Epigenetic inheritance systems contribute to the evolution of a germline

Abstract

Differentiation within multicellular organisms is controlled by epigenetic markers transmitted across cell division. The process of differentiation will modify these epigenetic markers so that information that one cell type possesses can be lost in the transition to another. Many of the systems that encode these markers also exist in unicellular organisms but do not control differentiation. Thus, during the evolution of multicellularity, epigenetic inheritance systems were probably exapted for their current use in differentiation. We show that the simultaneous use of an information carrier for differentiation and transmission across generations can lead to the evolution of cell types that do not directly contribute to the progeny of the organism and ergo a germ-soma distinction. This shows that an intrinsic instability during a transition from unicellularity to multicellularity may contribute to widespread evolution of a germline and its maintenance, a phenomenon also relevant to the evolution of eusociality. The difference in epigenetic information contents between different cell lines in a multicellular organism is also relevant for the full-success cloning of higher animals, as well as for the maintenance of single germlines over evolutionary timescales.This article is part of the themed issue 'The major synthetic evolutionary transitions'.

Keywords: differentiation; graph; hypercycle; soma; specialization.

Figure 1.

A hypothetical methylation pattern illustrates the loss of epigenetic information. Cell types A and B have different methylation patterns. Genetically encoded mechanisms transform A cell types to B and vice versa, during epigenesis. A’ is a new epimutant similar to A in the function that it performs in the multicellular body. The process that transforms A to B will also transform A’ to B. Since B can then not recreate A’, the epimutation is lost in differentiation.

Figure 2.

(a) The original life cycle of the organism. There is an adult stage with a fixed number of cells of two types, A and B. Both cell types can produce spores that maintain their epigenetic identity, and can reproduce/differentiate into a new adult. (b) Differentiation graph of the organism. Nodes represent cells of an epigenetic type, arrows represent the possibility for a cell type in the spore to produce another cell type in the adult through replication or differentiation.

Figure 3.

(a) Modified life cycle of the system with cells of type A, B and A′. (b) Differentiation graph with the epimutation A′. Notice that cells of type A′ produce cells of type A′ and B, but that cells of type B cannot produce cells of type A′.

Figure 4.

Evolution of a germline. At generation 1 epimutation A′ was introduced. A series of mutations caused the reproductive ability of B to decline to almost 0. The A′ is equivalent to a germline at the end of the run, and B soma. N_A = 4, N_B = 1. f = 1, f′ = 1.3, k = 4, L = 0.5 population size is 10³. Graphs show proportion of spores of the different types over time, and the average reproductive ability of B over time. Shown are results of one typical run.

Figure 5.

Differentiation graph for three cell types. Nodes represent cell type, arrows indicate that the cell type pointed to will be present in an adult that originated in a spore of the originating cell type. (a) Original differentiation graph. (b) Differentiation graph with epimutation in which A mutates to A′, and this epimutation is lost in the differentiation to B and C. (c) Differentiation graph in which A is mutated to A′. The epimutation is retained in differentiation to B, which leads to the creation of B′. The epimutation is lost in differentiation of A′ and B′ into C.

Figure 6.

Differentiation graph for the continuous model. Arrows indicate transitions between epigenetic states and labels indicate the rates.

Figure 7.

The effect of A′ in a continuous population. (a) The proportion of A′ in the stabilized population (after repeated growth and bottlenecks) is shown as a function of switch rates between types. Here, A′ has a fitness advantage of s = 1 over A types. The proportion of A′ is greater than 0 for all values tested though it is the highest when switching between phenotypes is infrequent. (b) The log₂ ratio of times it takes populations to reach N when B types do not reproduce versus when they do is shown as a function of switching rates. The white line encloses the area in parameter space in which the population grows faster if B does not reproduce. This regime has low proportion of A′ in (a) and intermediate switch rates between types. Thus, when B cannot reproduce, the population can increase its production of A′ and grow faster.

Figure 8.

Comparison between inheritance of genetic and epigenetic mutations in an organism without germline. On the left, a genetic mutation occurs and is transmitted to all offspring that are produced by the mutated cell. On the right, an epimutation occurs. It is transmitted only to the offspring of the mutated cell and is lost in the differentiation process. In the offspring, however, both mutated and non-mutated cells exist.