Publications by authors named "Gennady Churakov"

31 Publications

The multicomparative 2-n-way genome suite.

Genome Res 2020 10 29;30(10):1508-1516. Epub 2020 Jul 29.

Institute of Experimental Pathology, ZMBE, University of Münster, 48149 Münster, Germany.

To effectively analyze the increasing amounts of available genomic data, improved comparative analytical tools that are accessible to and applicable by a broad scientific community are essential. We built the "2-n-way" software suite to provide a fundamental and innovative processing framework for revealing and comparing inserted elements among various genomes. The suite comprises two user-friendly web-based modules. The 2-way module generates pairwise whole-genome alignments of target and query species. The resulting genome coordinates of blocks (matching sequences) and gaps (missing sequences) from multiple 2-ways are then transferred to the n-way module and sorted into projects, in which user-defined coordinates from reference species are projected to the block/gap coordinates of orthologous loci in query species to provide comparative information about presence (blocks) or absence (gaps) patterns of targeted elements over many entire genomes and phylogroups. Thus, the 2-n-way software suite is ideal for performing multidirectional, non-ascertainment-biased screenings to extract all possible presence/absence data of user-relevant elements in orthologous sequences. To highlight its applicability and versatility, we used 2-n-way to expose approximately 100 lost introns in vertebrates, analyzed thousands of potential phylogenetically informative bat and whale retrotransposons, and novel human exons as well as thousands of human polymorphic retrotransposons.
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http://dx.doi.org/10.1101/gr.262261.120DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7605268PMC
October 2020

The Volcano Rabbit in the Phylogenetic Network of Lagomorphs.

Genome Biol Evol 2019 01 1;11(1):11-16. Epub 2019 Jan 1.

Institute of Experimental Pathology (ZMBE), University of Münster, Germany.

The order Lagomorpha unifies pikas (Ochotonidae) and the hares plus rabbits (Leporidae). Phylogenetic reconstructions of the species within Leporidae based on traditional morphological or molecular sequence data provide support for conflicting hypotheses. The retroposon presence/absence patterns analyzed in this study revealed strong support for the broadly accepted splitting of lagomorphs into ochotonids and leporids with Pronolagus as the first divergence in the leporid tree. Furthermore, the retroposon presence/absence patterns nested the rare volcano rabbit, Romerolagus diazi, within an unresolved network of deeper leporid relationships and provide the first homoplasy-free image of incomplete lineage sorting and/or ancestral hybridization/introgression in rapidly radiated Leporidae. At the same time, the strongest retroposon presence/absence signal supports the volcano rabbit as a separate branch between the Pronolagus junction and a unified cluster of the remaining leporids.
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http://dx.doi.org/10.1093/gbe/evy257DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6319600PMC
January 2019

Speciation network in Laurasiatheria: retrophylogenomic signals.

Genome Res 2017 Jun 15;27(6):997-1003. Epub 2017 Mar 15.

Institute of Experimental Pathology, ZMBE, University of Münster, 48149 Münster, Germany.

Rapid species radiation due to adaptive changes or occupation of new ecospaces challenges our understanding of ancestral speciation and the relationships of modern species. At the molecular level, rapid radiation with successive speciations over short time periods-too short to fix polymorphic alleles-is described as incomplete lineage sorting. Incomplete lineage sorting leads to random fixation of genetic markers and hence, random signals of relationships in phylogenetic reconstructions. The situation is further complicated when you consider that the genome is a mosaic of ancestral and modern incompletely sorted sequence blocks that leads to reconstructed affiliations to one or the other relative, depending on the fixation of their shared ancestral polymorphic alleles. The laurasiatherian relationships among Chiroptera, Perissodactyla, Cetartiodactyla, and Carnivora present a prime example for such enigmatic affiliations. We performed whole-genome screenings for phylogenetically diagnostic retrotransposon insertions involving the representatives bat (Chiroptera), horse (Perissodactyla), cow (Cetartiodactyla), and dog (Carnivora), and extracted among 162,000 preselected cases 102 virtually homoplasy-free, phylogenetically informative retroelements to draw a complete picture of the highly complex evolutionary relations within Laurasiatheria. All possible evolutionary scenarios received considerable retrotransposon support, leaving us with a network of affiliations. However, the Cetartiodactyla-Carnivora relationship as well as the basal position of Chiroptera and an ancestral laurasiatherian hybridization process did exhibit some very clear, distinct signals. The significant accordance of retrotransposon presence/absence patterns and flanking nucleotide changes suggest an important influence of mosaic genome structures in the reconstruction of species histories.
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http://dx.doi.org/10.1101/gr.210948.116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5453332PMC
June 2017

The Beaver's Phylogenetic Lineage Illuminated by Retroposon Reads.

Sci Rep 2017 03 3;7:43562. Epub 2017 Mar 3.

Institute of Experimental Pathology (ZMBE), University of Münster, Münster, Germany.

Solving problematic phylogenetic relationships often requires high quality genome data. However, for many organisms such data are still not available. Among rodents, the phylogenetic position of the beaver has always attracted special interest. The arrangement of the beaver's masseter (jaw-closer) muscle once suggested a strong affinity to some sciurid rodents (e.g., squirrels), placing them in the Sciuromorpha suborder. Modern molecular data, however, suggested a closer relationship of beaver to the representatives of the mouse-related clade, but significant data from virtually homoplasy-free markers (for example retroposon insertions) for the exact position of the beaver have not been available. We derived a gross genome assembly from deposited genomic Illumina paired-end reads and extracted thousands of potential phylogenetically informative retroposon markers using the new bioinformatics coordinate extractor fastCOEX, enabling us to evaluate different hypotheses for the phylogenetic position of the beaver. Comparative results provided significant support for a clear relationship between beavers (Castoridae) and kangaroo rat-related species (Geomyoidea) (p < 0.0015, six markers, no conflicting data) within a significantly supported mouse-related clade (including Myodonta, Anomaluromorpha, and Castorimorpha) (p < 0.0015, six markers, no conflicting data).
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http://dx.doi.org/10.1038/srep43562DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5335264PMC
March 2017

Genome sequence of the basal haplorrhine primate Tarsius syrichta reveals unusual insertions.

