The rate of beneficial mutations surfing on the wave of a range expansion.

Many theoretical and experimental studies suggest that range expansions can have severe consequences for the gene pool of the expanding population. Due to strongly enhanced genetic drift at the advancing frontier, neutral and weakly deleterious mutations can reach large frequencies in the newly colo...

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Main Authors: Rémi Lehe, Oskar Hallatschek, Luca Peliti
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS Computational Biology
Online Access:http://europepmc.org/articles/PMC3315454?pdf=render
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spelling doaj-05f1b1adefff4ef9812e6cc351d409cf2020-11-25T02:00:16ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582012-01-0183e100244710.1371/journal.pcbi.1002447The rate of beneficial mutations surfing on the wave of a range expansion.Rémi LeheOskar HallatschekLuca PelitiMany theoretical and experimental studies suggest that range expansions can have severe consequences for the gene pool of the expanding population. Due to strongly enhanced genetic drift at the advancing frontier, neutral and weakly deleterious mutations can reach large frequencies in the newly colonized regions, as if they were surfing the front of the range expansion. These findings raise the question of how frequently beneficial mutations successfully surf at shifting range margins, thereby promoting adaptation towards a range-expansion phenotype. Here, we use individual-based simulations to study the surfing statistics of recurrent beneficial mutations on wave-like range expansions in linear habitats. We show that the rate of surfing depends on two strongly antagonistic factors, the probability of surfing given the spatial location of a novel mutation and the rate of occurrence of mutations at that location. The surfing probability strongly increases towards the tip of the wave. Novel mutations are unlikely to surf unless they enjoy a spatial head start compared to the bulk of the population. The needed head start is shown to be proportional to the inverse fitness of the mutant type, and only weakly dependent on the carrying capacity. The precise location dependence of surfing probabilities is derived from the non-extinction probability of a branching process within a moving field of growth rates. The second factor is the mutation occurrence which strongly decreases towards the tip of the wave. Thus, most successful mutations arise at an intermediate position in the front of the wave. We present an analytic theory for the tradeoff between these factors that allows to predict how frequently substitutions by beneficial mutations occur at invasion fronts. We find that small amounts of genetic drift increase the fixation rate of beneficial mutations at the advancing front, and thus could be important for adaptation during species invasions.http://europepmc.org/articles/PMC3315454?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Rémi Lehe
Oskar Hallatschek
Luca Peliti
spellingShingle Rémi Lehe
Oskar Hallatschek
Luca Peliti
The rate of beneficial mutations surfing on the wave of a range expansion.
PLoS Computational Biology
author_facet Rémi Lehe
Oskar Hallatschek
Luca Peliti
author_sort Rémi Lehe
title The rate of beneficial mutations surfing on the wave of a range expansion.
title_short The rate of beneficial mutations surfing on the wave of a range expansion.
title_full The rate of beneficial mutations surfing on the wave of a range expansion.
title_fullStr The rate of beneficial mutations surfing on the wave of a range expansion.
title_full_unstemmed The rate of beneficial mutations surfing on the wave of a range expansion.
title_sort rate of beneficial mutations surfing on the wave of a range expansion.
publisher Public Library of Science (PLoS)
series PLoS Computational Biology
issn 1553-734X
1553-7358
publishDate 2012-01-01
description Many theoretical and experimental studies suggest that range expansions can have severe consequences for the gene pool of the expanding population. Due to strongly enhanced genetic drift at the advancing frontier, neutral and weakly deleterious mutations can reach large frequencies in the newly colonized regions, as if they were surfing the front of the range expansion. These findings raise the question of how frequently beneficial mutations successfully surf at shifting range margins, thereby promoting adaptation towards a range-expansion phenotype. Here, we use individual-based simulations to study the surfing statistics of recurrent beneficial mutations on wave-like range expansions in linear habitats. We show that the rate of surfing depends on two strongly antagonistic factors, the probability of surfing given the spatial location of a novel mutation and the rate of occurrence of mutations at that location. The surfing probability strongly increases towards the tip of the wave. Novel mutations are unlikely to surf unless they enjoy a spatial head start compared to the bulk of the population. The needed head start is shown to be proportional to the inverse fitness of the mutant type, and only weakly dependent on the carrying capacity. The precise location dependence of surfing probabilities is derived from the non-extinction probability of a branching process within a moving field of growth rates. The second factor is the mutation occurrence which strongly decreases towards the tip of the wave. Thus, most successful mutations arise at an intermediate position in the front of the wave. We present an analytic theory for the tradeoff between these factors that allows to predict how frequently substitutions by beneficial mutations occur at invasion fronts. We find that small amounts of genetic drift increase the fixation rate of beneficial mutations at the advancing front, and thus could be important for adaptation during species invasions.
url http://europepmc.org/articles/PMC3315454?pdf=render
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