Rapid evolution of a large structural polymorphism during a bacterial epidemic

TL;DR

A large genetic variation in Daphnia magna is linked to immune response and rapidly changed during a bacterial outbreak.

Contribution

Discovery of a large structural polymorphism in Daphnia magna associated with immune function and rapid evolutionary change.

Findings

The LSP-5-1.1 haplotype is nearly perfectly correlated with susceptibility to Pasteuria ramosa.

Strong selection against LSP-5-1.1 occurred during a P. ramosa epidemic, increasing population resistance.

Balancing selection suggests counter selection against the resistant form by an unknown mechanism.

Abstract

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 large structural polymorphism (LSP) encompass 2–5 Mb regions where homology is undetectable and that contain largely non-overlapping sets of genes. One haplotype (LSP-5-1.1) shows a near-perfect correlation with susceptibility to a common strain of the virulent bacterium, Pasteuria ramosa, which is a common and widespread parasite of D. magna. Rapid selection against LSP-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 for this structural polymorphism—suggesting counter selection against the resistant form by a yet unidentified mechanism.

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