Nat Commun 2016 10 6;7:12997. Epub 2016 Oct 6.

McDonnell Genome Institute, Washington University School of Medicine, St. Louis, Missouri 63108, USA.

Tarsiers are phylogenetically located between the most basal strepsirrhines and the most derived anthropoid primates. While they share morphological features with both groups, they also possess uncommon primate characteristics, rendering their evolutionary history somewhat obscure. To investigate the molecular basis of such attributes, we present here a new genome assembly of the Philippine tarsier (Tarsius syrichta), and provide extended analyses of the genome and detailed history of transposable element insertion events. We describe the silencing of Alu monomers on the lineage leading to anthropoids, and recognize an unexpected abundance of long terminal repeat-derived and LINE1-mobilized transposed elements (Tarsius interspersed elements; TINEs). For the first time in mammals, we identify a complete mitochondrial genome insertion within the nuclear genome, then reveal tarsier-specific, positive gene selection and posit population size changes over time. The genomic resources and analyses presented here will aid efforts to more fully understand the ancient characteristics of primate genomes.
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http://dx.doi.org/10.1038/ncomms12997DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5059674PMC
October 2016

Genomic analysis reveals hidden biodiversity within colugos, the sister group to primates.

Sci Adv 2016 08 10;2(8):e1600633. Epub 2016 Aug 10.

Department of Veterinary Integrative Biosciences, Interdisciplinary Program in Genetics, Texas A&M University, College Station, TX 77843, USA.

Colugos are among the most poorly studied mammals despite their centrality to resolving supraordinal primate relationships. Two described species of these gliding mammals are the sole living members of the order Dermoptera, distributed throughout Southeast Asia. We generated a draft genome sequence for a Sunda colugo and a Philippine colugo reference alignment, and used these to identify colugo-specific genetic changes that were enriched in sensory and musculoskeletal-related genes that likely underlie their nocturnal and gliding adaptations. Phylogenomic analysis and catalogs of rare genomic changes overwhelmingly support the contested hypothesis that colugos are the sister group to primates (Primatomorpha), to the exclusion of treeshrews. We captured ~140 kb of orthologous sequence data from colugo museum specimens sampled across their range and identified large genetic differences between many geographically isolated populations that may result in a >300% increase in the number of recognized colugo species. Our results identify conservation units to mitigate future losses of this enigmatic mammalian order.
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http://dx.doi.org/10.1126/sciadv.1600633DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4980104PMC
August 2016

Incomplete Lineage Sorting and Hybridization Statistics for Large-Scale Retroposon Insertion Data.

PLoS Comput Biol 2016 Mar 11;12(3):e1004812. Epub 2016 Mar 11.

Institute of Experimental Pathology (ZMBE), University of Münster, Münster, Germany.

Ancient retroposon insertions can be used as virtually homoplasy-free markers to reconstruct the phylogenetic history of species. Inherited, orthologous insertions in related species offer reliable signals of a common origin of the given species. One prerequisite for such a phylogenetically informative insertion is that the inserted element was fixed in the ancestral population before speciation; if not, polymorphically inserted elements may lead to random distributions of presence/absence states during speciation and possibly to apparently conflicting reconstructions of their ancestry. Fortunately, such misleading fixed cases are relatively rare but nevertheless, need to be considered. Here, we present novel, comprehensive statistical models applicable for (1) analyzing any pattern of rare genomic changes, (2) testing and differentiating conflicting phylogenetic reconstructions based on rare genomic changes caused by incomplete lineage sorting or/and ancestral hybridization, and (3) differentiating between search strategies involving genome information from one or several lineages. When the new statistics are applied, in non-conflicting cases a minimum of three elements present in both of two species and absent in a third group are considered significant support (p<0.05) for the branching of the third from the other two, if all three of the given species are screened equally for genome or experimental data. Five elements are necessary for significant support (p<0.05) if a diagnostic locus derived from only one of three species is screened, and no conflicting markers are detected. Most potentially conflicting patterns can be evaluated for their significance and ancestral hybridization can be distinguished from incomplete lineage sorting by considering symmetric or asymmetric distribution of rare genomic changes among possible tree configurations. Additionally, we provide an R-application to make the new KKSC insertion significance test available for the scientific community at http://retrogenomics.uni-muenster.de:3838/KKSC_significance_test/.
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http://dx.doi.org/10.1371/journal.pcbi.1004812DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4788455PMC
March 2016

The genome of the vervet (Chlorocebus aethiops sabaeus).

Genome Res 2015 Dec 16;25(12):1921-33. Epub 2015 Sep 16.

