A Population Genetic Model for the Maintenance of R2
Retrotransposons in rRNA Gene Loci
Jun Zhou.¤a, Michael T. Eickbush.¤b, Thomas H. Eickbush*
Department of Biology, University of Rochester, Rochester, New York, United States of America
R2 retrotransposable elements exclusively insert into the tandemly repeated rRNA genes, the rDNA loci, of their animal
hosts. R2 elements form stable long-term associations with their host, in which all individuals in a population contain many
potentially active copies, but only a fraction of these individuals show active R2 retrotransposition. Previous studies have
found that R2 RNA transcripts are processed from a 28S co-transcript and that the likelihood of R2-inserted units being
transcribed is dependent upon their distribution within the rDNA locus. Here we analyze the rDNA locus and R2 elements
from nearly 100 R2-active and R2-inactive individuals from natural populations of Drosophila simulans. Along with previous
findings concerning the structure and expression of the rDNA loci, these data were incorporated into computer simulations
to model the crossover events that give rise to the concerted evolution of the rRNA genes. The simulations that best
reproduce the population data assume that only about 40 rDNA units out of the over 200 total units are actively transcribed
and that these transcribed units are clustered in a single region of the locus. In the model, the host establishes this
transcription domain at each generation in the region with the fewest R2 insertions. Only if the host cannot avoid R2
insertions within this 40-unit domain are R2 elements active in that generation. The simulations also require that most
crossover events in the locus occur in the transcription domain in order to explain the empirical observation that R2
elements are seldom duplicated by crossover events. Thus the key to the long-term stability of R2 elements is the stochastic
nature of the crossover events within the rDNA locus, and the inevitable expansions and contractions that introduce and
remove R2-inserted units from the transcriptionally active domain.
Citation: Zhou J, Eickbush MT, Eickbush TH (2013) A Population Genetic Model for the Maintenance of R2 Retrotransposons in rRNA Gene Loci. PLoS Genet 9(1):
Editor: David J. Begun, University of California Davis, United States of America
Received June 15, 2012; Accepted November 2, 2012; Published January 10, 2013
Copyright: ? 2013 Zhou et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This study was supported by NIH grant R01GM042790. The funders had no role in study design, data collection and analysis, decision to publish, or
preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: firstname.lastname@example.org
¤a Current address: Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, United States of America
¤b Current address: Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America
. These authors contributed equally to this work.
Abundant ribosomal RNA (rRNA) is essential for cellular
metabolism during all periods of development. The genes
encoding these RNAs reside as nearly identical tandemly repeated
units with each unit composed of an 18S, 5.8S and 28S rRNA
gene (Figure 1A). Surprisingly, these tandem genes, referred to as
rDNA loci, serve as a genomic niche for the insertion of various
mobile elements . These elements block the production of
functional rRNA from inserted units, however, the effects of this
potential disruption of rRNA production is minimized because
organisms typically contain many more rDNA units than are
needed for transcription [2–4].
The retrotransposon, R2, is the best understood of the rDNA
specific elements. R2 elements are present in many animal phyla
[5–7] but have been most intensively studied in Drosophila [8,9].
The same lineage of R2 elements is present in most Drosophila
groups, and no evidence has been found for horizontal jumps
between species . While difficult to establish definitively, this co-
evolution of R2 with its host may extend back to the origin of
the major animal phyla [6,7,10,11]. Clearly a balance must be
maintained between the levels of retrotransposition required to
preserve the elements and the number of rDNA units needed to
maintain host fitness.
