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

Kriegs JO, Matzke A, Churakov G, Kuritzin A, Mayr G, Brosius J, Schmitz J - BMC Evol. Biol. (2007)

Bottom Line: 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.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.This method should provide a useful tool for investigations in other taxonomic groups as well.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Experimental Pathology (ZMBE) University of Münster, Von-Esmarch-Str, 56, D-48149 Münster, Germany. kriegs@uni-muenster.de

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.

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Principle behind the TinT method. Examples of directed insertions of CR1 elements active at different periods. (A) Shows three different CR1 subytpes, active at non-overlapping periods and their resultant TinTs (in box below). As indicated by blue arrows, the youngest element (C2) inserted into both older subtypes (D2 and C4). D2 was active after C4 became inactive and inserted into the latter (red arrow). (B) Example of CR1 subtypes active at overlapping and non-overlapping periods. Only elements that were active during overlapping periods (C2 and B2) had the opportunity to insert each into the other. As the activity period of the B2 element only partially overlapped that of the C2, fewer insertions occurred in the B2-C2 direction (indicated by the thinner arrow). (C) Example of three CR1 subtypes active at overlapping periods. Note that the activity of C4 does not overlap that of F0, thus there was no opportunity for C4 to insert directly into F0. Again, fewer insertions of older elements into younger ones are indicated by thinner arrows.
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Figure 1: Principle behind the TinT method. Examples of directed insertions of CR1 elements active at different periods. (A) Shows three different CR1 subytpes, active at non-overlapping periods and their resultant TinTs (in box below). As indicated by blue arrows, the youngest element (C2) inserted into both older subtypes (D2 and C4). D2 was active after C4 became inactive and inserted into the latter (red arrow). (B) Example of CR1 subtypes active at overlapping and non-overlapping periods. Only elements that were active during overlapping periods (C2 and B2) had the opportunity to insert each into the other. As the activity period of the B2 element only partially overlapped that of the C2, fewer insertions occurred in the B2-C2 direction (indicated by the thinner arrow). (C) Example of three CR1 subtypes active at overlapping periods. Note that the activity of C4 does not overlap that of F0, thus there was no opportunity for C4 to insert directly into F0. Again, fewer insertions of older elements into younger ones are indicated by thinner arrows.

Mentions: While full-length CR1 elements are 4.5 kb long and contain two open reading frames [41], most CR1 sequences are truncated copies of their autonomous full-length master genes [39,43]. CR1 subtypes are characterized by diagnostic mutations that occurred in their specific master genes. Different full-length copies of master genes remained transcriptionally active over long, overlapping, periods of time and distributed corresponding retroelements in specific waves of activity as has been described in penguins [44]. To efficiently select phylogenetically informative CR1 elements from the chicken genome, it would be helpful to know which CR1 elements were active at which evolutionary time points. As CR1 elements, like most other retroposed elements, integrate almost randomly into the genome, they also frequently insert into other CR1 copies. But, at a given point in time only the active CR1 subtypes can insert into copies of their own or other CR1 subtypes (Figure 1). This provides information about which 'host' CR1 subtypes were already integrated at this particular time point. If the reverse case, in which the 'host' subtype inserted into an active CR1 subtype, cannot be found in the entire genome, one can assume that the 'host' subtype was probably already inactive at this particular time point. Thus, an analysis of the patterns of nested CR1 elements (transpositions in transpositions that we call the TinT method, Figure 1) provides a relative timetable of active CR1 elements. A first step towards a genome wide characterization of the activity ranges of CR1 elements is to search for the distribution patterns of nested retroposons. Churakov et al. [45] recently applied a novel method based on the single-case patterns of nested retroposons to characterize the historical appearance of various armadillo-specific SINE subfamilies. Similarly, Ichiyanagi and Okada used this method to determine the full lengths of SINEs in zebrafish [46] and Pace and Feschotte to investigate DNA transposon activity in the human genome [47].