Crucell Holland B.V., 2333 CN Leiden, The Netherlands;

We describe a genome reference of the African green monkey or vervet (Chlorocebus aethiops). This member of the Old World monkey (OWM) superfamily is uniquely valuable for genetic investigations of simian immunodeficiency virus (SIV), for which it is the most abundant natural host species, and of a wide range of health-related phenotypes assessed in Caribbean vervets (C. a. sabaeus), whose numbers have expanded dramatically since Europeans introduced small numbers of their ancestors from West Africa during the colonial era. We use the reference to characterize the genomic relationship between vervets and other primates, the intra-generic phylogeny of vervet subspecies, and genome-wide structural variations of a pedigreed C. a. sabaeus population. Through comparative analyses with human and rhesus macaque, we characterize at high resolution the unique chromosomal fission events that differentiate the vervets and their close relatives from most other catarrhine primates, in whom karyotype is highly conserved. We also provide a summary of transposable elements and contrast these with the rhesus macaque and human. Analysis of sequenced genomes representing each of the main vervet subspecies supports previously hypothesized relationships between these populations, which range across most of sub-Saharan Africa, while uncovering high levels of genetic diversity within each. Sequence-based analyses of major histocompatibility complex (MHC) polymorphisms reveal extremely low diversity in Caribbean C. a. sabaeus vervets, compared to vervets from putatively ancestral West African regions. In the C. a. sabaeus research population, we discover the first structural variations that are, in some cases, predicted to have a deleterious effect; future studies will determine the phenotypic impact of these variations.
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http://dx.doi.org/10.1101/gr.192922.115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4665013PMC
December 2015

Exploring Massive Incomplete Lineage Sorting in Arctoids (Laurasiatheria, Carnivora).

Mol Biol Evol 2015 Dec 3;32(12):3194-204. Epub 2015 Sep 3.

Institute of Experimental Pathology, ZMBE, University of Münster, Münster, Germany

Freed from the competition of large raptors, Paleocene carnivores could expand their newly acquired habitats in search of prey. Such changing conditions might have led to their successful distribution and rapid radiation. Today, molecular evolutionary biologists are faced, however, with the consequences of such accelerated adaptive radiations, because they led to sequential speciation more rapidly than phylogenetic markers could be fixed. The repercussions being that current genealogies based on such markers are incongruent with species trees.Our aim was to explore such conflicting phylogenetic zones of evolution during the early arctoid radiation, especially to distinguish diagnostic from misleading phylogenetic signals, and to examine other carnivore-related speciation events. We applied a combination of high-throughput computational strategies to screen carnivore and related genomes in silico for randomly inserted retroposed elements that we then used to identify inconsistent phylogenetic patterns in the Arctoidea group, which is well known for phylogenetic discordances.Our combined retrophylogenomic and in vitro wet lab approach detected hundreds of carnivore-specific insertions, many of them confirming well-established splits or identifying and solving conflicting species distributions. Our systematic genome-wide screens for Long INterspersed Elements detected homoplasy-free markers with insertion-specific truncation points that we used to distinguish phylogenetically informative markers from conflicting signals. The results were independently confirmed by phylogenetic diagnostic Short INterspersed Elements. As statistical analysis ruled out ancestral hybridization, these doubly verified but still conflicting patterns were statistically determined to be genomic remnants from a time of ancestral incomplete lineage sorting that especially accompanied large parts of Arctoidea evolution.
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http://dx.doi.org/10.1093/molbev/msv188DOI Listing
December 2015

Ancient traces of tailless retropseudogenes in therian genomes.

Genome Biol Evol 2015 Feb 26;7(3):889-900. Epub 2015 Feb 26.

Institute of Experimental Pathology, ZMBE, University of Münster, Germany

Transposable elements, once described by Barbara McClintock as controlling genetic units, not only occupy the largest part of our genome but are also a prominent moving force of genomic plasticity and innovation. They usually replicate and reintegrate into genomes silently, sometimes causing malfunctions or misregulations, but occasionally millions of years later, a few may evolve into new functional units. Retrotransposons make their way into the genome following reverse transcription of RNA molecules and chromosomal insertion. In therian mammals, long interspersed elements 1 (LINE1s) self-propagate but also coretropose many RNAs, including mRNAs and small RNAs that usually exhibit an oligo(A) tail. The revitalization of specific LINE1 elements in the mammalian lineage about 150 Ma parallels the rise of many other nonautonomous mobilized genomic elements. We previously identified and described hundreds of tRNA-derived retropseudogenes missing characteristic oligo(A) tails consequently termed tailless retropseudogenes. Additional analyses now revealed hundreds of thousands of tailless retropseudogenes derived from nearly all types of RNAs. We extracted 2,402 perfect tailless sequences (with discernible flanking target site duplications) originating from tRNAs, spliceosomal RNAs, 5S rRNAs, 7SK RNAs, mRNAs, and others. Interestingly, all are truncated at one or more defined positions that coincide with internal single-stranded regions. 5S ribosomal and U2 spliceosomal RNAs were analyzed in the context of mammalian phylogeny to discern the origin of the therian LINE1 retropositional system that evolved in our 150-Myr-old ancestor.
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http://dx.doi.org/10.1093/gbe/evv040DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5322556PMC
February 2015

Multiple lineages of ancient CR1 retroposons shaped the early genome evolution of amniotes.

Genome Biol Evol 2014 Dec 11;7(1):205-17. Epub 2014 Dec 11.

Institute of Experimental Pathology (ZMBE), University of Münster, Germany.

Chicken repeat 1 (CR1) retroposons are long interspersed elements (LINEs) that are ubiquitous within amniote genomes and constitute the most abundant family of transposed elements in birds, crocodilians, turtles, and snakes. They are also present in mammalian genomes, where they reside as numerous relics of ancient retroposition events. Yet, despite their relevance for understanding amniote genome evolution, the diversity and evolution of CR1 elements has never been studied on an amniote-wide level. We reconstruct the temporal and quantitative activity of CR1 subfamilies via presence/absence analyses across crocodilian phylogeny and comparative analyses of 12 crocodilian genomes, revealing relative genomic stasis of retroposition during genome evolution of extant Crocodylia. Our large-scale phylogenetic analysis of amniote CR1 subfamilies suggests the presence of at least seven ancient CR1 lineages in the amniote ancestor; and amniote-wide analyses of CR1 successions and quantities reveal differential retention (presence of ancient relics or recent activity) of these CR1 lineages across amniote genome evolution. Interestingly, birds and lepidosaurs retained the fewest ancient CR1 lineages among amniotes and also exhibit smaller genome sizes. Our study is the first to analyze CR1 evolution in a genome-wide and amniote-wide context and the data strongly suggest that the ancestral amniote genome contained myriad CR1 elements from multiple ancient lineages, and remnants of these are still detectable in the relatively stable genomes of crocodilians and turtles. Early mammalian genome evolution was thus characterized by a drastic shift from CR1 prevalence to dominance and hyperactivity of L2 LINEs in monotremes and L1 LINEs in therians.
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http://dx.doi.org/10.1093/gbe/evu256DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4316615PMC
December 2014

GPAC-genome presence/absence compiler: a web application to comparatively visualize multiple genome-level changes.

