Dynamic Evolution of Euchromatic Satellites on the X Chromosome in Drosophila melanogaster and the simulans Clade

Abstract

Satellite DNAs (satDNAs) are among the most dynamically evolving components of eukaryotic genomes and play important roles in genome regulation, genome evolution, and speciation. Despite their abundance and functional impact, we know little about the evolutionary dynamics and molecular mechanisms that shape satDNA distributions in genomes. Here, we use high-quality genome assemblies to study the evolutionary dynamics of two complex satDNAs, Rsp-like and 1.688 g/cm3, in Drosophila melanogaster and its three nearest relatives in the simulans clade. We show that large blocks of these repeats are highly dynamic in the heterochromatin, where their genomic location varies across species. We discovered that small blocks of satDNA that are abundant in X chromosome euchromatin are similarly dynamic, with repeats changing in abundance, location, and composition among species. We detail the proliferation of a rare satellite (Rsp-like) across the X chromosome in D. simulans and D. mauritiana. Rsp-like spread by inserting into existing clusters of the older, more abundant 1.688 satellite, in events likely facilitated by microhomology-mediated repair pathways. We show that Rsp-like is abundant on extrachromosomal circular DNA in D. simulans, which may have contributed to its dynamic evolution. Intralocus satDNA expansions via unequal exchange and the movement of higher order repeats also contribute to the fluidity of the repeat landscape. We find evidence that euchromatic satDNA repeats experience cycles of proliferation and diversification somewhat analogous to bursts of transposable element proliferation. Our study lays a foundation for mechanistic studies of satDNA proliferation and the functional and evolutionary consequences of satDNA movement.

Heterochromatin-dependent transcription of satellite DNAs in the Drosophila melanogaster female germline

“…Lastly, rearrangements in satDNA regions may contribute to mitotic defects, as heterochromatic satDNAs play important roles in chromosome segregation (e.g. (Dernburg, et al 1996;Bouzinba-Segard, et al 2006;Rosic, et al 2014) Drosophila complex satDNAs that we study here are highly dynamic, with their location varying dramatically between species (Larracuente 2014;Jagannathan, et al 2017;Sproul, et al 2020). The rapid turnover of satDNAs can have consequences for speciation-the 1.688 satellite is associated with genetic incompatibilities between species that results in mitotic defects and embryonic lethality (Ferree and Barbash 2009) for reasons that we still do not understand.…”

“…Sequencing data generated in this paper are available in the NCBI Sequence Read Archive under project accession PRJNA647441. All data files and code to recreate analyses and figures, and supplemental data files are deposited in GitHub (https://github.com/LarracuenteLab/Dmelanogaster_satDNA_regulation) (Wei 2020) and at the Dryad Digital Repository (link forthcoming).…”

RepeatProfiler: a pipeline for visualization and comparative analysis of repetitive DNA profiles

“…melanogaster and its close relatives are a group with: a very recent history of divergence (with known dates) (Garrigan et al, 2012), well-established phylogenetic relationships, abundant genomic resources (i.e., sequence data and repeat libraries), and several repeats with a recent history of dynamic activity (Jagannathan, Warsinger-Pepe, Watase, & Yamashita, 2017;Larracuente, 2014;Lohe & Roberts, 1988;Sproul, Khost, et al, 2020). We obtained consensus sequences of 59 abundant transposable elements (TEs) including LTR and non-LTR retrotransposons from a custom Drosophila repeat library (Chakraborty et al, 2020;Sproul, Khost, et al, 2020) and generated profiles from these TEs in a run that included four closely related Drosophila species (D. melanogaster, D. simulans, D. sechellia, and outgroup D. erecta), with 2-4 replicate individuals from each species. The ingroup species diversified in the last 2.5 million years and two species (D. simulans and D. sechellia) are only separated by an estimated ~240k years (Garrigan et al, 2012).…”

“…Despite their critical roles in genome and phenotype evolution and their known rapid turnover between closely related species (e.g. (Lower et al, 2017;Sproul, Khost, et al, 2020;Strachan, Coen, Webb, & Dover, 1982;Tetreault & Ungerer, 2016;Ugarković & Plohl, 2002)), repeat dynamics are seldom considered in evolutionary studies aiming to understand species boundaries and recent genome evolution. One caveat to using repeats in evolutionary studies is that their abundance may fluctuate widely across samples, even below the species level (Bosco, Campbell, Leiva-Neto, & Markow, 2007;McLain, Rai, & Fraser, 1987;Mestrović, Plohl, Mravinac, & Ugarković, 1998;Raskina, Barber, Nevo, & Belyayev, 2008).…”

Satellite DNA-like repeats are dispersed throughout the genome of the Pacific oyster Crassostrea gigas carried by Helentron non-autonomous mobile elements

“…A detailed view of the genomic inventory of satDNAs started to accumulate in different animal and plant species by combining advanced sequencing methods and specialized bioinformatics tools (for example 3,[33][34][35][36][37] ). However, information about content, distribution, and composition of short arrays of TRs located in euchromatic genome compartments and related or resembling satDNAs (therefore named satDNA-like sequences), and about genome environment in which they reside, remains limited and shown on a few species, mostly Drosophila and beetles 34,[38][39][40][41][42] .…”