Parallel adaptation: One or many waves of advance of an advantageous allele?

TL;DR

This paper models how multiple advantageous mutations can spread in parallel across a population, forming geographic patches that resemble local adaptation but are actually part of a complex, overlapping sweep process.

Contribution

It introduces a spatial model of parallel mutation spread, linking it to Poisson process crystallization models, and identifies a key length scale governing the likelihood of parallel sweeps.

Findings

Parallel mutations can create geographic patchworks mistaken for local adaptation.

A single characteristic length scale predicts the probability and scale of parallel mutation spread.

Parallel sweeps may be more common in widely dispersing species than previously thought.

Abstract

Our models for detecting the effect of adaptation on population genomic diversity are often predicated on a single newly arisen mutation sweeping rapidly to fixation. However, a population can also adapt to a new situation by multiple mutations of similar phenotypic effect that arise in parallel. These mutations can each quickly reach intermediate frequency, preventing any single one from rapidly sweeping to fixation globally (a "soft" sweep). Here we study models of parallel mutation in a geographically spread population adapting to a global selection pressure. The slow geographic spread of a selected allele can allow other selected alleles to arise and spread elsewhere in the species range. When these different selected alleles meet, their spread can slow dramatically, and so form a geographic patchwork which could be mistaken for a signal of local adaptation. This random spatial tessellation will dissipate over time due to mixing by migration, leaving a set of partial sweeps within the global population. We show that the spatial tessellation initially formed by mutational types is closely connected to Poisson process models of crystallization, which we extend. We find that the probability of parallel mutation and the spatial scale on which parallel mutation occurs is captured by a single characteristic length that reflects the expected distance a spreading allele travels before it encounters a different spreading allele. This characteristic length depends on the mutation rate, the dispersal parameter, the effective local density of individuals, and to a much lesser extent the strength of selection. We argue that even in widely dispersing species, such parallel geographic sweeps may be surprisingly common. Thus, we predict, as more data becomes available, many more examples of intra-species parallel adaptation will be uncovered.