Mol Biol Evol 2015 Jan 25;32(1):275-86. Epub 2014 Sep 25.

Institute of Experimental Pathology, ZMBE, University of Münster, Münster, Germany

Our understanding of genome-wide and comparative sequence information has been broadened considerably by the databases available from the University of California Santa Cruz (UCSC) Genome Bioinformatics Department. In particular, the identification and visualization of genomic sequences, present in some species but absent in others, led to fundamental insights into gene and genome evolution. However, the UCSC tools currently enable one to visualize orthologous genomic loci for a range of species in only a single locus. For large-scale comparative analyses of such presence/absence patterns a multilocus view would be more desirable. Such a tool would enable us to compare thousands of relevant loci simultaneously and to resolve many different questions about, for example, phylogeny, specific aspects of genome and gene evolution, such as the gain or loss of exons and introns, the emergence of novel transposed elements, nonprotein-coding RNAs, and viral genomic particles. Here, we present the first tool to facilitate the parallel analysis of thousands of genomic loci for cross-species presence/absence patterns based on multiway genome alignments. This genome presence/absence compiler uses annotated or other compilations of coordinates of genomic locations and compiles all presence/absence patterns in a flexible, color-coded table linked to the individual UCSC Genome Browser alignments. We provide examples of the versatile information content of such a screening system especially for 7SL-derived transposed elements, nuclear mitochondrial DNA, DNA transposons, and miRNAs in primates (http://www.bioinformatics.uni-muenster.de/tools/gpac, last accessed October 1, 2014).
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http://dx.doi.org/10.1093/molbev/msu276DOI Listing
January 2015

Retrophylogenomics place tarsiers on the evolutionary branch of anthropoids.

Sci Rep 2013 ;3:1756

Institute of Experimental Pathology, University of Münster, 48149 Münster, Germany.

One of the most disputed issues in primate evolution and thus of our own primate roots, is the phylogenetic position of the Southeast Asian tarsier. While much molecular data indicate a basal place in the primate tree shared with strepsirrhines (prosimian monophyly hypothesis), data also exist supporting either an earlier divergence in primates (tarsier-first hypothesis) or a close relationship with anthropoid primates (Haplorrhini hypothesis). The use of retroposon insertions embedded in the Tarsius genome afforded us the unique opportunity to directly test all three hypotheses via three pairwise genome alignments. From millions of retroposons, we found 104 perfect orthologous insertions in both tarsiers and anthropoids to the exclusion of strepsirrhines, providing conflict-free evidence for the Haplorrhini hypothesis, and none supporting either of the other two positions. Thus, tarsiers are clearly the sister group to anthropoids in the clade Haplorrhini.
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http://dx.doi.org/10.1038/srep01756DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3639448PMC
February 2014

Ancestry of the Australian termitivorous numbat.

Mol Biol Evol 2013 May 21;30(5):1041-5. Epub 2013 Feb 21.

Institute of Experimental Pathology (ZMBE), University of Münster, Münster, Germany.

The Australian numbat, Myrmecobius fasciatus, is the only marsupial that feeds almost exclusively on termites and that has a life following the diurnally restricted and dynamic geographical distribution of termites. The millions of years of this adaptation led to unique morphological and anatomical features, especially basicranial and dental characteristics, that make it difficult to identify a clear phylogenetic affiliation to other marsupials. From DNA sequence analyses, the family Myrmecobiidae is placed within the dasyuromorph marsupials, but the exact position varies from study to study, and support values are mostly rather modest. Here, we report the recovery and analysis of approximately 110,000 quasifossilized traces of mobile element insertions into the genome of a dasyurid marsupial (Tasmanian devil), 25 of which are phylogenetically informative for early dasyuromorphial evolution. Fourteen of these ancient retroposon insertions are shared by the 16 Dasyuromorphia species analyzed, including the numbat, but are absent in the outgroups. An additional 11 other insertions are present in all Dasyuridae but are absent in the numbat. These findings place numbats as the sister group to all living Dasyuridae and show that the investigated Dasyuromorphia, including the Myrmecobiidae, constitutes a monophyletic group that is separated from Peramelemorphia, Notoryctemorphia, and other marsupials.
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http://dx.doi.org/10.1093/molbev/mst032DOI Listing
May 2013

Retroposon insertion patterns of neoavian birds: strong evidence for an extensive incomplete lineage sorting era.

Mol Biol Evol 2012 Jun 3;29(6):1497-501. Epub 2012 Jan 3.

More than 150 Ma, the avian lineage separated from that of other dinosaurs and later diversified into the more than 10,000 species extant today. The early neoavian bird radiations most likely occurred in the late Cretaceous (more than 65 Ma) but left behind few if any molecular signals of their archaic evolutionary past. Retroposed elements, once established in an ancestral population, are highly valuable, virtually homoplasy-free markers of species evolution; after applying stringent orthology criteria, their phylogenetically informative presence/absence patterns are free of random noise and independent of evolutionary rate or nucleotide composition effects. We screened for early neoavian orthologous retroposon insertions and identified six markers with conflicting presence/absence patterns, whereas six additional retroposons established before or after the presumed major neoavian radiation show consistent phylogenetic patterns. The exceptionally frequent conflicting retroposon presence/absence patterns of neoavian orders are strong indicators of an extensive incomplete lineage sorting era, potentially induced by an early rapid successive speciation of ancestral Neoaves.
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http://dx.doi.org/10.1093/molbev/msr319DOI Listing
June 2012

Mesozoic retroposons reveal parrots as the closest living relatives of passerine birds.

