Mutation surfing and the evolution of dispersal during range expansions J. M. J. TRAVIS *, T. MU ¨ NKEMU ¨ LLER* & O. J. BURTON* *Zoology Building, Institute of Biological and Environmental Sciences, University of Aberdeen, Scotland, UK Laboratoire d’Ecologie Alpine, Universite ´ J. Fourier, Grenoble, France Introduction There is a growing interest in the evolutionary dynamics of populations that are expanding their ranges (see reviews by Ha ¨nfling & Kollmann, 2002; Lambrinos, 2004; Hastings et al., 2005; Phillips et al., 2010). Studies have demonstrated that a range of life history character- istics can come under strong selection at an expanding front (selfing-rates – Daehler, 1998; resistance to herbi- vores – Garcia-Rossi et al., 2003; dispersal behaviour – Simmons & Thomas, 2004; Phillips et al., 2006) and that, at least in some cases, their evolution can modify the spread dynamics (e.g. Simmons & Thomas, 2004; Phillips et al., 2006). Population geneticists have often used spatial patterns of genetic diversity within a species’ Correspondence: Justin M. J. Travis, Zoology Building, Institute of Biological and Environmental Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen, AB24 2TZ, Scotland, UK. Tel.: +44 1224 274483; fax: +44 1224 272396; e-mail: justin.travis@ abdn.ac.uk ª 2010 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 2656–2667 2656 JOURNAL COMPILATION ª 2010 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY Keywords: evolution; evolvability; invasion; range shifting. Abstract A growing body of empirical evidence demonstrates that at an expanding front, there can be strong selection for greater dispersal propensity, whereas recent theory indicates that mutations occurring towards the front of a spatially expanding population can sometimes ‘surf’ to high frequency and spatial extent. Here, we consider the potential interplay between these two processes: what role may mutation surfing play in determining the course of dispersal evolution and how might dispersal evolution itself influence mutation surfing? Using an individual-based coupled-map lattice model, we first run simulations to determine the fate of dispersal mutants that occur at an expanding front. Our results highlight that mutants that have a slightly higher dispersal propensity than the wild type always have a higher survival probability than those mutants with a dispersal propensity lower than, or very similar to, the wild type. However, it is not always the case that mutants with very high dispersal propensity have the greatest survival probability. When dispersal mortality is high, mutants of intermediate dispersal survive most often. Interestingly, the rate of dispersal that ultimately evolves at an expanding front is often substantially higher than that which confers a novel mutant with the greatest probability of survival. Second, we run a model in which we allow dispersal to evolve over the course of a range expansion and ask how the fate of a neutral or nonneutral mutant depends upon when and where during the expansion it arises. These simulations highlight that the success of a neutral mutant depends upon the dispersal genotypes that it is associated with. An important consequence of this is that novel mutants that arise at the front of an expansion, and survive, typically end up being associated with more dispersive genotypes than the wild type. These results offer some new insights into causes and the consequences of dispersal evolution during range expansions, and the methodology we have employed can be readily extended to explore the evolutionary dynamics of other life history characteristics. doi:10.1111/j.1420-9101.2010.02123.x
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Mutation surfing and the evolution of dispersal during range expansions
Abstract A growing body of empirical evidence demonstrates that at an expanding front, there can be strong selection for greater dispersal propensity, whereas recent theory indicates that mutations occurring towards the front of a spatially expanding population can sometimes ‘surf’ to high frequency and spatial extent. Here, we consider the potential interplay between these two processes: what role may mutation surfing play in determining the course of dispersal evolution and how might dispersal evolution itself influence mutation surfing? Using an individual-based coupled-map lattice model, we first run simulations to determine the fate of dispersal mutants that occur at an expanding front. Our results highlight that mutants that have a slightly higher dispersal propensity than the wild type always have a higher survival probability than those mutants with a dispersal propensity lower than, or very similar to, the wild type. However, it is not always the case that mutants with very high dispersal propensity have the greatest survival probability. When dispersal mortality is high, mutants of intermediate dispersal survive most often. Interestingly, the rate of dispersal that ultimately evolves at an expanding front is often substantially higher than that which confers a novel mutant with the greatest probability of survival. Second, we run a model in which we allow dispersal to evolve over the course of a range expansion and ask how the fate of a neutral or nonneutral mutant depends upon when and where during the expansion it arises. These simulations highlight that the success of a neutral mutant depends upon the dispersal genotypes that it is associated with. An important consequence of this is that novel mutants that arise at the front of an expansion, and survive, typically end up being associated with more dispersive genotypes than the wild type. These results offer some new insights into causes and the consequences of dispersal evolution during range expansions, and the methodology we have employed can be readily extended to explore the evolutionary dynamics of other life history characteristics.
