Cold climate adaptation is a plausible cause for evolution of multicellular sporulation in Dictyostelia

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 climatemimicking 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.

Evolution of Multicellular Complexity in the Dictyostelid Social Amoebas

“…As mentioned earlier, the fossil-calibrated phylogeny of Amoebozoa sets the split between the two major branches of Dictyostelia at 0.52 billion years ago (Figure 2), following the global glaciations known as "snowball earth" [51,52]. Combined, these observations suggest that Dictyostelium sporulation in multicellular fruiting bodies was an adaptation to cold climate [23].…”

“…By examining the survival curves of cysts and spores from 29 Dictyostelids from all major groups, Lawal and co-authors showed that spores withstand frost better than cysts, with group 4 spores being most frost-resistant. In non-freezing temperatures survival rates between spores and cysts were not significantly different [23]. Comparative ultrastructural studies of spores and cysts revealed that spores are more compacted than cysts and have well-defined three-layered walls, while cyst walls consist of only one or two layers.…”

“…It showed extensive slug migration, set aside a population of non-prespore cells for later support cell differentiation and evolved new cell types, called cup cells and basal disc cells. As highlighted before, its spores became more frost resistant [23]. It is not yet clear whether some of these changes are correlated and have a common genetic basis.…”

“…Previous molecular clock estimations of the divergence time of the two major branches of Dictyostelia varied widely, ranging from 330 million years ago (mya) to 650 mya [46][47][48], reflecting the difference in the datasets and the methods used. The most recent estimate, which is based on relaxed molecular clock dating, using an alignment of 240 proteins with new fossil calibration points of testate amoebas, lies shortly after the start of the Cambrian period at 519 ± 140 mya ( Figure 2) [23]. Albeit with a large margin of error, the estimate suggests that the divergence of Dictyostelids coincides with the famous Cambrian radiation of metazoans (although it is thought that most metazoan phyla already existed well before Cambrian).…”

“…Sociobiological factors, such as the conflicts between genetically non-homogeneous cells constituting the body, could have imposed a constraint for the evolution of complexity in aggregative multicellular organisms [19]. Also, environmental factors such as atmospheric oxygen concentration [20,21], global glaciation [22,23], as well as ecological factors such as the presence of predators/preys [24,25] may all have played important roles in the evolution of multicellularity.…”