Nat Commun 2011 Aug 23;2:443. Epub 2011 Aug 23.

Institute of Experimental Pathology (ZMBE), University of Münster, Von-Esmarch-Strasse 56, D-48149 Münster, Germany.

The relationships of passerines (such as the well-studied zebra finch) with non-passerine birds is one of the great enigmas of avian phylogenetic research, because decades of extensive morphological and molecular studies yielded highly inconsistent results between and within data sets. Here we show the first application of the virtually homoplasy-free retroposon insertions to this controversy. Our study examined ~200,000 retroposon-containing loci from various avian genomes and retrieved 51 markers resolving early bird phylogeny. Among these, we obtained statistically significant evidence that parrots are the closest and falcons the second-closest relatives of passerines, together constituting the Psittacopasserae and the Eufalconimorphae, respectively. Our new and robust phylogenetic framework has substantial implications for the interpretation of various conclusions drawn from passerines as model organisms. This includes insights of relevance to human neuroscience, as vocal learning (that is, birdsong) probably evolved in the psittacopasseran ancestor, >30 million years earlier than previously assumed.
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http://dx.doi.org/10.1038/ncomms1448DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3265382PMC
August 2011

A novel web-based TinT application and the chronology of the Primate Alu retroposon activity.

BMC Evol Biol 2010 Dec 2;10:376. Epub 2010 Dec 2.

Institute of Experimental Pathology, ZMBE, University of Münster, Von-Esmarch-Str, 56, 48149 Münster, Germany.

Background: DNA sequences afford access to the evolutionary pathways of life. Particularly mobile elements that constantly co-evolve in genomes encrypt recent and ancient information of their host's history. In mammals there is an extraordinarily abundant activity of mobile elements that occurs in a dynamic succession of active families, subfamilies, types, and subtypes of retroposed elements. The high frequency of retroposons in mammals implies that, by chance, such elements also insert into each other. While inactive elements are no longer able to retropose, active elements retropose by chance into other active and inactive elements. Thousands of such directional, element-in-element insertions are found in present-day genomes. To help analyze these events, we developed a computational algorithm (Transpositions in Transpositions, or TinT) that examines the different frequencies of nested transpositions and reconstructs the chronological order of retroposon activities.

Results: By examining the different frequencies of such nested transpositions, the TinT application reconstructs the chronological order of retroposon activities. We use such activity patterns as a comparative tool to (1) delineate the historical rise and fall of retroposons and their relations to each other, (2) understand the retroposon-induced complexity of recent genomes, and (3) find selective informative homoplasy-free markers of phylogeny. The efficiency of the new application is demonstrated by applying it to dimeric Alu Short INterspersed Elements (SINE) to derive a complete chronology of such elements in primates.

Conclusion: The user-friendly, web-based TinT interface presented here affords an easy, automated screening for nested transpositions from genome assemblies or trace data, assembles them in a frequency-matrix, and schematically displays their chronological activity history.
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http://dx.doi.org/10.1186/1471-2148-10-376DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3014933PMC
December 2010

Tracking marsupial evolution using archaic genomic retroposon insertions.

PLoS Biol 2010 Jul 27;8(7):e1000436. Epub 2010 Jul 27.

Institute of Experimental Pathology (ZMBE), University of Münster, Münster, Germany.

The Australasian and South American marsupial mammals, such as kangaroos and opossums, are the closest living relatives to placental mammals, having shared a common ancestor around 130 million years ago. The evolutionary relationships among the seven marsupial orders have, however, so far eluded resolution. In particular, the relationships between the four Australasian and three South American marsupial orders have been intensively debated since the South American order Microbiotheria was taxonomically moved into the group Australidelphia. Australidelphia is significantly supported by both molecular and morphological data and comprises the four Australasian marsupial orders and the South American order Microbiotheria, indicating a complex, ancient, biogeographic history of marsupials. However, the exact phylogenetic position of Microbiotheria within Australidelphia has yet to be resolved using either sequence or morphological data analysis. Here, we provide evidence from newly established and virtually homoplasy-free retroposon insertion markers for the basal relationships among marsupial orders. Fifty-three phylogenetically informative markers were retrieved after in silico and experimental screening of approximately 217,000 retroposon-containing loci from opossum and kangaroo. The four Australasian orders share a single origin with Microbiotheria as their closest sister group, supporting a clear divergence between South American and Australasian marsupials. In addition, the new data place the South American opossums (Didelphimorphia) as the first branch of the marsupial tree. The exhaustive computational and experimental evidence provides important insight into the evolution of retroposable elements in the marsupial genome. Placing the retroposon insertion pattern in a paleobiogeographic context indicates a single marsupial migration from South America to Australia. The now firmly established phylogeny can be used to determine the direction of genomic changes and morphological transitions within marsupials.
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http://dx.doi.org/10.1371/journal.pbio.1000436DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2910653PMC
July 2010

Retroposon insertions provide insights into deep lagomorph evolution.

Mol Biol Evol 2010 Dec 28;27(12):2678-81. Epub 2010 Jun 28.

