Biology subjects

Sproul, J. S.

Publications and source records attributed to Sproul, J. S..

10 recordsLinked to original sources

bioRxiv2026

Satellite DNA dynamics across phylogenetic scales in ground beetles and other insects

Satellite DNAs (satDNAs) are tandemly repeated sequences that can comprise large fractions of eukaryotic genomes. For decades, we have known that satellite DNAs are among the most rapidly evolving genomic components, yet few studies have examined their dynamics across broad evolutionary frameworks--likely in part because their rapid evolution complicates or precludes homology identification. We investigated satDNA dynamics across 50 ground beetle (Carabidae) species, sampling above and below the species level in the subgenus Plataphus of Bembidion. We used RepeatExplorer2 and a novel homology detection pipeline, which we validated using species of Drosophila for which satDNAs are well-documented, to study satDNA dynamics in a comparative framework. We show that satDNAs comprise large genomic fractions (mean = 25.7%, range = 3.2%-53%), with individual satDNA motifs accounting for >30% of total DNA within some species. We quantify major satDNA turnover among closely related species which drives extensive repatterning of repeat content over short evolutionary scales. To place our findings in a broader context, we also surveyed satDNA diversity across the beetle suborder (Adephaga), the beetle order (Coleoptera), and the next six largest insect orders (Lepidoptera, Diptera, Hymenoptera, Hemiptera, Orthoptera, Trichoptera), representing 400 additional species. While satDNA abundance was significantly elevated in the focal subgenus (Plataphus), high genomic proportions were also found in species across Adephaga, Coleoptera, Hymenoptera, and Diptera. Conversely, satDNA proportions were notably reduced in Lepidoptera and Trichoptera. Our investigation of satDNA dynamics at narrow and broad taxonomic scales provides a quantitative illustration of satDNA turnover across a well-sampled clade. It also identifies new high-potential systems for gaining mechanistic insights into the drivers and impacts of satDNA evolution, and raises questions regarding potential links between satDNA turnover, speciation, and core strategies of chromosome and genome architecture in diverse clades.

evolutionary biology↗

bioRxiv2022

Centromere-associated retroelement evolution in Drosophila melanogaster reveals an underlying conflict

Centromeres are chromosomal regions essential for coordinating chromosome segregation during cell division. While centromeres are defined by the presence of a centromere-specific histone H3 variant rather than a particular DNA sequence, they are typically embedded in repeat-dense chromosomal genome regions. In many species, centromeres are associated with transposable elements, but it is unclear if these elements are selfish or if they play a role in centromere specification or function. Here we use Drosophila melanogaster as a model to understand the evolution of centromere-associated transposable elements. G2/Jockey-3 is a non-LTR retroelement in the Jockey clade and the only sequence shared by all centromeres. We study the evolution of G2/Jockey-3 using short and long read population genomic data to infer insertion polymorphisms across the genome. We combine estimates of the age, frequency, and location of insertions to infer the evolutionary processes shaping G2/Jockey-3 and its association with the centromeres. We find that G2/Jockey-3 is an active retroelement targeted by the piRNA pathway that is enriched in centromeres at least in part due to an insertion bias. We do not detect signatures of positive selection on any G2/Jockey-3 insertions that would suggest than individual copies are favored by natural selection. Instead, we infer that most insertions are neutral or weakly deleterious both inside and outside of the centromeres. Therefore, G2/Jockey-3 evolution is consistent with it being a selfish genetic element that targets centromeres. We propose that targeting centromeres helps active retroelements escape host defenses, as the unique centromeric chromatin may prevent targeting by the host silencing machinery. At the same time, centromeric TEs insertions may be tolerated or even beneficial if they also contribute to the transcriptional and chromatin environment. Thus, we suspect centromere-associated retroelements like G2/Jockey-3 reflect a balance between conflict and cooperation at the centromeres.

genomics↗

bioRxiv2022

Repetitive elements in the era of biodiversity genomics: insights from 600+ insect genomes

Repetitive elements (REs) are integral to the composition, structure, and function of eukaryotic genomes, yet remain understudied in most taxonomic groups. We investigated REs across 601 insect species and report wide variation in REs dynamics across groups. Analysis of associations between REs and protein-coding genes revealed dynamic evolution at the interface between REs and coding regions across insects, including notably elevated RE-gene associations in lineages with abundant long interspersed nuclear elements (LINEs). We leveraged this large, empirical data set to quantify impacts of long-read technology on RE detection and investigate fundamental challenges to RE annotation in diverse groups. In long-read assemblies we detected [~]36% more REs than short-read assemblies, with long terminal repeats (LTRs) showing 162% increased detection, while DNA transposons and LINEs showed less respective technology-related bias. In most insect lineages, 25-85% of repetitive sequences were "unclassified" following automated annotation, compared to only [~]13% in Drosophila species. Although the diversity of available insect genomes has rapidly expanded, we show the rate of community contributions to RE databases has not kept pace, preventing efficient annotation and high-resolution study of REs in most groups. We highlight the tremendous opportunity and need for the biodiversity genomics field to embrace REs and suggest collective steps for making progress towards this goal.

