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. 2020 Oct 5;16(10):e1009082.
doi: 10.1371/journal.pgen.1009082. eCollection 2020 Oct.

Disentangling the determinants of transposable elements dynamics in vertebrate genomes using empirical evidences and simulations

Yann Bourgeois  1   2 , Robert P Ruggiero  2   3 , Imtiyaz Hariyani  2 , Stéphane Boissinot  2
Affiliations

Disentangling the determinants of transposable elements dynamics in vertebrate genomes using empirical evidences and simulations

Yann Bourgeois et al. PLoS Genet. .

Abstract

The interactions between transposable elements (TEs) and their hosts constitute one of the most profound co-evolutionary processes found in nature. The population dynamics of TEs depends on factors specific to each TE families, such as the rate of transposition and insertional preference, the demographic history of the host and the genomic landscape. How these factors interact has yet to be investigated holistically. Here we are addressing this question in the green anole (Anolis carolinensis) whose genome contains an extraordinary diversity of TEs (including non-LTR retrotransposons, SINEs, LTR-retrotransposons and DNA transposons). We observed a positive correlation between recombination rate and frequency of TEs and densities for LINEs, SINEs and DNA transposons. For these elements, there was a clear impact of demography on TE frequency and abundance, with a loss of polymorphic elements and skewed frequency spectra in recently expanded populations. On the other hand, some LTR-retrotransposons displayed patterns consistent with a very recent phase of intense amplification. To determine how demography, genomic features and intrinsic properties of TEs interact we ran simulations using SLiM3. We determined that i) short TE insertions are not strongly counter-selected, but long ones are, ii) neutral demographic processes, linked selection and preferential insertion may explain positive correlations between average TE frequency and recombination, iii) TE insertions are unlikely to have been massively recruited in recent adaptation. We demonstrate that deterministic and stochastic processes have different effects on categories of TEs and that a combination of empirical analyses and simulations can disentangle these mechanisms.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Count of heterozygous sites across all 28 individuals included in this study.
Vertical dotted lined delimit the five main genetic clusters and the two outgroups in this order: A. allisoni and A. porcatus, SF, NWF, NEF, GA and CA. See S1 Fig for more details about these clusters.
Fig 2
Fig 2. Allele frequency spectra for TEs belonging to two genetic clusters identified in the green anole.
NEF (N = 8 diploid individuals) corresponds to a large, stable population from Florida, and GA (N = 7 diploid individuals) corresponds to a more recently established population having colonized northern environments in the last 100,000 years.
Fig 3
Fig 3. Correlograms illustrating Spearman’s rank correlation coefficients between TE densities in 1 Mb windows and SNP-based statistics such as recombination rate (measured as r/μ, see Methods), pairwise relative (FST) and absolute (dXY) measures of differentiation, and derived SNP frequency in the NEF cluster (DAF).
Correlations with P>0.05 are indicated with a cross.
Fig 4
Fig 4. Boxplots of average TE frequency for each main TE category in the NEF population.
For SNPs, the derived allele frequency was obtained by assigning variants to ancestral and derived states using A. allisoni and A. porcatus.
Fig 5
Fig 5. Plots of average TE frequency against recombination rate computed over 1Mb windows for each main TE clade in the NEF population.
Fig 6
Fig 6. Plots of polymorphic TE density against recombination rate computed over 1Mb windows for each main TE clade in the NEF population.
Fig 7
Fig 7. Plots of fixed TE density against recombination rate computed over 1Mb windows for each main clade in the NEF population.
For Helitron and Hobo, there are not enough fixed insertions.
Fig 8
Fig 8
Top: plots of LINEs (i.e. nLTR-RTs excluding Penelope) length against recombination rate. Middle: Plots of average frequency, density of polymorphic insertions and density of fixed insertions for short LINEs, Bottom: same as middle row, for long LINEs. For middle and bottom plots, average frequencies and densities are computed for 10Mb windows.
Fig 9
Fig 9. Summary of simulations of TEs using SLiM3, using parameters realistic for the NEF cluster. Eight diploid individuals were sampled to mimic our sampling scheme.
Boxplots correspond to the results obtained over 100 simulations of a 4Mb fragment, divided into three regions of 1, 2 and 1 Mb. The first and last Mb correspond to regions of high recombination and high density of functional coding sites (respectively 10 times and 2 times higher than in the 2Mb central region). Coefficients of selection and other parameters are scaled using an effective population size of 1000 instead of 1,000,000 to reduce computation time (see Methods). 2Nes = -10 for 10% of non-coding sites and 2Nes = -100 for 70% of coding sites. Blue and red dotted lines correspond to average derived SNP frequencies in regions of low and high recombination respectively. A: model with constant transposition and no preferential insertion; B: model with a burst of transposition. C and D are the same than A and B respectively, but include preferential insertion in regions of higher recombination such that 70% of new elements go into these regions. TEs that fall in coding regions are strongly deleterious (selection coefficient 2Ns = -2000).
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References

    1. Sotero-Caio CG, Platt RN, Suh A, Ray DA. Evolution and diversity of transposable elements in vertebrate genomes. Genome Biol Evol. 2017;9: 161–177. 10.1093/gbe/evw264 - DOI - PMC - PubMed
    1. Chuong EB, Elde NC, Feschotte C. Regulatory activities of transposable elements: From conflicts to benefits. Nat Rev Genet. 2017;18: 71–86. 10.1038/nrg.2016.139 - DOI - PMC - PubMed
    1. Song MJ, Schaack S. Evolutionary Conflict between Mobile DNA and Host Genomes. Am Nat. 2018;192: 263–273. 10.1086/698482 - DOI - PubMed
    1. Venner S, Feschotte C, Biémont C. Dynamics of transposable elements: towards a community ecology of the genome. Trends Genet. 2009;25: 317–323. 10.1016/j.tig.2009.05.003 - DOI - PMC - PubMed
    1. Brookfield JFY. The ecology of the genome—Mobile DNA elements and their hosts. Nat Rev Genet. 2005;6: 128–136. 10.1038/nrg1524 - DOI - PubMed

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Grants and funding

This work was supported by New York University Abu Dhabi (NYUAD) research funds AD180 (to SB). The NYUAD Sequencing Core is supported by NYUAD Research Institute grant G1205-1205A to the NYUAD Center for Genomics and Systems Biology. The funding bodies had no role in designing the study, nor in data collection and interpretation.