Gene flow and gene flux shape evolutionary patterns of variation in Drosophila subobscura

Abstract

Gene flow (defined as allele exchange between populations) and gene flux (defined as allele exchange during meiosis in heterokaryotypic females) are important factors decreasing genetic differentiation between populations and inversions. Many chromosomal inversions are under strong selection and their role in recombination reduction enhances the maintenance of their genetic distinctness. Here we analyze levels and patterns of nucleotide diversity, selection and demographic history, using 37 individuals of Drosophila subobscura from Mount Parnes (Greece) and Barcelona (Spain). Our sampling focused on two frequent O-chromosome arrangements that differ by two overlapping inversions (OST and O(3+4)), which are differentially adapted to the environment as observed by their opposing latitudinal clines in inversion frequencies. The six analyzed genes (Pif1A, Abi, Sqd, Yrt, Atpα and Fmr1) were selected for their location across the O-chromosome and their implication in thermal adaptation. Despite the extensive gene flux detected outside the inverted region, significant genetic differentiation between both arrangements was found inside it. However, high levels of gene flow were detected for all six genes when comparing the same arrangement among populations. These results suggest that the adaptive value of inversions is maintained, regardless of the lack of genetic differentiation within arrangements from different populations, and thus favors the Local Adaptation hypothesis over the Coadapted Genome hypothesis as the basis of the selection acting on inversions in these populations.

Figure 1

Top: location of the six gene regions studied in the O₃₊₄ and O_ST arrangements in comparison with the ancestral O₃ arrangement. The O-chromosome is divided in sections SI and SII, where SI is the fragment covered by the overlapped inversions O₃₊₄. Bottom: sequenced fragment for each locus. Exonic regions are identified using gray boxes, and intronic regions are represented by lines. For each gene, the size of the sequenced fragment is given in parentheses.

Figure 2

Polytene chromosome of third instar larvae preparation of O₃₊₄/O_ST heterokaryotype. The two overlapped inversions (right of the image) are located opposite to the centromere, in region SI. A full color version of this figure is available at the Heredity journal online.

Figure 3

Neighbor-joining gene genealogy based on total nucleotide variation in (a) the concatenated data set of the five genes (Pif1A, Sqd, Yrt, Atpα and Fmr1) and in (b) the Fmr1 gene alone. D. madeirensis and D. pseudoobscura were used as outgroups. Only bootstrap values above 70% are shown. (Δ) O₃₊₄ from Mt. Parnes, (▵) O₃₊₄ from Barcelona, (◊) O_ST from Mt. Parnes and (♦) O_ST from Barcelona. Asterisks indicate recombinant individuals.