genomics↗

bioRxiv2021

Pathways to polar adaptation in fishes revealed by long-read sequencing

Long-read sequencing is driving a new reality for genome science where highly contiguous assemblies can be produced efficiently with modest resources. Genome assemblies from long-read sequences are particularly exciting for understanding the evolution of complex genomic regions that are often difficult to assemble. In this study, we leveraged long-read sequencing data to generate a high-quality genome assembly for an Antarctic eelpout, Opthalmolycus amberensis, the first for the globally distributed family Zoarcidae. We used this assembly to understand how O. amberensis has adapted to the harsh Southern Ocean and compared it to another group of Antarctic fishes: the notothenioids. We showed that selection has largely acted on different targets in eelpouts relative to notothenioids. However, we did find some overlap; in both groups, genes involved in membrane structure, thermal tolerance, and vision have evidence of selection. We found evidence for historical shifts of transposable element activity in O. amberensis and other polar fishes, perhaps reflecting a response to environmental change. We were specifically interested in the evolution of two complex genomic loci known to underlie key adaptations to polar seas: hemoglobin and antifreeze proteins (AFPs). We observed unique evolution of the hemoglobin MN cluster in eelpouts and related fishes in the suborder Zoarcoidei relative to other Perciformes. For AFPs, we identified the first species in the suborder with no evidence of afpIII sequences (Cebidichthys violaceus) in the genomic region where they are found in all other Zoarcoidei, potentially reflecting a lineage-specific loss of this cluster. Beyond polar fishes, our results highlight the power of long-read sequencing to understand genome evolution.

genomics↗

bioRxiv2021

Genome size evolution in the diverse insect order Trichoptera

BackgroundGenome size is implicated in form, function, and ecological success of a species. Two principally different mechanisms are proposed as major drivers of eukaryotic genome evolution and diversity: Polyploidy (i.e., whole genome duplication: WGD) or smaller duplication events and bursts in the activity of repetitive elements (RE). Here, we generated de novo genome assemblies of 17 caddisflies covering all major lineages of Trichoptera. Using these and previously sequenced genomes, we use caddisflies as a model for understanding genome size evolution in diverse insect lineages. ResultsWe detect a ~14-fold variation in genome size across the order Trichoptera. We find strong evidence that repetitive element (RE) expansions, particularly those of transposable elements (TEs), are important drivers of large caddisfly genome sizes. Using an innovative method to examine TEs associated with universal single copy orthologs (i.e., BUSCO genes), we find that TE expansions have a major impact on protein-coding gene regions, with TE-gene associations showing a linear relationship with increasing genome size. Intriguingly, we find that expanded genomes preferentially evolved in caddisfly clades with a higher ecological diversity (i.e., various feeding modes, diversification in variable, less stable environments). ConclusionOur findings provide a platform to test hypotheses about the potential evolutionary roles of TE activity and TE-gene associations, particularly in groups with high species, ecological, and functional diversities.

evolutionary biology↗

bioRxiv2021

Long-reads are revolutionizing 20 years of insect genome sequencing

The first insect genome (Drosophila melanogaster) was published two decades ago. Today, nuclear genome assemblies are available for a staggering 601 insect species representing 20 orders. In this study, we analyzed the most-contiguous assembly for each species and provide a "state of the field" perspective, emphasizing taxonomic representation, assembly quality, gene completeness, and sequencing technologies. Relative to species richness, genomic efforts have been biased towards four orders (Diptera, Hymenoptera, Collembola, and Phasmatodea), Coleoptera are underrepresented, and 11 orders still lack a publicly available genome assembly. The average insect genome assembly is 439.2 megabases in length with 87.5% of single-copy benchmarking genes intact. Most notable has been the impact of long-read sequencing; assemblies that incorporate long-reads are ~48x more contiguous than those that do not. We offer four recommendations as we collectively continue building insect genome resources: (1) seek better integration between independent research groups and consortia, (2) balance future sampling between filling taxonomic gaps and generating data for targeted questions, (3) take advantage of long read sequencing technologies, and (4) expand and improve gene annotations. Significance statementSince the first insect genome was sequenced ~20 years ago, sequencing technologies and the availability of insect genome assemblies have both advanced dramatically. In this study, we curated, analyzed, and summarized the field of insect genomics in terms of taxonomic representation, assembly quality, gene completeness, and sequencing technology. We show that 601 insect species have genome assemblies available, with some groups heavily overrepresented (e.g., Diptera) relative to others (e.g., Coleoptera). The major takeaway of our study is that genome assemblies produced with long reads are ~48x more contiguous than short read assemblies.

