The Frequency of Fitness Peak Shifts Is Increased at Expanding Range Margins Due to Mutation Surfing

Abstract

Dynamic species' ranges, those that are either invasive or shifting in response to environmental change, are the focus of much recent interest in ecology, evolution, and genetics. Understanding how range expansions can shape evolutionary trajectories requires the consideration of nonneutral variability and genetic architecture, yet the majority of empirical and theoretical work to date has explored patterns of neutral variability. Here we use forward computer simulations of population growth, dispersal, and mutation to explore how range-shifting dynamics can influence evolution on rugged fitness landscapes. We employ a two-locus model, incorporating sign epistasis, and find that there is an increased likelihood of fitness peak shifts during a period of range expansion. Maladapted valley genotypes can accumulate at an expanding range front through a phenomenon called mutation surfing, which increases the likelihood that a mutation leading to a higher peak will occur. Our results indicate that most peak shifts occur close to the expanding front. We also demonstrate that periods of range shifting are especially important for peak shifting in species with narrow geographic distributions. Our results imply that trajectories on rugged fitness landscapes can be modified substantially when ranges are dynamic.

Landscape structure and boundary effects determine the fate of mutations occurring during range expansions

“…An increasing number of simulation studies are investigating the dynamics and spatial spread of neutral mutations that occur during a period of range expansion (Ibrahim et al, 1996;Austerlitz and Garnier-Géré, 2003;Edmonds et al, 2004;Bialozyt et al, 2006;Klopfstein et al, 2006) but, to date, far less works have considered the fate of non-neutral mutations. It has recently been demonstrated that the surfing phenomenon observed by Edmonds et al (2004) and Klopfstein et al (2006) is likely to lead to the substantially increased survival and spread of deleterious mutants at the front Burton and Travis, 2008), and the results presented here corroborate with those results. Whereas previous works have focussed on using a centroid statistic to describe spread, here we have used spatial extent (as measured by the number of patches occupied) and total population size, in addition to looking at the maximum x-displacement obtained by a surviving mutation.…”

“…Second, with absorbing boundary conditions, the leading edge of the range expansion is most often away from the edge towards the centre of the lattice (Figure 4a), which is due to additional mortality at absorbing edges leading to less rapid population growth. Mutations are most likely to survive when they occur at, or very close to, the leading edge, as it is only then that they and their descendants are most likely to remain at the front and benefit from reduced competition (Klopfstein et al, 2006;Travis et al, 2007;Burton and Travis, 2008). The first of these effects applies equally to mutations regardless of their fitness effect, but the second has a much greater influence on deleterious mutations, as their survival is much more dependent on them surfing the expanding wave front than it is for neutral or beneficial mutations.…”

“…This model is an extension of recent studies investigating the dynamics of neutral (Edmonds et al, 2004;Klopfstein et al, 2006) and nonneutral Burton and Travis, 2008) mutations arising at expanding range margins. Here, we consider the effects of employing different boundary conditions and the position of a mutation's origin on the fate and distribution of both neutral mutations and those that alter the relative fitness of individuals.…”

“…Mutants, regardless of fitness effect, arising close to the front sometimes surf to high frequency and spatial extent Burton and Travis, 2008). The survival probability of deleterious mutations occurring on the front of an expanding range can be relatively high, up to nearly 20% (Figure 3a), and is conditional on this surfing behaviour.…”

“…Travis et al (2007) also showed that the spatial distribution of a surviving mutant differs considerably depending on its fitness effect, with most surviving beneficial mutations having their centroid close to where they originated, whereas most surviving deleterious mutations have a spatial distribution concentrated close to the expanding front. In a further recent extension, Burton and Travis (2008) developed a two-locus model, incorporating sign epistasis, and demonstrated that fitness peak shifts are more likely during range expansion due to the importance of this surfing effect for the survival and abundance of deleterious mutations. Here, we extend the methods used by Travis et al (2007) to consider how surfing dynamics are influenced by landscape structure.…”