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

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. Conclusions 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

Retrophylogenomics place tarsiers on the evolutionary branch of anthropoids

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

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

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.Victor C. Mason, Gang Li Patrick Minx, Jürgen Schmitz, Gennady Churakov, Liliya Doronina, Amanda D. Melin ... et al

Retroposed Elements as Archives for the Evolutionary History of Placental Mammals

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

Tracking Marsupial Evolution Using Archaic Genomic Retroposon Insertions

Genome-wide comparisons of shared retroposon insertion patterns resolve the phylogeny of marsupials, clearly distinguishing South American and Australian species and lending support to Didelphimorphia as the basal split

A Novel Class of Mammalian-Specific Tailless Retropseudogenes

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 ∼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

A novel web-based TinT application and the chronology of the Primate <it>Alu </it>retroposon activity

Abstract 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.</p

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

<div><p>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 <a href="http://retrogenomics.uni-muenster.de:3838/KKSC_significance_test/" target="_blank">http://retrogenomics.uni-muenster.de:3838/KKSC_significance_test/</a>.</p></div