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

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

Possible discrepancy between one- and two-sided (species) screenings.

<p>Screening for phylogenetic markers based on all possible tree topologies for three species A, B, C when only one reference genome A (a-c) or B (d-f) is available. The red lineage indicates the branches where markers can be detected. Screening from A reveals three markers. The two light red markers are artifacts from ancient incomplete lineage sorting (ILS) and the dark red marker is a phylogenetically informative marker. Screening from B reveals 11 markers with 8 markers supporting B plus C and one marker supporting A plus (B plus C). The two light red markers in (d) are the same detected from species A in (a). The correct topology is shown in tree (f). This correct tree would not be detectible by screening only from the genome of species A.</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

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

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

Schematic representation of all possible phylogenetic patterns.

<p>For the markers <i>n</i>₁—(AB)C, <i>n</i>_<i>2</i>—(AC)B, and <i>n</i>_<i>3</i>—(BC)A, their sum <i>n</i> is fixed (<i>n = n</i>_<i>1</i><i>+n</i>_<i>2</i><i>+n</i>_<i>3</i>). The triangle reflects all possible combinations of <i>n</i>₁, <i>n</i>_<i>2</i>, and <i>n</i>_<i>3</i>, whereby the values at the corners are (<i>n</i>_<i>1</i>:0:0), (0:<i>n</i>_<i>2</i>:0), and (0:0:<i>n</i>_<i>3</i>) (counterclockwise from the upper corner). The respective trees indicate supported tree configurations (<i>C-tree</i>, <i>A-tree</i>, and <i>B-tree</i>), red balls consolidate insertion support for the given branches. The grey scale arrowheads within the triangle indicate the statistically significant combinations of supporting tree configurations shown at the corners of the triangle; the darker the arrow the more significant support for the corresponding tree, the lighter the arrow the less support and the more the branching resembles a polytomy. The circular area at the center of the triangle denotes the <i>polytomy</i> zone (<i>ABC-tree</i>, where <i>n</i>_<i>1</i> = <i>n</i>_<i>2</i> = <i>n</i>_<i>3</i>). The trees on the outside edges of the central triangle indicate <i>hybridization</i> zones (<i>B-fusion</i>, <i>C-fusion</i>, and <i>A-fusion</i>, denoted as A(B)C hybridization (where <i>n</i>_<i>1</i>≥<i>n</i>_<i>2</i>, and <i>n</i>_<i>2</i><i>>n</i>_<i>3</i>), A(C)B hybridization (where <i>n</i>_<i>1</i>≥<i>n</i>_<i>3</i>, and <i>n</i>_<i>2</i><<i>n</i>₃), and B(A)C hybridization (where <i>n</i>_<i>2</i>≥<i>n</i>_<i>3</i>, and <i>n</i>_<i>1</i><<i>n</i>_<i>2</i>), respectively).</p

Data from: Speciation network in Laurasiatheria: retrophylogenomic signals

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

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

Abstract 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.</p