While permitting long term maintenance, the equilibrium
between the rDNA loci and R2 elements appears highly dynamic,
as the size of the rDNA loci vary greatly between individuals, and
individual copies of R2 are rapidly gained and lost from each
locus [12,13]. A critical contributor to this dynamic equilibrium is
the frequent unequal crossovers between the tandem repeats of
the rDNA loci, which preserve the high levels of sequence identity
between rRNA genes (Figure S1). Attempts have been made over
the years to model this concerted evolution of the rRNA genes
[14–16]. Recently we incorporated the presence of transposable
elements into standard crossover models of rDNA locus evolution
. Varying the rates of crossover, R2 retrotransposition, and
the number of rDNA units required for host fitness, stable
populations could be simulated with rDNA loci of various sizes
and levels of R2 insertion. Unfortunately, because little was
known about of the forces that controlled R2 activity, these
simulations simply assumed low rates of retrotransposition in all
individuals with R2.
PLOS Genetics | www.plosgenetics.org1 January 2013 | Volume 9 | Issue 1 | e1003179
Recent studies have now provided a better understanding of the
regulation of R2 activity in Drosophila simulans. First, regulation of
R2 activity appears to be at the level of transcription with control
over transcription mapping to the rDNA locus itself . Second,
R2 elements do not encode their own promoter but are co-
transcribed with the rDNA unit with their mature R2 transcript
processed from the co-transcript by a ribozyme encoded at the 59
end of R2 . Finally, R2 transcription correlates best with the
distribution of R2 elements across the rDNA locus rather than the
size of the rDNA locus or the number of R2 insertions .
Animals with no R2 transcripts contain at least one large region of
rDNA units free of R2, while animals with R2 transcripts contain a
more uniform distribution of R2 across the rDNA locus and thus
no large region free of R2 insertions [18,20]. Based on these
findings, we proposed a ‘‘transcription domain’’ model of R2
regulation in which the host identifies for transcription that region
of the rDNA locus with the lowest level of R2 insertions. In this
model, individual copies of R2 are transcribed only when the
largest contiguous region of the rDNA locus free of R2 insertions is
less than the size of the transcription domain (Figure 1B).
In this report we have expanded our study of natural
populations of Drosophila simulans to obtain better estimates of the
range of rDNA locus size and number of R2 in active and inactive
individuals. New computer simulations incorporating the tran-
scription domain model for R2 regulation are able to generate
stable populations containing rDNA loci with the dynamic
properties found in natural populations. Crossover frequency
and location, rates of retrotransposition, transcription domain size,
and reduction in host fitness are each evaluated for their effects on
the final equilibrium between mobile element and host.
Range of rDNA locus size and R2 number in natural
Correlation of R2 activity with the various properties of an
rDNA locus is simplified in D. simulans because all rDNA units in
this species are located in one locus on the X chromosome . In
a previous report , R2 transcript levels were determined for
180 lines each containing one rDNA locus from a natural
population in San Diego, CA or Atlanta, GA (iso-rDNA lines).
Eighteen lines representing the range of R2 transcript levels were
then selected to determine the sizes of their rDNA loci and
number of R2 copies. No correlation was detected between R2
transcript levels and either rDNA locus size or number of R2
elements. To better define the range of locus size and R2 number
in the two populations, these values were determined again for the
original 18 lines as well as for an additional 77 randomly chosen
lines from the two populations (see Materials and Methods).
Mean rDNA locus size was found to be 230 units (range 132–
373) for the 44 iso-rDNA lines from San Diego and 219 (range
115–386) for the 51 iso-rDNA lines from Atlanta. The mean R2
number was 52 (range 23–70) copies for the San Diego population
and 50 (range 31–79) for the Atlanta population. Based on the
insignificant difference in the range of values obtained for the two
populations (R2 number, P=0.75; rDNA locus size, P=0.42,
Kolmogorov-Smirnov test) as well as the similar numbers of
individuals with detectable levels of R2 transcription in the two
populations , all subsequent analyses use the combined data
sets. The distribution of locus sizes and R2 copy number
determined for the 95 iso-rDNA lines are shown in Figure 2A.
The number of rDNA units per locus varied over a 3-fold range
(115 to 386 units), as did the R2 number (23 to 79 copies). A
significant correlation was found between the rDNA locus size and
the number of R2 (Spearman rank correlation r=0.47, P=1028).
