Rapid evolution of a large highly-divergent haplotype region during a bacterial epidemic

The field of population genetics is primarily focused on simple genetic variants such as single nucleotide polymorphisms (SNPs), small insertions or deletions (INDELs), and copy-number variants (CNVs). However, large-scale genomic variants are beginning to undergo increased scrutiny as new sequencing methods facilitate their discovery. Here, we report an unusually large and highly variable structural feature in the Daphnia magna genome that is strongly associated with immune function. Alternative forms of this genomic structure encompass 2-5 Mb non-homologous regions that contain largely non-overlapping sets of genes. One highly divergent haplotype (HDH-5-1.1) shows a near-perfect correlation with susceptibility to a common strain of the virulent bacterial, Pasteuria ramosa, which is a common and widespread parasite of D. magna. Rapid selection against HDH-5-1.1 was observed during a natural P. ramosa epidemic, coinciding with a strong population-wide increase in resistance. Despite recurrent episodes of strong selection against Pasteuria susceptibility, we observe evidence of balancing selection at this hyper-divergent region - suggesting counter selection against the resistant form by a yet unidentified mechanism.