The homogenous mammalian order Lagomorpha comprises about 80 species in two families, Ochotonidae (pikas) and Leporidae (rabbits and hares). However, the phylogenetic relationships among leporids are controversial. Molecular data, particularly from mitochondrial sequences, give highly homoplasious signals. To resolve the controversy between mitochondrial and nuclear data, we analyzed genomic orthologous retroposon insertion sites, a virtually homoplasy-free marker system. From a differential screen of rabbit genomic data for intronic retroposon insertions of CSINE elements, we polymerase chain reaction-amplified and sequenced 11 retroposons in eight representative lagomorphs. We found three retroposons shared among all lagomorphs but absent in outgroups, four confirmed the monophyly of leporids, and three significantly supported Pronolagus as the sister group to all other leporids. One retroposon supported the monophyly of Lepus. The position of Pronolagus outside of the remaining leporids supports the sequence-based signals of nuclear genes and clearly refutes the misleading signals of mitochondrial genes.
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http://dx.doi.org/10.1093/molbev/msq162DOI Listing
December 2010

Rodent evolution: back to the root.

Mol Biol Evol 2010 Jun 25;27(6):1315-26. Epub 2010 Jan 25.

Institute of Experimental Pathology (ZMBE), University of Münster, Münster, Germany.

Some 70 Ma, rodents arose along a branch of our own mammalian lineage. Today, about 40% of all mammalian species are rodents and are found in vast numbers on almost every continent. Not only is their proliferation extensive but also the rates of DNA evolution vary significantly among lineages, which has hindered attempts to reconstruct, especially the root of, their evolutionary history. The presence or absence of rare genomic changes, such as short interspersed elements (SINEs), are, however, independent of high molecular substitution rates and provide a powerful, virtually homoplasy-free source for solving such phylogenetic problems. We screened 12 Gb of rodent genomic information using whole-genome three-way alignments, multiple lineage-specific sequences, high-throughput polymerase chain reaction amplifications, and sequencing to reveal 65 phylogenetically informative SINE insertions dispersed over 23 rodent phylogenetic nodes. Eight SINEs and six indels provide significant support for an early association of the Mouse-related and Ctenohystrica (guinea pig and relatives) clades, the Squirrel-related clade being the sister group. This early speciation scenario was also evident in the genomewide distribution pattern of B1-related retroposons, as mouse and guinea pig genomes share six such retroposon subfamilies, containing hundreds of thousands of elements that are clearly absent in the ground squirrel genome. Interestingly, however, two SINE insertions and one diagnostic indel support an association of Ctenohystrica with the Squirrel-related clade. Lineage sorting or a more complex evolutionary scenario that includes an early divergence of the Squirrel-related ancestor and a subsequent hybridization of the latter and the Ctenohystrica lineage best explains such apparently contradictory insertions.
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http://dx.doi.org/10.1093/molbev/msq019DOI Listing
June 2010

Mosaic retroposon insertion patterns in placental mammals.

Genome Res 2009 May 4;19(5):868-75. Epub 2009 Mar 4.

Institute of Experimental Pathology, Center for Molecular Biology of Inflammation, University of Münster, Münster, Germany.

One and a half centuries after Charles Darwin and Alfred Russel Wallace outlined our current understanding of evolution, a new scientific era is dawning that enables direct observations of genetic variation. However, pure sequence-based molecular attempts to resolve the basal origin of placental mammals have so far resulted only in apparently conflicting hypotheses. By contrast, in the mammalian genomes where they were highly active, the insertion of retroelements and their comparative insertion patterns constitute a neutral, virtually homoplasy-free archive of evolutionary histories. The "presence" of a retroelement at an orthologous genomic position in two species indicates their common ancestry in contrast to its "absence" in more distant species. To resolve the placental origin controversy we extracted approximately 2 million potentially phylogenetically informative, retroposon-containing loci from representatives of the major placental mammalian lineages and found highly significant evidence challenging all current single hypotheses of their basal origin. The Exafroplacentalia hypothesis (Afrotheria as the sister group to all remaining placentals) is significantly supported by five retroposon insertions, the Epitheria hypothesis (Xenarthra as the sister group to all remaining placentals) by nine insertion patterns, and the Atlantogenata hypothesis (a monophyletic clade comprising Xenarthra and Afrotheria as the sister group to Boreotheria comprising all remaining placentals) by eight insertion patterns. These findings provide significant support for a "soft" polytomy of the major mammalian clades. Ancestral successive hybridization events and/or incomplete lineage sorting associated with short speciation intervals are viable explanations for the mosaic retroposon insertion patterns of recent placental mammals and for the futile search for a clear root dichotomy.
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http://dx.doi.org/10.1101/gr.090647.108DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2675975PMC
May 2009

Genome analysis of the platypus reveals unique signatures of evolution.

Nature 2008 May;453(7192):175-83

Genome Sequencing Center, Washington University School of Medicine, Campus Box 8501, 4444 Forest Park Avenue, St Louis, Missouri 63108, USA.

We present a draft genome sequence of the platypus, Ornithorhynchus anatinus. This monotreme exhibits a fascinating combination of reptilian and mammalian characters. For example, platypuses have a coat of fur adapted to an aquatic lifestyle; platypus females lactate, yet lay eggs; and males are equipped with venom similar to that of reptiles. Analysis of the first monotreme genome aligned these features with genetic innovations. We find that reptile and platypus venom proteins have been co-opted independently from the same gene families; milk protein genes are conserved despite platypuses laying eggs; and immune gene family expansions are directly related to platypus biology. Expansions of protein, non-protein-coding RNA and microRNA families, as well as repeat elements, are identified. Sequencing of this genome now provides a valuable resource for deep mammalian comparative analyses, as well as for monotreme biology and conservation.
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http://dx.doi.org/10.1038/nature06936DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2803040PMC
May 2008

Retroposed SNOfall--a mammalian-wide comparison of platypus snoRNAs.

Genome Res 2008 Jun 7;18(6):1005-10. Epub 2008 May 7.