The physical properties of the rDNA locus in the 95 lines were
then compared to the level of R2 transcription. A trend towards
higher levels of R2 transcripts was associated with smaller rDNA
loci (Figure 2B), loci containing more R2 elements (Figure 2C),
and loci containing higher fractions of R2-inserted units
(Figure 2D). However, there was considerable scatter of transcript
levels associated with all ranges of locus size, R2 number and
insertion density. These properties of the rDNA locus are thus, not
adequate predictors of R2 transcription.
Frequency of R2 element duplications by recombination
Crossovers between sister chromatids have been suggested to be
the major recombinational force at work in the concerted
evolution of rDNA loci . In the absence of retrotransposition
repeated crossovers in combination with negative selection against
inserted units will eventually eliminate R2-inserted units from the
rDNA locus . However, in the short term, crossovers can
duplicate those R2-inserted units that are located within the offset
between the two sister chromatids (Figure S1). It is possible to
determine whether individual R2-inserted units have been
duplicated by crossovers because many R2s have distinctive 59
truncations generated during their retrotransposition [12,13].
Such 59 truncations are a characteristic property of the target-
primed reverse transcription mechanism used by non-LTR
Sensitive PCR assays using one primer upstream of the 28S
rDNA insertion site in combination with multiple primers
throughout the R2 element have been developed to score all 59
truncated R2s within individual rDNA loci [12,13,20]. By
quantifying the signal associated with each PCR band these
assays can be used to score whether the individual 59 truncated
elements exist as one, two, three etc. copies in the rDNA locus
[20,24]. Of the 386 R2 59 truncations present in the 18 original
lines representing the range of R2 transcript levels in the D.
simulans populations , 335 (86.8%) were determined to be
single-copy, 41 were present in two copies, 9 were present in three
copies, and 1 was present in four copies. This infrequent
duplication of R2-inserted units has also been found for stocks of
Selfish transposable elements survive in eukaryotic ge-
nomes despite the elaborate mechanisms developed by
the hosts to limit their activity. One accessible system that
simplifies the complex interactions between element and
host involves the R2 elements, which exclusively insert in
the tandemly arranged rRNA genes. R2 exhibits remarkable
stability in animal lineages even though each insertion
inactivates one rRNA gene. Here we determine the size of
the rDNA locus and R2 number in natural isolates of
Drosophila simulans. Combined with previous data con-
cerning the expression and regulation of R2, we develop a
detailed population genetic model for rRNA gene and R2
evolution that duplicates all properties of the rRNA loci in
natural populations. Critical components of the model are
that only a contiguous 40 unit array of rRNA gene units are
needed for transcription, that R2 elements are active only
when present in this transcription domain, and that most
of the crossovers in the rDNA loci occur in this domain.
These results suggest that the key to the long-term
survival of R2 is the redistribution of rDNA units in the
locus brought about by the crossovers that maintain
sequence identity in all rDNA units.
Model of R2 Maintenance
PLOS Genetics | www.plosgenetics.org2 January 2013 | Volume 9 | Issue 1 | e1003179
the following values where used for all simulations reported here;
loop-deletions, S=0.2; retrotranspositions, S=0.4. Localizing
these events to greater degrees within the transcription domain
increased the number of R2 elements within the rDNA loci,
because new R2-active chromosomes were more rapidly produced
in the population.
loci can change the size of the locus and eliminate/duplicate
specific copies of R2 elements. A small region of an rDNA locus is
diagramed with individual R2 elements indentified (orange boxes)
within rDNA units (black boxes). Two identical rDNA loci (i.e.
sister chromatids) are aligned but offset by three rDNA units. A
crossover between uninserted rDNA units located to either side of
element c (dotted lines) results in recombinants in which one locus
is three units shorter and missing element c, and one locus is three
units longer with two copies of element c.
