Range expansion promotes cooperation in an experimental microbial metapopulation

Abstract

Natural populations throughout the tree of life undergo range expansions in response to changes in the environment. Recent theoretical work suggests that range expansions can have a strong effect on evolution, even leading to the fixation of deleterious alleles that would normally be outcompeted in the absence of migration. However, little is known about how range expansions might influence alleles under frequency-or density-dependent selection. Moreover, there is very little experimental evidence to complement existing theory, since expanding populations are difficult to study in the natural environment. In this study, we have used a yeast experimental system to explore the effect of range expansions on the maintenance of cooperative behaviors, which commonly display frequency-and density-dependent selection and are widespread in nature. We found that range expansions favor the maintenance of cooperation in two ways: (i) through the enrichment of cooperators at the front of the expanding population and (ii) by allowing cooperators to "outrun" an invading wave of defectors. In this system, cooperation is enhanced through the coupling of population ecology and evolutionary dynamics in expanding populations, thus providing experimental evidence for a unique mechanism through which cooperative behaviors could be maintained in nature.microbes | Allee effect | eco-evolutionary feedback N atural populations often increase the geographical area that they occupy through population growth and dispersal into new territory (1-4). Such events, termed range expansions, occur repeatedly during the life history of a species in response to changes in the environment (for instance, forest fires or seasonal changes in climate) as well as changes in phenotype that allow the species to colonize regions that were previously inaccessible to them (1, 5). Despite their widespread occurrence, the effect of range expansions on genetic diversity has only begun to be explored. Recent theoretical analyses suggest that genetic drift on the low-density front of an expanding population can lead to the fixation of neutral (or even deleterious) alleles in a way that mimics positive selection (6, 7). This effect, known as "allele surfing," is a stochastic effect that has been demonstrated experimentally for neutral alleles in expanding bacterial colonies (8) and was recently suggested to underlie the global patterns of human phenotypic variation observed today (9-11).Here, we chose to study the maintenance of cooperative alleles in the context of populations undergoing range expansions. By definition, a "cooperator" provides a benefit to other members of the population at a cost to itself (12). Examples of cooperation are ubiquitous in the wild, ranging from siderophore production in bacteria to the formation of communities in human populations (12-15). However, given the appearance of "defectors" that exploit the benefit provided by the cooperators without incurring the cost, explaining the origin and maintenance of cooperation in nature remains...

Male tolerance and male–male bonds in a multilevel primate society

“…More specifically, mutations that occur at the edge of an expanding population can reach much higher allele frequencies than seen in stationary populations (44). This effect, known as "gene surfing" (45), has been documented in microbial communities (46,47), tortoises (48), and humans (49). Therefore an intriguing question is whether some of the variation among baboons may be related to demographic factors acting during the range expansion of the genus during the Pleistocene.…”

Range expansions transition from pulled to pushed waves as growth becomes more cooperative in an experimental microbial population

“…For example, range expansions of microbial populations have revealed the dependence of the invasion velocity on the supply of resources (37) and demographic stochasticity (33). Experiments with microbes have also demonstrated the strong effect of range expansion on competition (38)(39)(40)(41)(42)(43)(44) and neutral evolution via the founder effect or gene surfing (45,46). In this study, we focus on expansions with and without the Allee effect and quantify their differences.…”

Speed of Invasion of an Expanding Population by a Horizontally Transmitted Trait

“…Recent work (Klopfstein et al 2006;Hallatschek et al 2007;Excoffier and Ray 2008;Hallatschek andNelson 2008, 2009;Excoffier et al 2009;Korolev et al 2010) has focused on the amplification of genetic drift at the low-density fronts of expanding populations, strikingly demonstrated in experiments with neutral, fluorescently labeled strains of bacteria and yeast (Hallatschek et al 2007;Hallatschek and Nelson 2009). Range expansion may also favor the maintenance of cooperative traits, both by enrichment of cooperators at the front and by allowing them to outrun noncooperative cheats (Sen Datta et al 2013).…”