Haplotype structure – an overlooked key factor shaping the genomic selection response

Genetic redundancy, a hallmark of polygenic adaptation, implies that new trait optima can be reached by frequency changes of a subset of contributing loci. As a result, the genomic response to selection is often heterogeneous among replicate populations. However, linkage disequilibrium (LD) can constrain the genomic response because linked alleles respond jointly, rather than independently. The extent to which haplotype blocks with multiple selection targets shape the genomic response during polygenic adaptation remains unclear. We tested how haplotype structure affects genomic responses to polygenic adaptation with experimental evolution. Three sets of Drosophila simulans lines from the same natural population (supergroups), each with five replicates independently adapted to the same novel temperature regime. The genomic response of replicates within the supergroup was more similar than the response of replicates from different supergroups. This pattern is not expected for freely recombining loci, but it is consistent with the central role of haplotype structure in shaping the genomic response. This effect is evident in the stark contrast between supergroups, which is greater than the differentiation caused by adaptation to two environments. Replicates from a hot fluctuating environment (28/18°C) and a hot constant environment (23°C) clustered together according to supergroup. Computer simulations supported the key role of haplotype structure on the genomic response. Our study highlights the importance of haplotype structure for polygenic selection signatures and further illustrates the stochastic nature of adaptation even when populations adapt to the same selection pressure.