Institute of Experimental Pathology (ZMBE), University of Münster, Münster 48149, Germany.

Diversification of mammalian species began more than 160 million years ago when the egg-laying monotremes diverged from live bearing mammals. The duck-billed platypus (Ornithorhynchus anatinus) and echidnas are the only potential contemporary witnesses of this period and, thereby, provide a unique insight into mammalian genome evolution. It has become clear that small RNAs are major regulatory agents in eukaryotic cells, and the significant role of non-protein-coding (npc) RNAs in transcription, processing, and translation is now well accepted. Here we show that the platypus genome contains more than 200 small nucleolar (sno) RNAs among hundreds of other diverse npcRNAs. Their comparison among key mammalian groups and other vertebrates enabled us to reconstruct a complete temporal pathway of acquisition and loss of these snoRNAs. In platypus we found cis- and trans-duplication distribution patterns for snoRNAs, which have not been described in any other vertebrates but are known to occur in nematodes. An exciting novelty in platypus is a snoRNA-derived retroposon (termed snoRTE) that facilitates a very effective dispersal of an H/ACA snoRNA via RTE-mediated retroposition. From more than 40,000 detected full-length and truncated genomic copies of this snoRTE, at least 21 are processed into mature snoRNAs. High-copy retroposition via multiple host gene-promoted transcription units is a novel pathway for combining housekeeping function and SINE-like dispersal and reveals a new dimension in the evolution of novel snoRNA function.
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http://dx.doi.org/10.1101/gr.7177908DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2413151PMC
June 2008

Waves of genomic hitchhikers shed light on the evolution of gamebirds (Aves: Galliformes).

BMC Evol Biol 2007 Oct 9;7:190. Epub 2007 Oct 9.

Institute of Experimental Pathology (ZMBE) University of Münster, Von-Esmarch-Str, 56, D-48149 Münster, Germany.

Background: The phylogenetic tree of Galliformes (gamebirds, including megapodes, currassows, guinea fowl, New and Old World quails, chicken, pheasants, grouse, and turkeys) has been considerably remodeled over the last decades as new data and analytical methods became available. Analyzing presence/absence patterns of retroposed elements avoids the problems of homoplastic characters inherent in other methodologies. In gamebirds, chicken repeats 1 (CR1) are the most prevalent retroposed elements, but little is known about the activity of their various subtypes over time. Ascertaining the fixation patterns of CR1 elements would help unravel the phylogeny of gamebirds and other poorly resolved avian clades.

Results: We analyzed 1,978 nested CR1 elements and developed a multidimensional approach taking advantage of their transposition in transposition character (TinT) to characterize the fixation patterns of all 22 known chicken CR1 subtypes. The presence/absence patterns of those elements that were active at different periods of gamebird evolution provided evidence for a clade (Cracidae + (Numididae + (Odontophoridae + Phasianidae))) not including Megapodiidae; and for Rollulus as the sister taxon of the other analyzed Phasianidae. Genomic trace sequences of the turkey genome further demonstrated that the endangered African Congo Peafowl (Afropavo congensis) is the sister taxon of the Asian Peafowl (Pavo), rejecting other predominantly morphology-based groupings, and that phasianids are monophyletic, including the sister taxa Tetraoninae and Meleagridinae.

Conclusion: The TinT information concerning relative fixation times of CR1 subtypes enabled us to efficiently investigate gamebird phylogeny and to reconstruct an unambiguous tree topology. This method should provide a useful tool for investigations in other taxonomic groups as well.
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http://dx.doi.org/10.1186/1471-2148-7-190DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2169234PMC
October 2007

Retroposed elements and their flanking regions resolve the evolutionary history of xenarthran mammals (armadillos, anteaters, and sloths).

Mol Biol Evol 2007 Nov 19;24(11):2573-82. Epub 2007 Sep 19.

Institute of Experimental Pathology (ZMBE), University of Münster, Münster, Germany.

Armadillos, anteaters, and sloths (Order Xenarthra) comprise 1 of the 4 major clades of placental mammals. Isolated in South America from the other continental landmasses, xenarthrans diverged over a period of about 65 Myr, leaving more than 200 extinct genera and only 31 living species. The presence of both ancestral and highly derived anatomical features has made morphoanatomical analyses of the xenarthran evolutionary history difficult, and previous molecular analyses failed to resolve the relationships within armadillo subfamilies. We investigated the presence/absence patterns of retroposons from approximately 7,400 genomic loci, identifying 35 phylogenetically informative elements and an additional 39 informative rare genomic changes (RGCs). DAS-short interspersed elements (SINEs), previously described only in the Dasypus novemcinctus genome, were found in all living armadillo genera, including the previously unsampled Chlamyphorus, but were noticeably absent in sloths. The presence/absence patterns of the phylogenetically informative retroposed elements and other RGCs were then compared with data from the DNA sequences of the more than 12-kb flanking regions of these retroposons. Together, these data provide the first fully resolved genus tree of xenarthrans. Interestingly, multiple evidence supports the grouping of Chaetophractus and Zaedyus as a sister group to Euphractus within Euphractinae, an association that was not previously demonstrated. Also, flanking sequence analyses favor a close phylogenetic relationship between Cabassous and Tolypeutes within Tolypeutinae. Finally, the phylogenetic position of the subfamily Chlamyphorinae is resolved by the noncoding sequence data set as the sister group of Tolypeutinae. The data provide a stable phylogenetic framework for further evolutionary investigations of xenarthrans and important information for defining conservation priorities to save the diversity of one of the most curious groups of mammals.
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http://dx.doi.org/10.1093/molbev/msm201DOI Listing
November 2007

Evolutionary history of 7SL RNA-derived SINEs in Supraprimates.

Trends Genet 2007 Apr 20;23(4):158-61. Epub 2007 Feb 20.

Institute of Experimental Pathology, ZMBE, University of Münster, Von-Esmarch-Str. 56, D-48149 Münster, Germany.

The evolutionary relationships of 7SL RNA-derived SINEs such as the primate Alu or the rodent B1 elements have hitherto been obscure. We established an unambiguous phylogenetic tree for Supraprimates, and derived intraordinal relationships of the 7SL RNA-derived SINEs. As well as new elements in Tupaia and primates, we also found that the purported ancestral fossil Alu monomer was restricted to Primates, and provide here the first description of a potential chimeric promoter box region in SINEs.
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http://dx.doi.org/10.1016/j.tig.2007.02.002DOI Listing
April 2007

Retroposed elements as archives for the evolutionary history of placental mammals.

PLoS Biol 2006 Apr 14;4(4):e91. Epub 2006 Mar 14.

Institute of Experimental Pathology, Center for Molecular Biology of Inflammation, University of Münster, Münster, Germany.

Reconstruction of the placental mammalian (eutherian) evolutionary tree has undergone diverse revisions, and numerous aspects remain hotly debated. Initial hierarchical divisions based on morphology contained many misgroupings due to features that evolved independently by similar selection processes. Molecular analyses corrected many of these misgroupings and the superordinal hierarchy of placental mammals was recently assembled into four clades. However, long or rapid evolutionary periods, as well as directional mutation pressure, can produce molecular homoplasies, similar characteristics lacking common ancestors. Retroposed elements, by contrast, integrate randomly into genomes with negligible probabilities of the same element integrating independently into orthologous positions in different species. Thus, presence/absence analyses of these elements are a superior strategy for molecular systematics. By computationally scanning more than 160,000 chromosomal loci and judiciously selecting from only phylogenetically informative retroposons for experimental high-throughput PCR applications, we recovered 28 clear, independent monophyly markers that conclusively verify the earliest divergences in placental mammalian evolution. Using tests that take into account ancestral polymorphisms, multiple long interspersed elements and long terminal repeat element insertions provide highly significant evidence for the monophyletic clades Boreotheria (synonymous with Boreoeutheria), Supraprimates (synonymous with Euarchontoglires), and Laurasiatheria. More importantly, two retropositions provide new support for a prior scenario of early mammalian evolution that places the basal placental divergence between Xenarthra and Epitheria, the latter comprising all remaining placentals. Due to its virtually homoplasy-free nature, the analysis of retroposon presence/absence patterns avoids the pitfalls of other molecular methodologies and provides a rapid, unequivocal means for revealing the evolutionary history of organisms.
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http://dx.doi.org/10.1371/journal.pbio.0040091DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1395351PMC
April 2006

A novel abundant family of retroposed elements (DAS-SINEs) in the nine-banded armadillo (Dasypus novemcinctus).

Mol Biol Evol 2005 Apr 22;22(4):886-93. Epub 2004 Dec 22.

Institute of Experimental Pathology (ZMBE), University of Münster, Münster, Germany.

About half of the mammalian genome is composed of retroposons. Long interspersed elements (LINEs) and short interspersed elements (SINEs) are the most abundant repetitive elements and account for about 21% and 13% of the human genome, respectively. SINEs have been detected in all major mammalian lineages, except for the South American order Xenarthra, also termed Edentata (armadillos, anteaters, and sloths). Investigating this order, we discovered a novel high-copy-number family of tRNA derived SINEs in the nine-banded armadillo Dasypus novemcinctus, a species that successfully crossed the Central American land bridge to North America in the Pliocene. A specific computer algorithm was developed, and we detected and extracted 687 specific SINEs from databases. Termed DAS-SINEs, we further divided them into six distinct subfamilies. We extracted tRNA(Ala)-derived monomers, two types of dimers, and three subfamilies of chimeric fusion products of a tRNA(Ala) domain and an approximately 180-nt sequence of thus far unidentified origin. Comparisons of secondary structures of the DAS-SINEs' tRNA domains suggest selective pressure to maintain a tRNA-like D-arm structure in the respective founder RNAs, as shown by compensatory mutations. By analysis of subfamily-specific genetic variability, comparison of the proportion of direct repeats, and analysis of self-integrations as well as key events of dimerization and deletions or insertions, we were able to delineate the evolutionary history of the DAS-SINE subfamilies.
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http://dx.doi.org/10.1093/molbev/msi071DOI Listing
April 2005

A novel class of mammalian-specific tailless retropseudogenes.

Genome Res 2004 Oct 13;14(10A):1911-5. Epub 2004 Sep 13.

Institute of Experimental Pathology (ZMBE), University of Muenster, D-48149 Muenster, Germany.

In addition to their central function in protein biosynthesis, tRNAs also play a pervasive role in genome evolution and architecture because of their extensive ability to serve as templates for retroposition. Close to half of the human genome consists of discernible transposable elements, a vast majority of which are derived from RNA via reverse transcription and genomic integration. Apart from the presence of direct repeats (DRs) that flank the integrated sequence of retroposons, genomic integrations are usually marked by an oligo(A) tail. Here, we describe a novel class of retroposons that lack A-tails and are therefore termed tailless retropseudogenes. Analysis of approximately 2500 tRNA-related young tailless retropseudogene sequences revealed that they comprise processed and unprocessed (pre-)tRNAs, 3'-truncated in their loop regions, or truncated tRNA-derived SINE RNAs. Surprisingly, their mostly nonrandom integration is dependent on the priming of reverse transcription at sites determined by their 3'-terminal 2-18 nucleotides and completely independent from oligoadenylation of the template RNA. Thus, tailless retropseudogenes point to a novel, variant mechanism for the biogenesis of retrosequences.
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http://dx.doi.org/10.1101/gr.2720104DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC524414PMC
October 2004
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