The genetic basis of intrinsic and extrinsic post-zygotic reproductive isolation jointly promoting speciation in the lake whitefish species complex (Coregonus clupeaformis)

Understanding the genetic architecture of reproductive barriers and the evolutionary forces that drove their divergence represents a considerable challenge towards understanding speciation. The objective of this study was to determine the genetic basis of intrinsic and extrinsic post-zygotic isolation in diverging populations of dwarf and normal lake whitefish with allopatric glacial origins. We found that the rate of embryonic mortality was 5.3-6.5 times higher in dwarf-normal hybrid backcrosses during development than in F1 dwarf and normal crosses. When comparing embryos that died during development against larvae that successfully hatched, patterns of Mendelian segregation at 101 loci whose linkage is known identified 13 loci distributed over seven linkage groups that exhibited significant shifts in segregation ratios leading to significant segregation distortion at these loci in the surviving progeny. Controlled crosses and quantitative trait loci analysis revealed a significant genetic basis for developmental time until emergence, a trait critical to fish larval survival in nature. Hatching backcross progeny exhibited asynchronous emergence and transgressive segregation, suggesting that extrinsic post-zygotic isolation may select against hybridization in specific environmental contexts. Evidence of a genetic basis for increased embryonic mortality followed by asynchronous emergence indicated that intrinsic and extrinsic mechanisms are not mutually exclusive in the formation and maintenance of reproductive isolation, but may be jointly promoting population divergence and ultimately speciation.