The emergence of predators in early life: there was no Garden of Eden

Abstract

Background: Eukaryote cells are suggested to arise somewhere between 0.85~2.7 billion years ago. However, in the present world of unicellular organisms, cells that derive their food and metabolic energy from larger cells engulfing smaller cells (phagocytosis) are almost exclusively eukaryotic. Combining these propositions, that eukaryotes were the first phagocytotic predators and that they arose only 0.85~2.7 billion years ago, leads to an unexpected prediction of a long period (approximately 1-3 billion years) with no phagocytotes -- a veritable Garden of Eden.

Methodology: We test whether such a long period is reasonable by simulating a population of very simple unicellular organisms -- given only basic physical, biological and ecological principles. Under a wide range of initial conditions, cellular specialization occurs early in evolution; we find a range of cell types from small specialized primary producers to larger opportunistic or specialized predators.

Conclusions: Both strategies, specialized smaller cells and phagocytotic larger cells are apparently fundamental biological strategies that are expected to arise early in cellular evolution. Such early predators could have been 'prokaryotes', but if the earliest cells on the eukaryote lineage were predators then this explains most of their characteristic features.

Figure 1. A stable size distribution is reached from different starting points.

The vertical-axis shows unicell diameter, the x-axis is time expressed in simulation turns. The intensity of the color, ranging from dark to light red on a logarithmic scale, shows the frequencies of unicells in each size class. Although the beginning situations (1a–1d) are very different, all 4 simulations converge to similar population dynamics. In 1a and 1b all cells start at the same size but are larger (1a) or smaller (1b) than the final average size. In 1c and 1d the sizes of the initial unicells are selected from either a uniform (1c) or bimodal (1d) distribution. Additional information on conditions and parameter values are described in Supplementary Information.

Figure 2. Proportion of energy derived from predation.

The dashed red line shows the relative proportion of unicells in each size class; the large majority of unicells are in the 10–20 range. Black dots are the proportion of energy derived from predation for the ∼4% of individual unicells that have obtained some food from predation. (Not shown separately are the vast majority of unicells, ∼96%, that have derived all their energy from primary production.) The green solid line is the fraction of unicells in each size class that have derived the majority of their energy from predation. Only the rare cells larger than about 24 units obtain most of their energy from predation. Parameters and conditions are described in Supplementary Information, table 2.

Figure 3. In each turn of the simulation all unicells are treated in a fixed order.

If the unicell starves or dies due to the chance of random death it is removed from the simulation (though this could be modeled by saprophytes). If its energy store is sufficient then the unicell divides, creating two new unicells. These child unicells are usually half the size of their parent but there is a small chance of uneven division. New unicells cannot take any action in the first turn they are created and a unicell that divides can take no further action that turn. If a unicell doesn't have sufficient energy to divide it looks for food. First it considers what the best source of food is within its physical radius, if there is no suitable source then it will move towards the best source in its sensory radius.