Parallelism in evolution of highly repetitive DNAs in sibling species

Abstract

Characterization of heterochromatin in the flour beetle Tribolium audax revealed two highly repetitive DNA families, named TAUD1 and TAUD2, which together constitute almost 60% of the whole genome. Both families originated from a common ancestral ∼110-bp repeating unit. Tandem arrangement of these elements in TAUD1 is typical for satellite DNAs, whereas TAUD2 represents a dispersed family based on 1412-bp complex higher-order repeats composed of inversely oriented ∼110 bp units. Comparison with repetitive DNAs in the sibling species Tribolium madens showed similarities in nucleotide sequence and length of basic repeating units and also revealed structural and organizational parallelism in tandem and dispersed families assembled from these elements. In both Tribolium species, one tandem and one dispersed family build equivalent distribution patterns in the pericentromeric heterochromatin of all chromosomes including supernumeraries. Differences in the nucleotide sequence and in the complexity of higher-order structures between families of the same type suggest a scenario according to which rearranged variants of the corresponding ancestral families were formed and distributed in genomes during or after the speciation event, following the same principles independently in each descendant species. We assume that random effects of sequence dynamics should be constrained by organizational and structural features of repeating units and possible requirements for spatial distribution of particular sequence elements. An interspersed pattern of repetitive families also points to the intensive recombination events in heterochromatin. Synergy between the meiotic bouquet stage and satellite DNA sequence dynamics could make a positive feedback loop that promotes the observed genome-wide distribution. At the same time, considering the abundance of these DNAs in heterochromatin spanning the (peri)centromeric chromosomal segments, we speculate that diverged repetitive sequences might represent the DNA basis of reproductive barrier between the two sibling species. © The Author 2010. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved.