Reduced social function in experimentally evolvedDictyostelium discoideumimplies selection for social conflict in nature

Abstract

Many microbes interact with one another, but the difficulty of directly observing these interactions in nature makes interpreting their adaptive value complicated. The social amoeba Dictyostelium discoideum forms aggregates wherein some cells are sacrificed for the benefit of others. Within chimeric aggregates containing multiple unrelated lineages, cheaters can gain an advantage by undercontributing, but the extent to which wild D. discoideum has adapted to cheat is not fully clear. In this study, we experimentally evolved D. discoideum in an environment where there were no selective pressures to cheat or resist cheating in chimeras. D. discoideum lines grown in this environment evolved reduced competitiveness within chimeric aggregates and reduced ability to migrate during the slug stage. By contrast, we did not observe a reduction in cell number, a trait for which selection was not relaxed. The observed loss of traits that our laboratory conditions had made irrelevant suggests that these traits were adaptations driven and maintained by selective pressures D. discoideum faces in its natural environment. Our results suggest that D. discoideum faces social conflict in nature, and illustrate a general approach that could be applied to searching for social or non-social adaptations in other microbes.

Testing the coordination hypothesis: incompatibilities in the absence of a single-cell bottleneck in an experimentally evolved social amoeba.

“…The relatively short duration of our experimental evolution, and the large population sizes, preclude genetic drift causing changes in tgrB1 and tgrC1 across multiple lines. And there was no selection for changes in the tgr loci because there was no multicellular development during the experimental evolution of these lines (Larsen et al, 2023). As expected in the absence of direct selection, cheating ability declined (Larsen et al, 2023).…”

“…However, an increase in spore production may not necessarily result in improved fitness if it is generated at the cost of stalk formation or by producing smaller spores. Support for this possibility comes from the experiment that generated these lines (Larsen et al, 2023). Because there was no social stage during the evolution, we expected most aspects of social fitness to usually change negatively, and the ability to cheat did decline.…”

“…First, we made pairwise mixes of clonal ancestors with one of their evolved lineages. We used 10 D. discoideum ancestors (QS6, QS9, QS11, QS18, QS69, QS70, QS159, QS161, QS395, QS859) that had been experimentally evolved in triplicate to generate 30 evolved lines in total (Larsen et al, 2023). We made pairwise mixes of the ancestral clones (A) with each of their own derived lines (E1, E2, E3) to generate a total of 30 mixed lines (A+E1, A+E2, A+E3; we call these "lines" for consistency but they are really mixtures without a common history).…”

“…With abundant nutrients, these D. discoideum lines did not form multicellular groups and would therefore have experienced no selection for novel kin recognition variants. These evolved lines of D. discoideum showed average reduced social function in terms of slug movement distance and cheating capability (Larsen et al, 2023). Thus, in the absence of direct selection for these traits, indirect and presumably deleterious genetic changes occurred, via drift or antagonistic pleiotropy with traits under selection.…”

“…When lineages selected from the same ancestor are evolved without the multicellular stage, the descendants are not expected to recognize each other as foreign when mixed. In a recent experimental evolution study (Larsen et al, 2023), we created such lineages of D. discoideum clones. Amoebas were transferred on nutrient plates before the onset of starvation for 30 transfers (more than 200-300 cell divisions).…”