Long-term evolution of transposable elements

Abstract

Transposable elements are often considered parasitic DNA sequences, able to invade the genome of their host thanks to their self-replicating ability. This colonization process has been extensively studied, both theoretically and experimentally, but their long-term coevolution with the genomes is still poorly understood. In this work, we aim to challenge previous population genetics models by considering features of transposable elements as quantitative, rather than discrete, variables. We also describe more realistic transposable element dynamics by accounting for the variability of the insertion effect, from deleterious to adaptive, as well as mutations leading to a loss of transposition activity and to nonautonomous copies. Individual-based simulations of the behavior of a transposable-element family over several thousand generations show different ways in which active or inactive copies can be maintained for a very long time. Results reveal an unexpected impact of genetic drift on the "junk DNA" content of the genome and strongly question the likelihood of the sustainable long-term stable transposition-selection equilibrium on which numerous previous works were based.

Fig. 1.

Scheme of the transposition model. Each copy i is defined by its specific activity 0 ≤ a_i ≤ 1 (representing its capacity to produce a functional transposition machinery), transposition rate u_i, and deletion rate v_i. The activity can change with mutations, occuring with a rate m. Small circles and rectangles represent the transposition machinery and the copies inserted in the genome respectively (black, full activity; gray, partial activity; white, no activity).

Fig. 2.

Description of the characteristic dynamics identified. (A) Equilibrium (obtained with the parameter set m = 10⁻⁵, σ_a = 0.1, p_s>0 = 0.01%). (B) Cycles (m = 10⁻³, σ_a = 1, p_s>0 = 0.01%). (C) Domestication (m = 10⁻³, σ_a = 1; p_s>0 = 0.5%). (D) Loss (m = 10⁻³, σ_a = 1, p_s>0 = 0.1%). The x axis represents the time in generations. First column, distribution of the copy number among the individuals of the population; second column, distribution of the fitnesses among the individuals of the population; third column, distribution of the activity among all of the elements present in the population; and fourth column, distribution of the selective impact among all elements. The gray scale corresponds to the distribution of the parameter of each generation (dark gray for high frequencies).

Fig. 3.

Influence of population size on TE evolution. The three histograms represent the percentage of each situation (active transposition, domestication, and loss) after a given number of generations (A, 5,000 generations; B, 10,000 generations; C, 20,000 generations) over 40 repetitions for each parameter set. Other parameters: m = 10⁻³, σ_a = 1, p_s>0 = 0.1%.

Fig. 4.

Summary of the expected dynamics of a TE family in the genome of a species.