A Model for the Evolution of Extremely Fragmented Macronuclei in Ciliates

While all ciliates possess nuclear dimorphism, several ciliates – like those in the classes Phyllopharyngea, Spirotrichea, and Armophorea – have an extreme macronuclear organization. Their extensively fragmented macronuclei contain upwards of 20,000 chromosomes, each with upwards of thousands of copies. These features have evolved independently on multiple occasions throughout ciliate evolutionary history, and currently no models explain these structures in an evolutionary context. In this paper, we propose that competition between two forces – the limitation and avoidance of chromosomal imbalances as a ciliate undergoes successive asexual divisions, and the costs of replicating massive genomes – is sufficient to explain this particular nuclear structure. We present a simulation of ciliate cell evolution under control of these forces, allowing certain features of the population to change over time. Over a wide range of parameters, we observe the repeated emergence of this unusual genomic organization found in nature. Although much remains to be understood about the evolution of macronuclear genome organization, our results show that the proposed model is a plausible explanation for the emergence of these extremely fragmented, highly polyploid genomes.