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Mutation surfing and the evolution of dispersal during rangeexpansions
J. M. J. TRAVIS*, T. MUNKEMULLER*� & O. J. BURTON*
*Zoology Building, Institute of Biological and Environmental Sciences, University of Aberdeen, Scotland, UK
�Laboratoire d’Ecologie Alpine, Universite J. Fourier, Grenoble, France
Introduction
There is a growing interest in the evolutionary dynamics
of populations that are expanding their ranges (see
reviews by Hanfling & Kollmann, 2002; Lambrinos,
2004; Hastings et al., 2005; Phillips et al., 2010). Studies
have demonstrated that a range of life history character-
istics can come under strong selection at an expanding
front (selfing-rates – Daehler, 1998; resistance to herbi-
vores – Garcia-Rossi et al., 2003; dispersal behaviour –
Simmons & Thomas, 2004; Phillips et al., 2006) and that,
at least in some cases, their evolution can modify the
propensity than has evolved in a stationary range have
very low surfing probabilities; they are highly unlikely to
remain for long on the front as the wild-type individuals
are more dispersive. Interestingly, however, these low
dispersal mutants frequently survive for substantial
periods. This is explained by the fact that mutants are
introduced into a low-density region at an expanding
front. This provides an opportunity for the mutants to
gain a foothold and obtain reasonable local abundance
Den
sity
0 100 200 300 400 500
020
040
060
0
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MutantWild
Evo
lved
dis
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ate
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0.0
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0.4
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0.8(b)
Den
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0(c)
Evo
lved
dis
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0.0
0.2
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x-direction
(d)
Fig. 6 Example results for a surfing mutation (plot a and b) and a
surviving but not surfing mutation (plot c and d) after 300 timesteps
in simulations with evolution. The surfing mutation occupies the
complete wave of expansion from the point of introduction to the
front and has much higher evolved dispersal rates. However, if the
mutation survives but does not surf, it is vice versa. The wild type
has higher densities and higher dispersal rates at the front. Density is
the sum of individuals present across the 25 columns. These results
are for combination 2 of the parameter values with mut = 0.001.
The expansion occurs on a 25 by 500 cell lattice.
Dispersal mortality
Evo
lved
dis
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ate
0.0
0.2
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0.6
0.8
0.1 0.6
WildMutant
Fig. 7 Overall, evolving dispersal rates of the mutant tend to be
higher than those evolving for the wild type. Boxplots aggregate
results after 300 timesteps for all simulated times of introduction
and all different reproduction rates.
Mutation surfing and dispersal evolution 2663
ª 2 0 1 0 T H E A U T H O R S . J . E V O L . B I O L . 2 3 ( 2 0 1 0 ) 2 6 5 6 – 2 6 6 7
J O U R N A L C O M P I L A T I O N ª 2 0 1 0 E U R O P E A N S O C I E T Y F O R E V O L U T I O N A R Y B I O L O G Y
even when they do not become long-term ‘surfers’. This
process is clearly illustrated in Fig. 5c,d: here, large
proportions of the introduced mutants remain some-
where along the expanding front for several generations
and, even once they have fallen away from the front,
they have accumulated sufficient numbers and selection
is sufficiently weak that they often persist for a