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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    • "This indicates that, of the initially well-mixed drop containing millions of cells, only a fraction formed clonal patches in the growing colony. To quantify the effect of nutrient limitation on diversity loss, we used a previously developed measure of 'heterozygosity' (Nei et al., 1975; Hallatschek and Nelson, 2008; Korolev et al., 2010; Korolev et al., 2011; Materials and methods, Supplementary Figure S5), which refers to diversity at a particular position (pixel) in the colony, averaged over many such local diversity measures in a larger region. The region over which we measure is either an expanding concentric ring around the colony inoculum, which captures the change in diversity as the colony expands (Supplementary Figure S5), or the whole colony (below). "
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    ABSTRACT: Dense microbial groups such as bacterial biofilms commonly contain a diversity of cell types that define their functioning. However, we have a limited understanding of what maintains, or purges, this diversity. Theory suggests that resource levels are key to understanding diversity and the spatial arrangement of genotypes in microbial groups, but we need empirical tests. Here we use theory and experiments to study the effects of nutrient level on spatio-genetic structuring and diversity in bacterial colonies. Well-fed colonies maintain larger well-mixed areas, but they also expand more rapidly compared with poorly-fed ones. Given enough space to expand, therefore, well-fed colonies lose diversity and separate in space over a similar timescale to poorly fed ones. In sum, as long as there is some degree of nutrient limitation, we observe the emergence of structured communities. We conclude that resource-driven structuring is central to understanding both pattern and process in diverse microbial communities.
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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.
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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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