Repetitive DNA profiles Reveal Evidence of Rapid Genome Evolution and Reflect Species Boundaries in Ground Beetles

Abstract

<jats:title>A<jats:sc>bstract</jats:sc></jats:title><jats:p>Genome architecture is a complex, multidimensional property of an organism defined by the content and spatial organization of the genome’s component parts. Comparative study of entire genome architecture in model organisms is shedding light on mechanisms underlying genome regulation, evolution, and diversification; but such studies require costly analytical approaches which make extensive comparative study impractical for most groups. However, lower-cost methods that measure a single architectural component (e.g., distribution of one class of repeats) have potential as a new data source for evolutionary studies insofar as that measure correlates with more complex biological phenomena, and for which it could serve as part of an explanatory framework. We investigated copy number variation (CNV) profiles in ribosomal DNA (rDNA) as a simple measure reflecting the distribution of rDNA subcomponents across the genome. We find that signatures present in rDNA CNV profiles strongly correlate with species boundaries in the <jats:italic>breve</jats:italic> species group of <jats:italic>Bembidion</jats:italic>, and vary across broader taxonomic sampling in <jats:italic>Bembidion</jats:italic> subgenus <jats:italic>Plataphus</jats:italic>. Profiles of several species show evidence of re-patterning of rDNA-like sequences throughout the genome, revealing evidence of rapid genome evolution (including among sister pairs) not evident from analysis of traditional data sources such as multi-gene data sets. Major re-patterning of rDNA-like sequences has occurred frequently within the evolutionary history of <jats:italic>Plataphus</jats:italic>. We confirm that CNV profiles represent an aspect of genomic architecture (i.e., the linear distribution of rDNA components across the genome) via fluorescence <jats:italic>in-situ</jats:italic> hybridization. In at least one species, novel rDNA-like elements are spread throughout all chromosomes. We discuss the potential of copy number profiles of rDNA, or other repeats, as a low-cost tool for incorporating signal of genomic architecture variation in studies of species delimitation and genome evolution.</jats:p>

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

“…We validated the pipeline using previously published short‐read data from ground beetles, tomatoes, and Drosophila , and simulated data from Drosophila . RepeatProfiler automates a general workflow of using RE profiles in evolutionary studies presented in Sproul and Maddison (2018) and Sproul, Barton, et al (2020). Those studies explored reference bias, profile stability across varying read depth, tested whether profiles could be obtained from targeted sequencing workflows (i.e., hybrid capture) and museum specimens, and used fluorescence in situ hybridization to relate information in profiles back to repeat architecture on chromosomes.…”

“…Dynamic variation in repeat abundance may add noise when comparing patterns across samples, which can confound signals that may be present (Martín‐Peciña et al, 2019). Development of approaches that can extract evolutionary signal despite repeat abundance variation can potentially increase the resolution of evolutionary studies among populations and species (Sproul, Barton, et al, 2020).…”

“…Here we present RepeatProfiler as a tool for both exploration and comparative analysis of repetitive DNA element patterns with low‐coverage, short‐read data. The pipeline was motivated by a previous study by Sproul, Barton, et al (2020), which highlighted the potential of RE profiles in species delimitation studies. RepeatProfiler maps reads to reference repeat sequences, generates enhanced read depth/copy number profiles for visualizing patterns, and facilitates statistical comparison of profiles within and among samples.…”

“…Comparing profiles for the same repeat reference between multiple samples can reveal species‐specific differences in sequence composition (e.g., substitutions, indels), relative abundance, truncations, and amplification of partial repeats throughout the genome. This approach to studying REs which is also used by other recent tools (e.g., DeviaTE [Weilguny & Kofler, 2019]) bypasses issues related to multiple mapping and incomplete genome assemblies because all genomic reads are mapped to reference sequences and the resulting profiles capture variation in the repeat sequence, regardless of their genomic distribution (Fernandes et al, 2020; Sproul et al, 2020). Studying profiles of multiple REs in a comparative framework can provide evidence of gene flow boundaries, highlight potential mechanisms underlying repeat evolution, and detect signatures of rapid genome evolution not evident in less dynamic components of the genome (Sproul, Barton, et al, 2020; Sproul & Maddison, 2018).…”

Draft Genome Assemblies and Annotations ofAgrypnia vestitaWalker, andHesperophylax magnusBanks Reveal Substantial Repetitive Element Expansion in Tube Case-making Caddisflies (Insecta: Trichoptera)

“…LINEs (especially L1) play major roles in genome stability, cancer, and aging (De Cecco et al, 2019; Van Meter et al, 2014). In many groups LINEs are hypothesized to play important evolutionary roles, including roles in rapid genome evolution though their own movement (Kordiš et al, 2006; Suh et al, 2015; Warren et al, 2008), and by facilitating expansion of other repeat classes (Grandi and An, 2013; Sproul et al, 2020). It is possible that these elements have been important drivers in the expansion of integripalpian genomes.…”