Patterns of geographic variation of thermal adapted candidate genes in Drosophila subobscura sex chromosome arrangements

Abstract

Background: The role of chromosomal arrangements in adaptation is supported by the repeatable clinal variation in inversion frequencies across continents in colonizing species such as Drosophila subobscura. However, there is a lack of knowledge on the genetic variation in genes within inversions, possibly targets of climatic selection, across a geographic latitudinal gradient. In the present study we analysed four candidate loci for thermal adaptation, located close to the breakpoints, in two chromosomal arrangements of the sex (A) chromosome of Drosophila subobscura with different thermal preferences. Individual chromosomes with A₂ (the inverted arrangement considered warm adapted) or A_ST (the standard ancestral arrangement considered cold adapted) were sequenced across four European localities at varying latitudes, up to ~ 2500 Kms apart.

Results: Importantly, we found very low differentiation for each specific arrangement across populations as well as no clinal patterns of genomic variation. This suggests wide gene exchange along the cline. Differentiation between the sex chromosome arrangements was significant in the two more proximal regions relative to the A_ST orientation but not in the distal ones, independently of their location inside or outside the inversion. This can be possibly due to variation in the levels of gene flux and/or selection acting in these regions.

Conclusions: Gene flow appears to have homogenized the genetic content within-arrangement at a wide geographical scale, despite the expected diverse selective pressures in the specific natural environments of the different populations sampled. It is thus likely that the inversion frequency clines in this species are being maintained by local adaptation in face of gene flow. The differences between arrangements at non-coding regions might be associated with the previously observed differential gene expression in different thermal regimes. Higher resolution genomic scans for individual chromosomal arrangements performed over a large environmental gradient are needed to find the targets of selection and further elucidate the adaptive mechanisms maintaining chromosomal inversion polymorphisms.

Keywords: Chromosomal arrangements; Climatic selection; Clinal variation; Drosophila subobscura; Gene flow; Genetic differentiation; Geographic variation; Thermal adaptation; UTR variation.

Fig. 1

Sampling sites of D. subobscura and frequency, as coloured pies for each locality, of the three sex chromosome arrangements detected (data from [25]). A_ST – dark grey, A₂ – light grey; A₁ – white

Fig. 2

Cytological location of the genes analysed. The grey box represents the region inverted in the A₂ arrangement. Black bars indicate the cytological location of each gene in each chromosomal arrangement

Fig. 3

Principal Coordinate analysis based on genetic differentiation (F_ST) among arrangements and localities for the PhKgamma gene. A_ST groups are represented in blue and A₂ in orange; different localities are indicated by different symbols

Fig. 4

Principal Coordinate analysis based on genetic differentiation (F_ST) among arrangements and localities for the Ubc-E2H gene. A_ST groups are represented in blue and A₂ in orange; different localities are indicated by different symbols

Fig. 5

Genetic diversity (π) within each arrangement and D_xy between arrangements along all gene regions. D_xy – black line; π A_ST – dashed line; π A₂ – dotted line. 5’UTR, intronic and exonic regions are discriminated (see also Table 1). The four gene regions are ordered following the A_ST arrangement (see Fig. 2)