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

Kriegs JO, Matzke A, Churakov G, Kuritzin A, Mayr G, Brosius J, Schmitz J - BMC Evol. Biol. (2007)

Principle behind the TinT method. Examples of directed insertions of CR1 elements active at different periods. (A) Shows three different CR1 subytpes, active at non-overlapping periods and their resultant TinTs (in box below). As indicated by blue arrows, the youngest element (C2) inserted into both older subtypes (D2 and C4). D2 was active after C4 became inactive and inserted into the latter (red arrow). (B) Example of CR1 subtypes active at overlapping and non-overlapping periods. Only elements that were active during overlapping periods (C2 and B2) had the opportunity to insert each into the other. As the activity period of the B2 element only partially overlapped that of the C2, fewer insertions occurred in the B2-C2 direction (indicated by the thinner arrow). (C) Example of three CR1 subtypes active at overlapping periods. Note that the activity of C4 does not overlap that of F0, thus there was no opportunity for C4 to insert directly into F0. Again, fewer insertions of older elements into younger ones are indicated by thinner arrows.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2169234&req=5

Figure 1: Principle behind the TinT method. Examples of directed insertions of CR1 elements active at different periods. (A) Shows three different CR1 subytpes, active at non-overlapping periods and their resultant TinTs (in box below). As indicated by blue arrows, the youngest element (C2) inserted into both older subtypes (D2 and C4). D2 was active after C4 became inactive and inserted into the latter (red arrow). (B) Example of CR1 subtypes active at overlapping and non-overlapping periods. Only elements that were active during overlapping periods (C2 and B2) had the opportunity to insert each into the other. As the activity period of the B2 element only partially overlapped that of the C2, fewer insertions occurred in the B2-C2 direction (indicated by the thinner arrow). (C) Example of three CR1 subtypes active at overlapping periods. Note that the activity of C4 does not overlap that of F0, thus there was no opportunity for C4 to insert directly into F0. Again, fewer insertions of older elements into younger ones are indicated by thinner arrows.
Mentions: While full-length CR1 elements are 4.5 kb long and contain two open reading frames [41], most CR1 sequences are truncated copies of their autonomous full-length master genes [39,43]. CR1 subtypes are characterized by diagnostic mutations that occurred in their specific master genes. Different full-length copies of master genes remained transcriptionally active over long, overlapping, periods of time and distributed corresponding retroelements in specific waves of activity as has been described in penguins [44]. To efficiently select phylogenetically informative CR1 elements from the chicken genome, it would be helpful to know which CR1 elements were active at which evolutionary time points. As CR1 elements, like most other retroposed elements, integrate almost randomly into the genome, they also frequently insert into other CR1 copies. But, at a given point in time only the active CR1 subtypes can insert into copies of their own or other CR1 subtypes (Figure 1). This provides information about which 'host' CR1 subtypes were already integrated at this particular time point. If the reverse case, in which the 'host' subtype inserted into an active CR1 subtype, cannot be found in the entire genome, one can assume that the 'host' subtype was probably already inactive at this particular time point. Thus, an analysis of the patterns of nested CR1 elements (transpositions in transpositions that we call the TinT method, Figure 1) provides a relative timetable of active CR1 elements. A first step towards a genome wide characterization of the activity ranges of CR1 elements is to search for the distribution patterns of nested retroposons. Churakov et al. [45] recently applied a novel method based on the single-case patterns of nested retroposons to characterize the historical appearance of various armadillo-specific SINE subfamilies. Similarly, Ichiyanagi and Okada used this method to determine the full lengths of SINEs in zebrafish [46] and Pace and Feschotte to investigate DNA transposon activity in the human genome [47].

Bottom Line: 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.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.This method should provide a useful tool for investigations in other taxonomic groups as well.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Experimental Pathology (ZMBE) University of Münster, Von-Esmarch-Str, 56, D-48149 Münster, Germany. kriegs@uni-muenster.de

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.

Show MeSH
Related in: MedlinePlus