Genomic Signatures of Cooperation and Conflict in the Social Amoeba

Abstract

Summary Cooperative systems are susceptible to invasion by selfish individuals that profit from receiving the social benefits but fail to contribute. These so-called “cheaters” can have a fitness advantage in the laboratory, but it is unclear whether cheating provides an important selective advantage in nature. We used a population genomic approach to examine the history of genes involved in cheating behaviors in the social amoeba Dictyostelium discoideum, testing whether these genes experience rapid evolutionary change as a result of conflict over spore-stalk fate. Candidate genes and surrounding regions showed elevated polymorphism, unusual patterns of linkage disequilibrium, and lower levels of population differentiation, but they did not show greater between-species divergence. The signatures were most consistent with frequency-dependent selection acting to maintain multiple alleles, suggesting that conflict may lead to stalemate rather than an escalating arms race. Our results reveal the evolutionary dynamics of cooperation and cheating and underscore how sequence-based approaches can be used to elucidate the history of conflicts that are difficult to observe directly.

Population genetics of sexual conflict in the genomic era

“…Recently, population genomic approaches have proved useful in scanning for putative signatures of sexual conflict based on DNA sequence diversity parameters 38 , the idea being that balancing selection from sexual conflict will lead to distinct signatures in molecular sequence data. These approaches are based on sequence data alone and, unlike the case studies described above, do not require information about phenotypes or fitness.…”

“…Preliminary 29 and published studies 25,38,40,41 of sexual conflict have measured nucleotide diversity with Tajima's D (Box 2), which estimates the proportion of nucleotide sites in a given sequence that are polymorphic within a population. This approach is based on the assumption that balancing selection from sexual conflict will lead to the maintenance of multiple alleles, which will in turn cause higher than expected levels of sequence diversity compared to regions not under balancing selection.…”

“…For this reason, it is most useful to compare the distribution of Tajima's D for different sets of genes to determine whether certain regions or functionalities are more often associated with balancing selection than a comparison group of genes 26,38,40 .…”

Evolution on the bright side of life: microorganisms and the evolution of mutualism

“…Achieving this will require more theoretical work focused on coevolution in mutualism, along with rigorous experiments that test those theories. Some of this can be achieved by using genomics to test for molecular dynamics consistent with coevolution in natural populations of mutualists . In microorganisms, time‐shift experiments can be used to test whether and how coevolution is occurring at the phenotypic level .…”

Stable eusociality via maternal manipulation when resistance is costless

“…By this I mean a trait (e.g., morphological, molecular, or behavioral) that ancestrally served as an adaptation for manipulation or resistance but lost this function. For example, conflict relics predict the putative conflicting genes to have a high within species genetic diversity (reflecting conflict) that is shared between recently diverged species (reflecting that conflict is ancestral but not current) (see Ostrowski et al, 2015). Because conflict relics are not expected if eusociality originates via offspring control, conflict relics also allow to disentangle manipulation and offspring control as a source of eusociality, even with costless resistance.…”