genomics↗

bioRxiv2020

Draft Genome Assemblies and Annotations of Agrypnia vestita Walker, and Hesperophylaxmagnus Banks Reveal Substantial Repetitive Element Expansion in Tube Case-making Caddisflies (Insecta: Trichoptera)

Trichoptera (caddisflies) play an essential role in freshwater ecosystems; for instance, larvae process organic material from the water and are food for a variety of predators. Knowledge on the genomic diversity of caddisflies can facilitate comparative and phylogenetic studies thereby allowing scientists to better understand the evolutionary history of caddisflies. While Trichoptera are the most diverse aquatic insect order, they remain poorly represented in terms of genomic resources. To date, all long-read based genomes have been sequenced from individuals in the retreat-making suborder, Annulipalpia, leaving [~]275 Ma of evolution without high-quality genomic resources. Here, we report the first long-read based de novo genome assemblies of two tube case-making Trichoptera from the suborder Integripalpia, Agrypnia vestita Walker and Hesperophylax magnus Banks. We find that these tube case-making caddisflies have genome sizes that are at least three-fold larger than those of currently sequenced annulipalpian genomes and that this pattern is at least partly driven by major expansion of repetitive elements. In H. magnus, long interspersed nuclear elements (LINEs) alone exceed the entire genome size of some annulipalpian counterparts suggesting that caddisflies have high potential as a model for understanding genome size evolution in diverse insect lineages. SignificanceThere is a lack of genomic resources for aquatic insects. So far, only three high-quality genomes have been assembled, all from individuals in the retreat-making suborder Annulipalpia. In this article, we report the first high-quality genomes of two case-making species from the suborder Integripalpia, which are essential for studying genomic diversity across this ecologically diverse insect order. Our research reveals larger genome sizes in the tube case-makers (suborder Integripalpia, infraorder Phryganides), accompanied by a disproportionate increase of repetitive DNA. This suggests that genome size is at least partly driven by a major expansion of repetitive elements. Our work shows that caddisflies have high potential as a model for understanding how genomic diversity might be linked to functional diversification and forms the basis for detailed studies on genome size evolution in caddisflies. Data depositionThis project has been deposited at NCBI under the Bioproject ID: PRJNA668166

genomics↗

bioRxiv2020

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

Study of DNA repeats in model organisms highlights the role of repetitive DNA in many processes that drive genome evolution and phenotypic change. Because repetitive DNA is much more dynamic than single-copy DNA, repetitive sequences can reveal signals of evolutionary history over short time scales that may not be evident in sequences from slower-evolving genomic regions. Many tools for studying repeats are directed toward organisms with existing genomic resources, including genome assemblies and repeat libraries. However, signals in repeat variation may prove especially valuable in disentangling evolutionary histories in diverse non-model groups, for which genomic resources are limited. Here we introduce RepeatProfiler, a tool for generating, visualizing, and comparing repetitive DNA profiles from low-coverage, short-read sequence data. RepeatProfiler automates the generation and visualization of repetitive DNA coverage depth profiles and allows for statistical comparison of profile shape across samples. In addition, RepeatProfiler facilitates comparison of profiles by extracting signal from sequence variants across profiles which can then be analyzed as molecular morphological characters using phylogenetic analysis. We validate RepeatProfiler with data sets from ground beetles (Bembidion), flies (Drosophila), and tomatoes (Solanum). We highlight the potential of repetitive DNA profiles as a high-resolution data source for studies in species delimitation, comparative genomics, and repeat biology.

bioinformatics↗

bioRxiv2020

Repetitive DNA profiles reveal evidence of rapid genome evolution and reflect species boundaries in ground beetles

AO_SCPLOWBSTRACTC_SCPLOWGenome architecture is a complex, multidimensional property of an organism defined by the content and spatial organization of the genomes 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 breve species group of Bembidion, and vary across broader taxonomic sampling in Bembidion subgenus Plataphus. 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 Plataphus. We confirm that CNV profiles represent an aspect of genomic architecture (i.e., the linear distribution of rDNA components across the genome) via fluorescence in-situ 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.

evolutionary biology↗

bioRxiv2019

Dynamic evolution of euchromatic satellites on the X chromosome in Drosophila melanogaster and the simulans clade

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 evolutionary dynamics of two complex satDNAs, Rsp-like and 1.688 gm/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 spreads by inserting into existing clusters of the older, more abundant 1.688 satellite, in events that were 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.

genomics↗