Abstract
A common feature of eukaryotic centromeres is the presence of large tracts of tandemly arranged repeats, known as satellite DNA. However, these centromeric repeats appear to experience rapid evolution under forces such as molecular drive and centromere drive, seemingly without consequence to the integrity of the centromere. Moreover, blocks of heterochromatin within the karyotype, including the centromere, are hotspots for chromosome rearrangements that may drive speciation events by contributing to reproductive isolation. However, the relationship between the evolution of heterochromatic sequences and the karyotypic dynamics of these regions remains largely unknown. Here, we show that a single conserved satellite DNA sequence in the order Rodentia of the genus Peromyscus localizes to recurrent sites of chromosome rearrangements and heterochromatic amplifications. Peromyscine species display several unique features of chromosome evolution compared to other Rodentia, including stable maintenance of a strict chromosome number of 48 among all known species in the absence of any detectable interchromosomal rearrangements. Rather, the diverse karyotypes of Peromyscine species are due to intrachromosomal variation in blocks of repeated DNA content. Despite wide variation in the copy number and location of repeat blocks among different species, we find that a single satellite monomer maintains a conserved sequence and homogenized tandem repeat structure, defying predictions of molecular drive. The conservation of this satellite monomer results in common, abundant, and large blocks of chromatin that are homologous among chromosomes within one species and among diverged species. Thus, such a conserved repeat may have facilitated the retention of polymorphic chromosome variants within individuals and intrachromosomal rearrangements between species—both factors that have previously been hypothesized to contribute towards the extremely wide range of ecological adaptations that this genus exhibits.
Highlights
In most eukaryotic genomes, large arrays of tandem repeats are often confined to functionally defined subregions within chromosomes, such as the centromere and telomere
Given our finding that this P. eremicus satellite is conserved in P. leucopus and previous work demonstrating Peromyscus maniculatus satellite repeat (PMsat) is found in divergent species of Rodentia (Cricetus cricetus) (Louzada et al 2015), we set out to test whether the sequence was a primary component of heterochromatin blocks and/or centromeric regions in other Peromyscus species via fluorescence microscopy using the complete monomer
Given the conservation of this satellite sequence across all major clades within the Peromyscus genus, the predominant satellite at Peromyscus centromeres does not follow the predictions of the “library model” of satellite DNA evolution (Salser et al 1976)—a hypothesis that would explain high centromere sequence divergence between closely related but karyotypically distinct species, such as that observed in the Peromyscine species
Summary
Large arrays of tandem repeats are often confined to functionally defined subregions within chromosomes, such as the centromere and telomere. While maintaining a functional centromere is necessary to sustain chromosome stability by mediating proper kinetochore and microtubule attachment, the satellite DNA sequences that underlie this region are surprisingly among the most rapidly evolving portions of the eukaryotic genome (Henikoff et al 2001), largely affected by processes such as molecular drive (Dover 1982) and centromere drive (Henikoff and Malik 2002; Malik and Henikoff 2002). Satellites and other centromeric repeats in the mammalian genome evolve via concerted evolution, a nonindependent process of molecular drive by which a species or population maintains an unusually high intraspecific repeat homogeneity and, concomitantly, a high interspecific heterogeneity (Dover 1982). The centromere is a host to both rapid nucleotide and karyotypic variation
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