Microbial Ecology and Population Biology
The evolution and potentially even the survival of a spatially expanding population depends on its genetic diversity, which can decrease rapidly due to a serial founder effect. The strength of the founder effect is predicted to depend strongly on the details of the growth dynamics. Here, we probe this dependence experimentally using a single microbial species, Saccharomyces cerevisiae, expanding in multiple environments that induce varying levels of cooperativity during growth. We observe a
... h. We observe a drastic reduction in diversity during expansions when yeast grows noncooperatively on simple sugars, but almost no loss of diversity when cooperation is required to digest complex metabolites. These results are consistent with theoretical expectations: When cells grow independently from each other, the expansion proceeds as a pulled wave driven by growth at the low-density tip of the expansion front. Such populations lose diversity rapidly because of the strong genetic drift at the expansion edge. In contrast, diversity loss is substantially reduced in pushed waves that arise due to cooperative growth. In such expansions, the low-density tip of the front grows much more slowly and is often reseeded from the genetically diverse population core. Additionally, in both pulled and pushed expansions, we observe a few instances of abrupt changes in allele fractions due to rare fluctuations of the expansion front and show how to distinguish such rapid genetic drift from selective sweeps. range expansions | cooperative growth | serial founder effect | genetic drift | Allee effect S patial population expansions occur at multiple scales, from the growth of bacterial biofilms and tumors to the spread of epidemics across the globe (1-4). Natural populations often undergo range shifts or range expansions, in response to changing climate, and increasingly, following introduction into novel geographical areas due to trade, travel, and other anthropogenic factors (5-7). The fate of these spatially expanding populations depends on their genetic diversity, which allows them to adapt to the new environment (8). The very process of spatial expansion is, however, predicted to erode the diversity of the population (9, 10), since the newly colonized territory is seeded by only a subset of the genotypes that exist in the original population. This phenomenon, known as the founder effect, greatly amplifies genetic drift in the population and leads to diversity loss and accumulation of deleterious mutations (11-13). Thus, a firm understanding of the founder effect is necessary to predict and control the fate of expanding species. While diversity is lost during all expansions, the rate of loss is theoretically expected to be strongly influenced by the expansion dynamics, which depend on the details of dispersal and growth. Depending on the expansion dynamics, population expansions can be classified into 2 categories-pulled and pushed. In populations that do not exhibit any within-species cooperation, the growth rate is maximum at low densities and decreases monotonically as the density increases. In such populations, migrants at the low-density tip of the wave grow at the fastest rate and drive the expansion into the new area. Such expansions are called pulled waves, and their expansion velocity, also known as the Fisher velocity, depends solely on the diffusion rate of the individuals and the growth rate of the species at low density. On the other hand, pushed waves occur in the presence of cooperative growth within the population (i.e., positive density dependence of the growth rate, also known as the Allee effect) whereby the tip grows at a much lower rate than the higher-density bulk (14-17). Since the growth rate at low density in such populations is lower than in the bulk, the Fisher velocity for such populations is lower than the actual expansion velocity, while the wave fronts are steeper compared to Fisher waves with identical diffusion and low-density growth rates (14, 15, 18) . This difference in the dynamics of pulled and pushed waves is predicted to have substantial genetic consequences (19-21), although they have not been fully tested quantitatively in empirical studies (22) . In their simplest form, range expansions can be viewed as a series of founding events, where a small subpopulation establishes a colony in a new territory, grows rapidly, and then seeds the next founder population. This series of population bottlenecks quickly erodes the genetic diversity in the population, a process aptly called the serial founder effect. The bottlenecks are less severe for species with an Allee effect because growth in the low-density founding colonies is subdued. Indeed, the slow growth of the founders provides sufficient time for the arrival of migrants from the genetically diverse population bulk. Thus, genetic diversity is predicted to persist much longer and over longer distances in populations with an Allee effect (Fig. 1A) . This differential rate of diversity loss in pulled and pushed waves is well characterized in a wide range of theoretical models (20, 21, 23-25) and has also been observed empirically in field studies (26). However, it has been difficult to directly connect the empirical observations to theory (22, 26), in part because these natural expansions cannot be replicated, and also because numerous Significance Spatially expanding populations lose genetic diversity rapidly because of repeated bottlenecks formed at the colonization front. However, the rate of diversity loss depends on the specifics of the expanding population, such as its growth and dispersal dynamics. We have previously demonstrated that changing the amount of within-species cooperation leads to a qualitative transition in the nature of expansion from pulled (driven by growth at the low-density tip) to pushed (driven by migration from the high-density region at the front, but behind the tip). Here we demonstrate experimentally that pushed waves result in strongly reduced genetic drift during range expansions, thus preserving genetic diversity in the newly colonized region.