Parallel Adaptation: One or Many Waves of Advance of an Advantageous Allele?

Abstract

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 environment by multiple mutations of similar phenotypic effect that arise in parallel, at the same locus or different loci. These mutations can each quickly reach intermediate frequency, preventing any single one from rapidly sweeping to fixation globally, leading to a ''soft'' sweep in the population. Here we study various models of parallel mutation in a continuous, geographically spread population adapting to a global selection pressure. The slow geographic spread of a selected allele due to limited dispersal can allow other selected alleles to arise and start to spread elsewhere in the species range. When these different selected alleles meet, their spread can slow dramatically and so initially form a geographic patchwork, a random tessellation, which could be mistaken for a signal of local adaptation. This 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 are captured by a single compound parameter, a characteristic length, which 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. While our knowledge of these parameters is poor, we argue that even in widely dispersing species, such parallel geographic sweeps may be surprisingly common. Thus, we predict that as more data become available, many more examples of intraspecies parallel adaptation will be uncovered.

Human population structure and the adaptive response to pathogen-induced selection pressures

“…This observation loosely fits with the parallel mutation model of Ralph & Coop [36] in which multiple adaptive haplotypes arise and spread in response to the same selective pressure. The geographical extent of the spread is perhaps associated with age of the mutation.…”

“…In a recent paper, Ralph & Coop [36] explore the consequences of the speed at which an advantageous allele spreads for the genetic architecture of a trait. In particular, they consider cases in which adaptation to a novel selection pressure (such as a novel pathogen) might take place by 'multiple' mutations of similar phenotypic consequence that arise independently at the same locus or different loci (parallel mutations).…”

“…The waves eventually meet and form a tiling of the habitat with unique advantageous haplotypes. Adapted from Ralph & Coop [36].…”

Population genetics of malaria resistance in humans

“…Mediterranean S alleles appear to descend from the African S alleles, many of them from the Benin haplotype (Flint et al, 1998). Recently, Ralph and Coop (2010) have shown that such parallel adaptation of multiple S alleles is not inconsistent with their theoretical spatial model and general estimates of mutation rate, gene flow, selection and population size, a finding consistent with that of Karasov et al (2010) who suggest that mutation does not limit adaptation in many situations. On the other hand, it has been proposed that a plausible explanation for much of the haplotype diversity around S alleles is that it reflects past recombination and gene conversion (Flint et al, 1998).…”

Genetic hitchhiking in spatially extended populations

“…The analogue of the stochastic partial differential equation (3) has no solution in dimensions two or higher and so the theory that we have appealed to above has no counterpart. Ralph and Coop (2010) examine the patterns of diversity resulting from competing selective sweeps arising through parallel adaptation. The randomness in their model is associated with the time and spatial location at which favoured alleles arise rather than genetic drift.…”