High relatedness maintains multicellular cooperation in a social amoeba by controlling cheater mutants

Abstract

The control of cheating is important for understanding major transitions in evolution, from the simplest genes to the most complex societies. Cooperative systems can be ruined if cheaters that lower group productivity are able to spread. Kin-selection theory predicts that high genetic relatedness can limit cheating, because separation of cheaters and cooperators limits opportunities to cheat and promotes selection against low-fitness groups of cheaters. Here, we confirm this prediction for the social amoeba Dictyostelium discoideum; relatedness in natural wild groups is so high that socially destructive cheaters should not spread. We illustrate in the laboratory how high relatedness can control a mutant that would destroy cooperation at low relatedness. Finally, we demonstrate that, as predicted, mutant cheaters do not normally harm cooperation in a natural population. Our findings show how altruism is preserved from the disruptive effects of such mutant cheaters and how exceptionally high relatedness among cells is important in promoting the cooperation that underlies multicellular development.ooperation is a hallmark of major transitions in biological complexity: from molecules to genes, from genes to chromosomes, from primitive cells to complex cells, from cells to multicellular organisms, and from multicellular organisms to societies (1-3). Cooperative groups are vulnerable, however, to exploitation by cheaters, individuals that have access to group benefits without contributing their fair share (1-3). Among cells and individuals, high relatedness is thought to aid in selection against cheaters (4-6). High relatedness means that cheaters and cooperators will tend to be in different groups, which both limits opportunities for cheaters to exploit cooperators and exposes any group-level defects of cheaters to selection. Curiously, although such control is central to selfish-gene theory, tests at the genetic level have been limited by the kinds of information available. In large organisms, relatedness is often estimated, but cheater genes are unknown. In microorganisms, cheater genes can be found (7-13), but little is known about relatedness in natural social groups.The life cycle of social amoebae presents a challenge to the importance of relatedness in promoting selection against cheaters and an opportunity to test it. When the normally solitary amoebae are starved of their bacterial food source, they gather into a multicellular aggregate that forms a fruiting body. Here, Ϸ25% of cells altruistically die, forming a stalk that holds up the remaining cells, differentiated as spores, for dispersal (14-17). Thus, unlike more familiar organisms that develop from one cell, development begins by aggregation of many dispersed cells. Different clones can mix and cheat each other (18,19), for example by avoiding contributing to the sterile stalk (7). Models (20)(21)(22), experiments (7,23,24), and a natural observation (24), suggest that cooperative fruiting body formation can be threatened by the spread of mutant cheat...

Evolution of cooperation and control of cheating in a social microbe

“…This is because the benefits of the sacrifice that stalk cells make will mostly go to relatives, and thus could be favored under kin selection. The importance of high relatedness can be seen in an experiment that used the knockout cheater fbxA (49). In this study, we showed that at low relatedness, the fbxA cheater knockout wins within groups at all mixture frequencies.…”

“…This approach gave much higher relatednesses, between 0.86 and 0.98 depending on the sample and technique (49). Thus, relatedness is clearly high enough for kin selection under reasonable values of costs and benefits, and chimerism is common enough for social competition to be favored evolutionarily.…”

Structured growth and genetic drift raise relatedness in the social amoeba Dictyostelium discoideum

“…However, the effect structured growth has on relatedness has not been quantitatively assessed for any social microbe, and so to address this issue, we use the social amoeba Dictyostelium discoideum, now a model organism for social evolution studies [17][18][19]. When food is scarce, starving Dictyostelium cells aggregate to form a fruiting body where around one-fifth die to form a stalk, lifting the remaining cells aloft as viable spores [20].…”

The cell adhesion molecule DdCAD-1 regulates morphogenesis through differential spatiotemporal expression inDictyostelium discoideum

“…In addition, aggregative development exposes D. discoideum to chimerism, which includes cheating, whereby individuals have access to group benefits without contributing their fair share. This phenomenon raises the issues of how social cooperation persists in nature and what factors would permit individuals with a compromised phenotype to survive (Foster et al, 2004;Nowak, 2006;Gilbert et al, 2007). Among the many potential factors, cells tend to cooperate with genetically similar individuals and the cell adhesion genes csaA and tgrC1 have been found to confer survival advantages to D. discoideum cells that carry the same or highly related genes (Queller et al, 2003;Benabentos et al, 2009).…”