Diagram showing how crossovers within the rDNA
with simulated loci generated by limiting crossovers to the center
of the rDNA locus. (A) Empirical data determined for rDNA loci
from the populations in Figure 2 are re-plotted to show the
distributions of rDNA locus size (left panel), total R2 number per
locus (middle panel), and the number of instances R2 copies had
been duplicated by crossovers (right panel). These plots are
identical to those in Figure 3A. (B) Simulation data based on the
modeling approach described in ref. 17, and utilize the same
parameters as in Figure 3B, except that all crossover events are
clustered at the center of the rDNA locus. The three panels
showing the distributions of locus size, number of R2, and R2
duplication state are shown below the corresponding data from the
Comparison of rDNA loci from natural populations
transcription domain model simulations described in this report.
A flow chart of the computer program used for the
structures reached for the simulated populations was independent
of the starting properties of the rDNA loci. The mean rDNA locus
size (top three lines) and R2-inserted units (bottom three lines) for
the populations in the first 6000 generations of the simulation are
shown for different starting conditions: blue traces (large initial loci
with many R2s), red traces (smaller loci with fewer R2s) and green
traces (loci with only one R2 insertion). R2-inserted units were
randomly distributed in the starting rDNA loci. Because individual
simulations show large stochastic changes, the traces represent the
mean values of 50 replicates. All parameter values used in these
simulations are the same as those used in Figure 3C, Figure 4 and
Figure 5. Lower final mean values for the simulations initiated
with only one R2 copy per locus (green) resulted from the loss of all
R2 elements from the population in 11% of the simulations. Those
populations that retained R2 had the same mean values for locus
size and R2 number as in the other two simulations.
Data showing that the final equilibrium of rDNA
distribution of R2 elements in the simulations involving the
transcription domain model. The simulation parameters are the
same as that shown in Figure 3C, Figure 4 and Figure 5. A.
Location of the transcription domain. At the end of the simulations
each rDNA loci was divided into 20 equal-sized segments, and the
fraction of the transcription domains in the population that were
located in each segment was plotted. B. Distribution of R2
elements across the rDNA locus in the R2-inactive loci. The mean
fraction of the rDNA units inserted with R2 for each of the 20
equal-sized segments of the rDNA loci has been plotted. C.
Distribution of R2 elements across the locus in the R2-active loci.
The data plotted is as in B. The central one-third of the R2-active
loci have about a 60% higher mean frequency of R2 insertions
than the R2-inactive loci.
Location of the rDNA transcription domain and
the simulations was not highly sensitive to the size of the
populations. The simulation parameters are the same as that
shown in Figure 3C, Figure 4 and Figure 5. The same four
properties of the loci that were shown in Figure 6 and Figure 7 are
also shown here: black symbols, the mean rDNA locus size; blue
symbols, the mean number of R2 elements; red symbols, the
fraction of the R2 elements that were single copy (i.e. not
duplicated by a crossover event); and green symbols, the fraction
of individuals in the population with active R2 elements. For most
population sizes the average values and standard errors presented
were based on 50 simulations. In the case of 2,000 individual
population, 100 simulations were conducted. Because of the time
associated with each simulation, in the case of the 200,000
individual and 1,000,000 individual populations only 15 simula-
tions and 2 simulations, respectively, were conducted. The
standard error among the simulations was associated with random
genetic drift and therefore decreased dramatically with population
Data showing that the final equilibrium reached in
was used in this report to simulate the R2 elements and the rDNA
loci in populations of D. simulans. The random number generator
available at http://fmg-www.cs.ucla.edu/geoff/mtwist.html was
used in all simulations.
A text file of the computer program, written in C, that
We thank Xian Zhang for his original programming script and his insights
during the initial stages of this analysis. We thank Jack Werren and Daven
Presgraves for comments on an early version of the manuscript, and Danna
Eickbush and William Burke for their comments on the final versions.
Wrote the paper: JZ MTE THE. Conceived and designed the experiments:
JZ MTE THE. Analyzed the data: JZ MTE THE. Performed the
experiments: JZ MTE. Contributed reagents/materials/analysis tools: JZ
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Model of R2 Maintenance
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