Spatial soft sweeps: Patterns of adaptation in populations with long-range dispersal.

Jayson Paulose,Oskar Hallatschek,Joachim Hermisson,Graham Coop

doi:10.1371/journal.pgen.1007936

Jayson Paulose, Oskar Hallatschek + Show 2 more

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https://doi.org/10.1371/journal.pgen.1007936

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Abstract

Adaptation in extended populations often occurs through multiple independent mutations responding in parallel to a common selection pressure. As the mutations spread concurrently through the population, they leave behind characteristic patterns of polymorphism near selected loci—so-called soft sweeps—which remain visible after adaptation is complete. These patterns are well-understood in two limits of the spreading dynamics of beneficial mutations: the panmictic case with complete absence of spatial structure, and spreading via short-ranged or diffusive dispersal events, which tessellates space into distinct compact regions each descended from a unique mutation. However, spreading behaviour in most natural populations is not exclusively panmictic or diffusive, but incorporates both short-range and long-range dispersal events. Here, we characterize the spatial patterns of soft sweeps driven by dispersal events whose jump distances are broadly distributed, using lattice-based simulations and scaling arguments. We find that mutant clones adopt a distinctive structure consisting of compact cores surrounded by fragmented “haloes” which mingle with haloes from other clones. As long-range dispersal becomes more prominent, the progression from diffusive to panmictic behaviour is marked by two transitions separating regimes with differing relative sizes of halo to core. We analyze the implications of the core-halo structure for the statistics of soft sweep detection in small genomic samples from the population, and find opposing effects of long-range dispersal on the expected diversity in global samples compared to local samples from geographic subregions of the range. We also discuss consequences of the standing genetic variation induced by the soft sweep on future adaptation and mixing.

Highlights

Rare beneficial alleles can rapidly increase their frequency in a population in response to a new selective pressure
When a species is spread out over a large geographic range, different regions may adapt to the same selection pressure by acquiring distinct beneficial mutations
Dispersal strongly influences soft sweep patterns, as it determines how a mutation that arose in one region might

Summary

Introduction

Rare beneficial alleles can rapidly increase their frequency in a population in response to a new selective pressure. When adaptation is limited by the availability of mutations, a single beneficial mutation may sweep through the entire population in the classical scenario of a “hard sweep”. Populations may exploit a high availability of beneficial mutations due to standing variation, recurrent new mutation, or recurrent migration [1,2,3,4,5] to respond quickly to new selection pressures. Multiple adaptive alleles may sweep through the population concurrently, leaving genealogical signatures that distinguish them from hard sweeps. Well-studied examples in humans include multiple origins for the sickle cell trait which confers resistance to malaria [8], and of lactose tolerance within and among geographically separated human populations [9, 10]

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