Abstract
The evolutionary transition towards multicellular life often involves growth in groups of undifferentiated cells followed by differentiation into soma and germ-like cells. Theory predicts that germ soma differentiation is facilitated by a convex trade-off between survival and reproduction. However, this has never been tested and these transitions remain poorly understood at the ecological and genetic level. Here, we study the evolution of cell groups in ten isogenic lines of the unicellular green algae Chlamydomonas reinhardtii with prolonged exposure to a rotifer predator. We confirm that growth in cell groups is heritable and characterized by a convex trade-off curve between reproduction and survival. Identical mutations evolve in all cell group isolates; these are linked to survival and reducing associated cell costs. Overall, we show that just 500 generations of predator selection were sufficient to lead to a convex trade-off and incorporate evolved changes into the prey genome.
Highlights
The evolutionary transition towards multicellular life often involves growth in groups of undifferentiated cells followed by differentiation into soma and germ-like cells
We found significantly more cell groups, where cells adhered to each other after cell division (Fig. S1), among the isolates from the predation lines compared to isolates from non-predation lines (predation 49 out of 97 algal clones tested, no predation 15 out of 112 tested morphotypes (Chi-square: χ2 = 26.07, p = 3.29*10−7; Fig. 1b))
Growth in groups increased survival (i.e., rotifer growth rate was significantly reduced for cell groups; linear mixed effect model (LME) with strain as random effect: F1,202 = 6.40, p = 0.012; Fig. 1c and Fig. S2) but reduced average algal growth rate compared to single cells (LME: F1,202 = 15.82, p = 9.74*10−5; Fig. 1c)
Summary
The evolutionary transition towards multicellular life often involves growth in groups of undifferentiated cells followed by differentiation into soma and germ-like cells. In order to understand the conditions and constraints for the evolution of cell groups and subsequent steps towards multicellularity, with separation into soma cells (cell groups) and germ cells (single cells starting the generation), we need to recognize the evolution of traits and their trade-offs in response to predation. For the evolution of multicellular life, no cell groups are expected to evolve when an increase in reproduction leads initially to only small changes in survival (Fig. 1a, dashed line = concave trade-off curve)[27]. We use whole-genome sequence information for nine pairs of evolved single cells and cell groups to identify shared mutations for the different morphotypes (single cells, cell groups) and develop a graphical model summarizing the genomic changes involved in increasing survival and its associated costs in cell groups of C. reinhardtii
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