Programmed Allee effect in bacteria causes a tradeoff between population spread and survival

Dispersal is necessary for spread into new habitats, but it has also been shown to inhibit spread. Theoretical studies have suggested that the presence of a strong Allee effect may account for these counterintuitive observations. Experimental demonstration of this notion is lacking due to the difficulty in quantitative analysis of such phenomena in a natural setting. We engineered Escherichia coli to exhibit a strong Allee effect and examined how the Allee effect would affect the spread of the engineered bacteria. We showed that the Allee effect led to a biphasic dependence of bacterial spread on the dispersal rate: spread is promoted for intermediate dispersal rates but inhibited at low or high dispersal rates. The shape of this dependence is contingent upon the initial density of the source population. Moreover, the Allee effect led to a tradeoff between effectiveness of population spread and survival: increasing the number of target patches during dispersal allows more effective spread, but it simultaneously increases the risk of failing to invade or of going extinct. We also observed that total population growth is transiently maximized at an intermediate number of target patches. Finally, we demonstrate that fluctuations in cell growth may contribute to the paradoxical relationship between dispersal and spread. Our results provide direct experimental evidence that the Allee effect can explain the apparently paradoxical effects of dispersal on spread and have implications for guiding the spread of cooperative organisms.A fundamental question in biology is how the spread and survival of an organism is influenced by various factors (1), including population density (2), dispersal rate (3), and habitat configuration (4). Addressing this question has implications for understanding and controlling biological invasions caused by the introduction of a new species into an established ecosystem (1), the spread of infectious diseases, or the emergence of new pathogens (5).Dispersal has been recognized as being particularly critical in promoting successful spread (e.g., ref. 1; additional examples in SI Text). However, dispersal has also been shown to reduce spread (e.g., ref. 6; additional examples in SI Text). Theoretical studies have proposed that this paradoxical observation can be explained by the Allee effect, which is defined as a positive relationship between individual fitness and the total density of the population (7, 8). In the extreme case, called a strong Allee effect, the population will display a negative fitness, which can be manifested as a negative growth rate, when its initial density is below a critical threshold. Often, a strong Allee effect can be due to the inability to initiate a cooperative behavior at low density (7). This dynamic is observed in several contexts of biology including invasive species, reintroduction biology, epidemiology, the infection of an individual host by microbial pathogens, and quorum sensing (SI Text).By assuming a strong Allee effect, theoretical studies have predicted that dispersal can have a dual effect on population survival and spread. Slow dispersal can prevent the colonization of new territories because the number of individuals arriving in a new area is insufficient to establish a new population (e.g., ref. 9; additional examples in SI Text). Fast dispersal can act as a drain on a source population, which can become too small to be maintained (e.g., ref. 10; additional examples in SI Text). These predictions have been invoked previously to explain the failure of organisms to expand their ranges or to become established (SI Text and Table S1).Although this theoretical explanation is plausible, its experimental demonstration is lacking. This is particularly difficult to verify experimentally in a natural setting because such settings are subject to numerous confounding factors that can obscure the contribution of individual components to the outcome of successful spread. Along this line, it has been suggested that environmental and demographic stochasticity may contribute to population extinction, even in species without an Allee effect (SI Text). The role of a strong Allee effect is further complicated by the limited number of empirical studies that demonstrate the existence of an Allee effect (11), in part due to difficulty in quantifying and studying small populations.To overcome these difficulties, we engineered a gene circuit to confer a strong Allee effect in Escherichia coli and examined its impact on spread and survival. Synthetic biology involves creating novel behaviors in biological systems using gene circuits. These synthetic systems have resulted in numerous novel behaviors including spatial patterning (12) and modulation of fitness (13). Synthetic systems have several advantages over both field and theoretical studies (14). These systems provide a well-defined system to focus on the key, fundamental parameters in a more definitive manner, and they allow direct mapping between modeling and experiments. Although modeling is often used as a driving force in such studies, the ability to confirm the model predictions in a living system serves as a critical proof-of-principle for the plausibility of these predictions. The use of synthetic gene circuits can be thought of as an extension to the use of microbes as model systems to examine questions in evolution and ecology (e.g., ref. 15).