Genetic drift at expanding frontiers promotes gene segregation

Abstract

Competition between random genetic drift and natural selection play a central role in evolution: Whereas nonbeneficial mutations often prevail in small populations by chance, mutations that sweep through large populations typically confer a selective advantage. Here, however, we observe chance effects during range expansions that dramatically alter the gene pool even in large microbial populations. Initially well mixed populations of two fluorescently labeled strains of Escherichia coli develop well defined, sector-like regions with fractal boundaries in expanding colonies. The formation of these regions is driven by random fluctuations that originate in a thin band of pioneers at the expanding frontier. A comparison of bacterial and yeast colonies (Saccharomyces cerevisiae) suggests that this large-scale genetic sectoring is a generic phenomenon that may provide a detectable footprint of past range expansions.genetic distance ͉ founder effect ͉ microorganisms ͉ range expansion A principal tenet of modern evolutionary biology is that Darwinian selection and random genetic drift compete in driving evolutionary change (1). It is widely accepted that genetic drift can have significant effects on small populations (2) that may even lead to speciation (3). In large populations, however, random sampling effects are generally considered weak compared with selection (4-6) (law of large numbers). A major departure from this paradigmatic behavior occurs when large populations undergo range expansions. The descendents of individuals first settling in a new territory are most likely to dominate the gene pool as the expansion progresses (7-9). Random sampling effects among these pioneers results in genetic drift that can have profound consequences on the diversity of the expanding population. Indeed, spatially varying levels of genetic diversity and colonization patterns appear to be correlated in many species (10-13). For example, the often observed south-north gradient in neutral genetic diversity [''southern richness to northern purity'' (14)] on the northern hemisphere is thought to reflect past range expansions induced by glacial cycles (12). Although these trends indicate that genetic drift during range expansions has shaped the gene pool of many species, the underlying spatial mechanism remains obscure: Diversity gradients are often difficult to interpret and potentially interfere with the signal of spreading beneficial mutations (15,16). In fact, a major challenge of present-day population genetics is to decide whether natural selection or a past demographic process is responsible for the prevalence of common mutations (17).Here, we use simple microbial systems to study the nature of random genetic drift in range expansions of large populations. We observe chance effects that segregate the gene pool into well defined, sector-like regions of reduced genetic diversity. The genetic segregation on the population level is the consequence of number fluctuations on a much smaller scale, within a thin region of reproducing p...

Genetic hitchhiking in spatially extended populations

“…11a). Hallatschek et al (2007) suggest that the motion of lineages within the front is superdiffusive (with variance increasing like t 4/3 ). Although our simulations appear to show mean square displacement increasing linearly with time, there is some noise and it would require more work to reject superdiffusivity.…”

“…The 'surfing' to high frequency of neutral alleles that arise at the frontier of an expanding species, observed in simulations of the stepping stone model, mirrors the rare appearances of highly successful individuals at the wavefront of a population evolving according to (3) described in §2.3. Hallatschek et al (2007); Hallatschek and Nelson (2010) consider expanding microbial colonies and through both in vitro experiments and numerical simulation of individual based models shows how two competing, but equally fit, strains, expanding into new territory in a circular wave, naturally subdivide into sectors of the two types. There are many other observations of sectoring in expanding colonies (e.g Yin (1993); Wei and Krone (2005); Krone et al (2007)).…”

“…On the one hand fixation will take much longer, extending the timescale over which recombination can 'free' the hitchhiking allele, but on the other hand, local founder events at the wavefront may greatly increase genetic drift (Klopfstein et al, 2006;Excoffier et al, 2009;Hallatschek et al, 2007;Nelson, 2008, 2010).…”

Biofilm formation and toxin production provide a fitness advantage in mixed colonies of environmental yeast isolates

“…Instead, growth is mostly limited to the front at the leading edge of the colony (Hallatschek et al., 2007). Therefore, the change in the proportion of the biofilm strain was used as a proxy for fitness.…”

“…Despite their vulnerability to individual cheaters, biofilms are ubiquitous and stable. The leading hypothesis for the stability of biofilm communities is the spatial structure: Competition, cooperation, and passive processes like clonal growth can generate patches of related cooperative cells able to outcompete unrelated cells (e.g., (Anderson, Garcia, & Cotter, 2014; van Gestel, Weissing, Kuipers, & Kovacs, 2014; Hallatschek, Hersen, Ramanathan, & Nelson, 2007; Millet et al., 2014; Momeni, Brileya, Fields, & Shou, 2013; Müller, Neugeboren, Nelson, & Murray, 2014; Nadell & Bassler, 2011; Nadell, Foster, & Xavier, 2010; Van Dyken, Müller, Mack, & Desai, 2013; Xavier & Foster, 2007), recently reviewed in detail in ref. (Nadell, Drescher, & Foster, 2016)).…”