrangements. Similar to other populations of D. subobscura, two main haplotypes (I and II) were found, as well as a series of less common ones. The frequencies of haplotypes I and II accounted for 25.8% and 71.0%, respectively, in the population from the Derventa River Gorge, and for 32.4% and 58.1%, respectively, in the population from Sicevo Gorge. One of the haplotypes harbored a large insertion (2.7 kb) in the A+T rich region. The frequency distribution of both haplotypes did not depart from neutrality. Contrary to prior studies, we did not detect any significant linkage disequilibrium between the two most frequent mtDNA haplotypes and any of the chromosomal arrangements in either of the populations. We conclude that linkage disequilibrium is not a general occurrence in natural populations of D. subobscura, and we discuss how transient coadaptations, ecologically specific selective pressures, and demographics could contribute to population-specific patterns of linkage disequilibrium.

Negative frequency dependent selection on sympatric mtDNA haplotypes in Drosophila subobscura

“…In this species, variation is ubiquitous and strikingly geographically homogenous, with two dominant mtDNA haplotypes (termed I and II) typically co- occurring within populations at stable frequencies of approximately 50:50, across both the new and the old world [9, 22–28]. Moreover, experimental studies have shown that the two mtDNA haplotypes are not functionally equivalent: flies that harbor these haplotypes differ in major life history traits such as metabolic rate [29], fertility [30], viability, longevity and desiccation resistance [8, 31] and two earlier studies of laboratory cage populations were able to reject genetic drift as the sole mediator of mtDNA haplotype changes [9, 32].…”

“…We here note that linkage disequilibrium between mtDNA haplotypes and the nuclear genome, e.g. chromosomal inversions, is very low at most in D. subobscura [33, 38, 39], which is expected given the fact the two genomes do not cosegregate in males [17, 18]. …”

Inbreeding and thermal adaptation inDrosophila subobscura

“…In G 0 , the inversions (or chromosomal arrangements) and karyotypes found are characteristic of the Avala mountain population (Zivanovic and Mestres 2010a) and also of the Balkan region (Zivanovic et al 1995(Zivanovic et al , 2002Zivanovic 2007;Rasic et al 2008;Stamenkovic-Radak et al 2008;Kenig et al 2010;Zivanovic and Mestres 2011;Jelić et al 2012). No significant changes between G 0 and G 12 were observed for the inversion and arrangement frequencies.…”

Local adaptation at fine spatial scale through chromosomal inversions and mito-nuclear epistasis: Findings in Drosophila subobscura (Diptera: Drosophilidae)

“…Linkage disequilibrium among mitochondrial haplotypes and chromosomal arrangements was tested separately in each population, and for the whole sample set according to Jelić et al (2012a, b) and Oliver et al (2002). D and D´ values were estimated (Lewontin, 1964).…”

“…Seasonal bottlenecks and population expansion are responsible for the excess of singleton mutations Christie et al, 2010). Considering the two most frequent haplotypes, selection possibly acts jointly on combinations of mitochondrial and nuclear alleles, and several studies have analysed the linkage disequilibrium (LD) between mitochondrial haplotypes and chromosomal inversions (Oliver et al, 2002;Jelić et al, 2012a, b). These studies show transient LD due to temporal and spatial differences in the action of ecologically specifi c selection pressures.…”