Gene surfing in expanding populations

Lyman Laboratory of Physics, Harvard University, 17 Oxford Street, Cambridge, MA 02138, USA.
Theoretical Population Biology (Impact Factor: 1.7). 03/2008; 73(1):158-70. DOI: 10.1016/j.tpb.2007.08.008
Source: PubMed


Large scale genomic surveys are partly motivated by the idea that the neutral genetic variation of a population may be used to reconstruct its migration history. However, our ability to trace back the colonization pathways of a species from their genetic footprints is limited by our understanding of the genetic consequences of a range expansion. Here, we study, by means of simulations and analytical methods, the neutral dynamics of gene frequencies in an asexual population undergoing a continual range expansion in one dimension. During such a colonization period, lineages can fix at the wave front by means of a "surfing" mechanism [Edmonds, C.A., Lillie, A.S., Cavalli-Sforza, L.L., 2004. Mutations arising in the wave front of an expanding population. Proc. Natl. Acad. Sci. 101, 975-979]. We quantify this phenomenon in terms of (i) the spatial distribution of lineages that reach fixation and, closely related, (ii) the continual loss of genetic diversity (heterozygosity) at the wave front, characterizing the approach to fixation. Our stochastic simulations show that an effective population size can be assigned to the wave that controls the (observable) gradient in heterozygosity left behind the colonization process. This effective population size is markedly higher in the presence of cooperation between individuals ("pushed waves") than when individuals proliferate independently ("pulled waves"), and increases only sub-linearly with deme size. To explain these and other findings, we develop a versatile analytical approach, based on the physics of reaction-diffusion systems, that yields simple predictions for any deterministic population dynamics. Our analytical theory compares well with the simulation results for pushed waves, but is less accurate in the case of pulled waves when stochastic fluctuations in the tip of the wave are important.

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    • "Initially, deleterious mutations accumulate at a higher rate than beneficial mutations, resulting in a decrease of the mean fitness. Because the expansion slows down over time, selection becomes more efficient on the wave front (Hallatschek and Nelson 2008), and after some time, an equilibrium is reached, and deleterious mutations are established at the same rate as beneficial mutations (fig. 7B). "
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    ABSTRACT: Expanding populations incur a mutation burden, the so-called expansion load. Using a mixture of individual-based simulations and analytical modeling, we study the expansion load process in models where population growth depends on the population's fitness (i.e., hard selection). We show that expansion load can severely slow down expansions and limit a species' range, even in the absence of environmental variation. We also study the effect of recombination on the dynamics of a species range and on the evolution of mean fitness on the wave front. If recombination is strong, mean fitness on front approaches an equilibrium value at which the effects of fixed mutations cancel each other out. The equilibrium rate at which new demes are colonized is similar to the rate at which beneficial mutations spread through the core. Without recombination, the dynamics is more complex, and beneficial mutations from the core of the range can invade the front of the expansion, which results in irregular and episodic expansion. Although the rate of adaptation is generally higher in recombining organisms, the mean fitness on the front may be larger in the absence of recombination because high-fitness individuals from the core have a higher chance to invade the front. Our findings have important consequences for the evolutionary dynamics of species ranges as well as on the role and the evolution of recombination during range expansions.
    The American Naturalist 04/2015; 185(4):E81-E93. DOI:10.1086/680220 · 3.83 Impact Factor
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    • "Identifying the initial founder population in Australia is important to help determine if genetic changes are caused by local adaptation, genetic drift or other evolutionary forces (Dlugosch and Parker 2008). The original founder population is predicted to have the highest genotypic diversity due to genetic drift further reducing diversity in subsequent founder populations (Hallatschek and Nelson 2008). Among all the Australian A. rabiei populations, the SA-Kingsford population contained the highest genotypic diversity, as well as the most alleles (40 out of 70 total alleles), the highest gene diversity (H = 0.174) and allelic richness (A R = 1.83), indicating it as the original founder Fig. 3 Median-joining network obtained for 20 polymorphic microsatellite loci for Australian A. rabiei isolates collected from different host genotypes with different resistance levels (N = 206). "
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    ABSTRACT: The study examined the genetic structure and potential for adaption to host genotype of Ascochyta rabiei, a major necrotrophic fungal pathogen of chickpea. For this, A. rabiei populations derived from six major chickpea growing regions in Australia were characterized using 20 polymorphic microsatellite markers. The overall gene (H = 0.094) and genotypic (D = 0.80) diversities among the entire population were low, indicating the establishment of a recent founder population. Since, no significant genetic differentiation was detected among growing regions, subsequent anthropogenic dispersal was proposed, mainly through seed movement. The highest genotypic diversity and allelic richness was detected at Kingsford, South Australia, thought to be one of the sites of industry establishment in the 1970s and hence the centre of introduction. Despite assessing 206 isolates collected in 2010 from host genotypes with differential disease responses, no significant co-occurrence of fungal haplotype with host genotype was detected. Rather a single haplotype that accounted for 70 % of the total isolates assessed was detected on all host genotypes assessed and from all regions. Therefore, we propose that up until 2010, host reaction was not a major influence on the Australian A. rabiei population structure. Additionally, the detection of a single mating type only, MAT1-2 indicated asexual reproduction, further influencing low haplotype diversity and resulting in a population comprising of multiple clones with relatively few haplotypes compared to populations in other continents.
    Biological Invasions 02/2015; 17(2). DOI:10.1007/s10530-014-0752-8 · 2.59 Impact Factor
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    • "While supplementing the field studies, the mathematical models of the spatio-temporal dynamics of the studied trophic systems give an idealized description of the interactions between the populations of the phytophagous insect, the weed plant, and the cultivar competing with it (Kovalev and Vechernin, 1986, 1989; Tyutyunov and Titova, 2013; Tyutyunov et al., 2013). Such models can explain both the regularities of microevolutionary changes in the phytophage population (Kovalev, 1989b; Tyutyunov et al., 2007, 2013; Edmonds et al., 2008; Hallatschek and Nelson, 2008; Lehe et al., 2012) and the mechanism of SPW efficiency: the local result of suppression of dense weed biomass in the passing of the SPW is reinforced by the competitors of the common ragweed which remain suppressed in the absence of the leaf beetle (Fig. 1). The results of field research and observations, and also computing experiments with mathematical models reveal the systemic effect of the biological weed control method, which is intensified manifold due to synergistic interaction of phytophage population waves and competitive replacement of the weed by the local plant species (Kovalev and Onosovskaya, 1989; Ipatov et al., 1989; Kovalev et al., 1989; Matishov et al., 2011). "
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    ABSTRACT: Evaluation of the efficiency of large-scale projects of phytophage introduction for weed control is of importance for both the theory and practice of biological control. Introduction of the ragweed leaf beetle Zygogramma suturalis F. into the USSR in the 1960–80s is an example of such a project. The main theoretical result of this project was the discovery of the phenomenon of the solitary population wave (SPW), which is a necessary condition for successful biological control of the invasive weed. Recent investigations confirm the long-term efficiency of acclimation of the common ragweed phytophages in the South of Russia. The disappearance of a huge phytomass of the common ragweed in the fields, an abrupt drop in the seed density in the soil, reduction of the infestation areas, and absence of large and dense weed patches in satellite images testify to the fact that the goal of phytophage introduction, i.e., suppression of the common ragweed in agrophytocenoses, has been met. The tasks of the next phase of ragweed suppression are discussed in view of the role of the common ragweed as a synanthropic allergic agent and a ruderal plant growing in anthropogenically transformed territories.
    Entomological Review 02/2015; 95(1):1-14. DOI:10.1134/S0013873815010017
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