Abstract
Unicellular protozoa that encyst individually upon starvation evolved at least eight times into organisms that instead form multicellular fruiting bodies with spores. The Dictyostelia are the largest and most complex group of such organisms. They can be subdivided into 4 major groups, with many species in groups 1–3 having additionally retained encystment. To understand fitness differences between spores and cysts, we measured long-term survival of spores and cysts under climate-mimicking conditions, investigated spore and cyst ultrastructure, and related fitness characteristics to species ecology. We found that spores and cysts survived 22 °C equally well, but that spores survived wet and dry frost better than cysts, with group 4 spores being most resilient. Spore walls consist of three layers and those of cysts of maximally two, while spores were also more compacted than cysts, with group 4 spores being the most compacted. Group 4 species were frequently isolated from arctic and alpine zones, which was rarely the case for group 1–3 species. We inferred a fossil-calibrated phylogeny of Dictyostelia, which showed that its two major branches diverged 0.52 billion years ago, following several global glaciations. Our results suggest that Dictyostelium multicellular sporulation was a likely adaptation to a cold climate.
Highlights
The emergence of multicellular life forms was a major event in the history of life
Phylogenetic comparative analysis showed that the last common ancestor (LCA) of Dictyostelia erected small fruiting structures directly from aggregates, while retaining encystation as an alternative survival strategy
To gain insight into structural differences between spores and cysts that could be related to fitness, we investigated spore and cyst ultrastructure by electron microscopy
Summary
The emergence of multicellular life forms was a major event in the history of life. The three most familiar transitions to multicellularity yielded the animals, plants and fungi. Phylogenetic comparative analysis showed that the last common ancestor (LCA) of Dictyostelia erected small fruiting structures directly from aggregates, while retaining encystation as an alternative survival strategy It formed a cellular stalk by transdifferentiation of prespore cells at the fruiting body tip (Fig. 1). Because it comes at a cost to the number of propagating cells, there must be a distinct advantage to sporulating in fruiting bodies as opposed to encysting individually Both spores and cysts have cellulosic walls, but differ in shape. Sporulation in multicellular fruiting structures is commonly thought to aid wide-spread dispersal of organisms, as is the case for fungi with their hydrophobic spores This is less clear for the Dictyostelia, whose hydrophilic spores are not carried by wind. Our combined results suggest that Dictyostelid multicellular sporulation may have been triggered by global cooling during the neoproterozoic “snowball earth” episodes
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