Gene flow and gene flux shape evolutionary 1 patterns of variation in Drosophila 2 subobscura 3 4

15 16 Running title: Gene exchange shaping variation 17 Word count (main text): 5709 18 19 2 Gene flow (defined as allele exchange between populations) and gene flux (defined as 20 allele exchange during meiosis in heterokaryotypic females) are important factors 21 decreasing genetic differentiation between populations and inversions. Many 22 chromosomal inversions are under strong selection and their role in recombination 23 reduction enhances the maintenance of their genetic distinctness. Here we analyze levels 24 and patterns of nucleotide diversity, selection and demographic history using 37 25 individuals of Drosophila subobscura from Mount Parnes (Greece) and Barcelona 26 (Spain). Our sampling focused on two frequent O-chromosome arrangements that differ 27 by two overlapping inversions (O ST and O 3+4), which are differentially adapted to the 28 environment as observed by their opposing latitudinal clines in inversion frequencies. 29 The six analyzed genes (Pif1A, Abi, Sqd, Yrt, Atpα and Fmr1) were selected for their 30 location across the O-chromosome and their implication in thermal adaptation. Despite 31 the extensive gene flux detected outside the inverted region, significant genetic 32 differentiation between both arrangements was found inside it. However, high levels of 33 gene flow were detected for all six genes when comparing the same arrangement among 34 populations. These results suggest that the adaptive value of inversions is maintained 35 regardless the lack of genetic differentiation within arrangements from different 36 populations, and thus favors the Local Adaptation hypothesis over the Coadapted 37 Genome hypothesis as the basis of the selection acting on inversions in these 38 populations. 39 40 dating 42 3 INTRODUCTION 43 Chromosomal inversions are a major mechanism shaping the level and distribution of 44 genomic diversity within and between species. Inversion polymorphism has been 45 described in several Drosophila species (Krimbas and Powell, 1992) and has been 46 observed to vary seasonally, and with altitude and latitude 1993) has played an important role in demonstrating the adaptive role of inversions, as 50 shown by the coinciding latitudinal clines on inversion frequencies found in Palearctic 51 also suggest the adaptive 54 value of inversions in D. subobscura. Despite the evidence for an adaptive role of 55 inversions, the genetic and mechanistic basis underlying their role in adaptation remains 56 unknown. 57 Several hypotheses have been suggested to explain the maintenance of inversion 58 polymorphism in populations (reviewed in Hoffmann and Rieseberg, 2008). The 59 coadaptation hypothesis (Dobzhansky, …