Biology subjects

Ostrowski, E. A.

Publications and source records attributed to Ostrowski, E. A..

5 recordsLinked to original sources

bioRxiv2025

Hypermutable hotspot enables the rapid evolution of self/non-self recognition genes in Dictyostelium

Cells require highly polymorphic receptors to perform accurate self/non-self recognition. In the amoeba Dicytostelium discoideum, polymorphic TgrB1 & TgrC1 proteins are used to bind sister cells and exclude cheaters, but it remains unknown how cells continually generate this extreme genetic diversity. Here, we created a collection of chromosome-length, whole genome sequences from 10 Dictyostelium discoideum isolates and sister species to understand the evolution of the large tgr gene family. Our dataset includes AX2-214, a widely used D. discoideum lab strain, as well as complete genomes for two Chlamydia-like endosymbionts harbored within amoebae. We find that tgrB1 and C1 lie in a hypermutational hotspot, with haplotypes that undergo repeated intralocus recombination, duplications, transpositions, and inversions. These structural dynamics are highly localized adjacent to tgrB and C, resulting in the gain and loss of dozens of genes. The tgrBC genes themselves frequently duplicate and recombine, leading to the rapid generation of unique tgrBC repertoires. In the broader tgr gene family, some genes (e.g. tgrN) are single copy and syntenic across all the genomes, whereas others (e.g. tgrA) prolifically duplicate at similar rates to Dictyostelium transposons. Thus, the tgr genes are among the most rapidly evolving families genome-wide. We propose that the intense diversification within the tgrBC locus can help explain how these genes acquire such extreme levels of polymorphism, with parallels to the MHC immune genes in mammals and other allorecognition systems. This collection of amoeba genomes is also an ideal dataset for comparative genomics and molecular evolution in Amoebozoa. SignificanceThe ability to distinguish self from non-self is an essential part of innate immunity and multicellularity. In the amoeba Dicytostelium discoideum, cells form transient multicellular structures via aggregation. In the process, they exclude distantly-related cheater strains via highly polymorphic cell surface proteins, TgrB1 and TgrC1. We used this system to ask: how do organisms continually generate new variation in recognition factors? After sequencing a collection of Dictyostelium spp. genomes, we found that the tgrB and tgrC genes lie in an extraordinarily variable locus- a region with such high rates of gene birth and death that genomic similarities are quickly lost, even between closely related isolates. Thus, amoeba cell recognition mirrors self/non-self evolutionary dynamics found across the Tree of Life.

evolutionary biology↗

bioRxiv2024

Natural variation in fruiting body morphology in the amoeba Dictyostelium discoideum

Reproductive altruism, where some individuals reproduce and others do not, is considered one of the pinnacles of cooperative societies. However, the optimal level of reproductive altruism is likely to depend on inclusive fitness considerations, including the relatedness of reproducing to non-reproducing individuals, as well as the benefits and costs accruing to each, respectively. In the social amoeba Dictyostelium discoideum, thousands of cells aggregate to form a multicellular fruiting body. During this process, some cells die, forming a rigid stalk that supports the rest of the cells, which become viable spores. The level of stalk investment by the social group can therefore be considered a metric of altruism investment. Importantly, genetically unrelated cells can co-aggregate to produce chimeric fruiting bodies, and selection can favour genotypes that behave selfishly by preferentially forming spores and avoiding forming the stalk. Owing to the extreme differences in fitness consequences of stalk cells versus spores, the level of altruism investment is likely to be under strong selection. Here we examined clonal fruiting body morphology in four natural populations to assess the extent to which stalk investment varies within populations and is maintained to different extents among populations. We found variation in fruiting body size and stalk investment, at both a cm-scale and between geographically isolated populations. These findings indicate the divergent evolution of altruism investment with and among populations and demonstrate widespread potential for cheating.

evolutionary biology↗

bioRxiv2024

Dominance hierarchies are linear but shallow in the social amoeba Dictyostelium discoideum.

Social groups often form dominance hierarchies, and these hierarchies are almost always linear. However, why linear dominance hierarchies emerge is not well understood. In the social amoeba Dictyostelium discoideum, cells form a multicellular fruiting body when starved, which consists of a ball of viable spores held aloft by a stalk of dead cells. In genetically mixed ( chimeric) fruiting bodies, conflicts can arise over the equitable sacrifice of cells to the dead stalk, and some strains predictably dominate others in the spores. Using pairwise mixes of strains that co-occurred in small soil samples, we determined the dominance hierarchies in four natural populations of Dictyostelium. These hierarchies were significantly linear in two of four populations, but also extremely shallow, indicating that co-occurring strains are competitively similar. We used quantitative genetic analyses to assess the causes of social dominance. Each strains solo spore production was a significant predictor of its performance in pairs. However, we detected additional genetic contributions of both the focal and partner strain, indicating additional cryptic traits that mediate social competitiveness. In contrast to earlier studies showing strong fitness differences among strains collected over a larger spatial scale, we show that co-occurring strains are remarkably competitively equivalent, resulting in linear yet shallow hierarchies. Our results underscore the importance of biologically relevant spatial scales in assessing fitness interactions among microbes. They also explain why social trait diversity might be observed despite dominance hierarchies that should eliminate this variation.

evolutionary biology↗

bioRxiv2023

Costs of resistance limit the effectiveness of cooperation enforcement

Cooperative groups are susceptible to invasion by cheaters that reap the benefits but fail to pay the costs. Both theory and experimental work have shown that cheating can select for counter-adaptations to resist cheating. But then why is cheating so common? One key hypothesis is that trade-offs prevent resistors from taking over, but evidence to support the trade-off model is lacking. Here we evolved resistance to different cheaters and tested for trade-offs. Improvements against one cheater frequently entailed correlated improvements against novel cheaters. However, direct responses to selection were typically stronger than correlated responses to selection, resulting in a pattern of local adaptation of resistance. Control populations, evolved in the absence of a cheater, showed improvements in spore germination, whereas cheater-evolved populations did not, suggesting that the evolution of resistance retards or prevents other fitness improvements. Taken together, our findings suggest that, although cheater resistance can evolve rapidly, it may also involve subtle trade-offs that can help to explain the maintenance of polymorphism in cheating and resistance in nature.

evolutionary biology↗

bioRxiv2022

From individual behaviors to collective outcomes: fruiting body formation in Dictyostelium as a group-level phenotype

Collective phenotypes, which arise from the interactions among individuals, can be important for the evolution of higher levels of biological organization. However, how a groups composition determines its collective phenotype remains poorly understood. When starved, cells of the social amoeba Dictyostelium discoideum cooperate to build a multicellular fruiting body, and the morphology of the fruiting body is likely advantageous to the surviving spores. We assessed how the number of strains, as well as their genetic and geographic relationships to one another, impact the groups morphology and productivity. We find that some strains consistently enhance or detract from the productivity of their groups, regardless of the identity of the other group members. We also detect extensive pairwise and higher-order genotype interactions, which collectively have a large influence on the group phenotype. Whereas previous work in Dictyostelium has focused almost exclusively on whether spore production is equitable when strains cooperate to form multicellular fruiting bodies, our results suggest a previously unrecognized impact of chimeric co-development on the group phenotype. Our results demonstrate how interactions among members of a group influence collective phenotypes and how group phenotypes might in turn impact selection on the individual.

evolutionary biology↗