A polychromatic ‘greenbeard’ locus determines patterns of cooperation in a social amoeba

Abstract

Cheaters disrupt cooperation by reaping the benefits without paying their fair share of associated costs. Cheater impact can be diminished if cooperators display a tag (‘greenbeard') and recognise and preferentially direct cooperation towards other tag carriers. Despite its popular appeal, the feasibility of such greenbeards has been questioned because the complex patterns of partner-specific cooperative behaviours seen in nature require greenbeards to come in different colours. Here we show that a locus (‘Tgr') of a social amoeba represents a polychromatic greenbeard. Patterns of natural Tgr locus sequence polymorphisms predict partner-specific patterns of cooperation by underlying variation in partner-specific protein–protein binding strength and recognition specificity. Finally, Tgr locus polymorphisms increase fitness because they help avoid potential costs of cooperating with incompatible partners. These results suggest that a polychromatic greenbeard can provide a key mechanism for the evolutionary maintenance of cooperation.

Wild Dictyostelium discoideum social amoebae show plastic responses to the presence of nonrelatives during multicellular development

“…Variation in rates of splitting indicates plasticity in coordination among cells during multicellular development in D . discoideum as was previously found (Gruenheit et al, ; Hirose et al, ). Though our data are suggestive of larger group sizes in chimeras, the difference was not statistically significant and warrant replication with a larger number of wild strains.…”

“…To conclude, our results support that plasticity in cell signaling and group size should be considered alongside variation in fixed factors such as allorecognition type (Gruenheit et al, ; Hirose et al, ), cell or stalk size (Votaw & Ostrowski, ; Wolf et al, ), and bet‐hedging by means of nonaggregating cells (Martínez‐García & Tarnita, ), to fully understand how social conflict affects the evolution of aggregative social groups in D . discoideum and other microbes.…”

“…We did confirm consistent directional expression changes of candidate genes identified from a 5‐way chimeric mix of strains that were engineered to differ only at allorecognition loci (Hirose et al, ) in our data (Figure c), although we found little overlap between these candidate genes and our significantly differentially expressed genes. This latter result suggests to us that while allorecognition loci are important for social interactions during the multicellular cycle (Gruenheit et al, ; Hirose et al, ), they are unlikely to be the exclusive factor that will determine the fate of these interactions. The former result may simply be due to the large insertions that generated the cheater mutants acting at different developmental stages than the one we examined.…”

“…Second, D . discoideum possess highly polymorphic cell adhesion proteins ( tgrB1 and tgrC1 genes) that allow cells to bind better to others cells of their own strain under laboratory conditions, presumably for discrimination against nonrelatives (allorecognition) during fruiting body development (Benabentos et al, ; Gruenheit et al, ; Hirose, Benabentos, Ho, Kuspa, & Shaulsky, ). The presence of such loci indicates that mixed aggregations are not uncommon and perfect segregation via these tgr gene alleles would leave little opportunity for cheating, yet sorting is often incomplete.…”

“…Some strains may produce more numerous but smaller and less viable spores relative to others (Wolf et al, 2015), and some strains may perform bet-hedging against frequent environmental change by investing in more nonaggregating cells that can germinate more quickly when favorable conditions return (Martínez-García & Tarnita, 2016;Tarnita, Washburne, Martinez-Garcia, Sgro, & Levin, 2015). Second, D. discoideum possess highly polymorphic cell adhesion proteins (tgrB1 and tgrC1 genes) that allow cells to bind better to others cells of their own strain under laboratory conditions, presumably for discrimination against nonrelatives (allorecognition) during fruiting body development (Benabentos et al, 2009;Gruenheit et al, 2017;Hirose, Benabentos, Ho, Kuspa, & Shaulsky, 2011). The presence of such loci indicates that mixed aggregations are not uncommon and perfect segregation via these tgr gene alleles would leave little opportunity for cheating, yet sorting is often incomplete.…”