Deleterious Mutations Can Surf to High Densities on the Wave Front of an Expanding Population

Abstract

There is an increasing recognition that evolutionary processes play a key role in determining the dynamics of range expansion. Recent work demonstrates that neutral mutations arising near the edge of a range expansion sometimes surf on the expanding front leading them rather than that leads to reach much greater spatial distribution and frequency than expected in stationary populations. Here, we extend this work and examine the surfing behavior of nonneutral mutations. Using an individual-based coupled-map lattice model, we confirm that, regardless of its fitness effects, the probability of survival of a new mutation depends strongly upon where it arises in relation to the expanding wave front. We demonstrate that the surfing effect can lead to deleterious mutations reaching high densities at an expanding front, even when they have substantial negative effects on fitness. Additionally, we highlight that this surfing phenomenon can occur for mutations that impact reproductive rate (i.e., number of offspring produced) as well as mutations that modify juvenile competitive ability. We suggest that these effects are likely to have important consequences for rates of spread and the evolution of spatially expanding populations.

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

“…Our results are consistent with previous studies in demonstrating that mutation surfing can play an important role in determining the survival probability and spatial distribution of mutants occurring at a front (Edmonds et al, 2004;Klopfstein et al, 2006;Travis et al, 2007). These new results serve to highlight that both the survival probability and the characteristics of surviving mutants are highly dependent on landscape structure and the dispersal behaviour of individuals around habitat edges.…”

“…A recent, direct extension of the Edmonds et al (2004) approach has demonstrated that the surfing effect is important regardless of a mutant's fitness effect ; mutations occurring close to the front of an expanding range always have a higher probability of survival, on average reach a higher total abundance and are present within a greater number of demes. 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.…”

“…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. In particular we are interested in how habitat edges, and the behaviour of individuals at those edges, determine the dynamics of a novel mutation.…”

Exploring neutral and adaptive processes in expanding populations of gilthead sea bream, Sparus aurata L., in the North-East Atlantic

“…Among the several genetic consequences of range expansion described in Excoffier et al (2009a), the surfing of rare variants on the front of the expansion wave can mimic divergent selection, generating strong F ST values only at few loci (Travis et al, 2007(Travis et al, , 2010Excoffier and Ray, 2008;Hallatschek and Nelson, 2008). BLAST results failed to provide any tangible evidence of functional genes associated with Ad-10 and/or Bld-10.…”

Early insights into the genetic consequences of range expansions

“…It is only in the last 3-4 years that researchers have started to explore in detail the interaction between selection and colonization during range expansions, especially in conjunction with the surfing phenomenon (Travis et al, 2007;Excoffier et al, 2009). We will never know for sure, but it might be that, had Ibrahim et al included selection in their simulation study, their paper would have not fared so well, because most researchers would have been unprepared.…”