Heterogeneous genomic architecture of skeletal armour traits in sticklebacks

Abstract

Abstract Whether populations adapt to similar selection pressures using the same underlying genetic variants depends on population history and the distribution of standing genetic variation at the metapopulation level. Studies of sticklebacks provide a case in point: when colonizing and adapting to freshwater habitats, three-spined sticklebacks (Gasterosteus aculeatus) with high gene flow tend to fix the same adaptive alleles in the same major loci, whereas nine-spined sticklebacks (Pungitius pungitius) with limited gene flow tend to utilize a more heterogeneous set of loci. In accordance with this, we report results of quantitative trait locus (QTL) analyses using a backcross design showing that lateral plate number variation in the western European nine-spined sticklebacks mapped to 3 moderate-effect QTL, contrary to the major-effect QTL in three-spined sticklebacks and different from the 4 QTL previously identified in the eastern European nine-spined sticklebacks. Furthermore, several QTL were identified associated with variation in lateral plate size, and 3 moderate-effect QTL with body size. Together, these findings indicate more heterogenous and polygenic genetic underpinnings of skeletal armour variation in nine-spined than three-spined sticklebacks, indicating limited genetic parallelism underlying armour trait evolution in the family Gasterostidae.