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The evolution of transposable elements in natural populations of self-fertilizing Arabidopsis thaliana and its outcrossing relative Arabidopsis lyrata.

Lockton S, Gaut BS - BMC Evol. Biol. (2010)

Bottom Line: Here, we collected a large TE-display data set in self-fertilizing Arabidopsis thaliana, and compared it to data gathered in outcrossing Arabidopsis lyrata.Across TE families, we estimated higher allele frequencies and lower selection coefficients on A. thaliana TE insertions relative to A. lyrata TE insertions.There are also species-specific differences that could be attributed to the effects of mating system, including higher overall allele frequencies in the selfing lineage and a greater proportion of among population TE diversity in the outcrossing lineage.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine, USA. slockton@gmail.com

ABSTRACT

Background: Transposable Elements (TEs) make up the majority of plant genomes, and thus understanding TE evolutionary dynamics is key to understanding plant genome evolution. Plant reproductive systems are diverse and mating type variation is one factor among many hypothesized to influence TE evolutionary dynamics. Here, we collected a large TE-display data set in self-fertilizing Arabidopsis thaliana, and compared it to data gathered in outcrossing Arabidopsis lyrata. We analyzed seven TE families in four natural populations of each species to tease apart the effects of mating system, demography, transposition, and selection in determining patterns of TE diversity.

Results: Measures of TE band differentiation were largely consistent across TE families. However, patterns of diversity in A. thaliana Ac elements differed significantly from that other TEs, perhaps signaling a lack of recent transposition. Across TE families, we estimated higher allele frequencies and lower selection coefficients on A. thaliana TE insertions relative to A. lyrata TE insertions.

Conclusions: The differences in TE distributions between the two Arabidopsis species represents a synthesis of evolutionary forces that include the transposition dynamics of individual TE families and the demographic histories of populations. There are also species-specific differences that could be attributed to the effects of mating system, including higher overall allele frequencies in the selfing lineage and a greater proportion of among population TE diversity in the outcrossing lineage.

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Related in: MedlinePlus

Site Frequency Spectra of all pooled TEs ("Pooled"), and each TE family in species-wide samples of A. thaliana (black bordered bars) and A. lyrata (grey bars with grey borders).
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Figure 4: Site Frequency Spectra of all pooled TEs ("Pooled"), and each TE family in species-wide samples of A. thaliana (black bordered bars) and A. lyrata (grey bars with grey borders).

Mentions: AMOVA utilizes TE-display bands, but allele frequencies are often more helpful for evaluating evolutionary dynamics. For TE-display data, a band from an inbred species is more likely to represent a homozygous locus than bands in an outcrossing species. We therefore used independent estimates of the inbreeding coefficient (F) to estimate allele frequencies (pTE) from our TE band data (see Methods). This method intrinsically corrects for possibilities that A. lyrata may not always be obligately outcrossing (e.g., [64]) but does assume a constant rate of selfing in A. thaliana. With pTE estimates, we can examine site frequency spectra (SFS), which form the basis for inferring the strength of selection [65,66]. We combined data across populations to construct species-wide samples. Species-wide, and across all TE families, the A. lyrata median pTE was 0.061, but the A. thaliana median pTE of 0.125 was substantially higher (Table 1; Wilcoxon rank sum test, p = 1.28 × 10-6). In addition to lower median frequencies, the A. lyrata SFS showed a skew towards lower frequency insertions in A. lyrata relative to A. thaliana (Fig. 4). This skew is evident not only for the SFS pooled among TE families, but also for most individual TEs (Fig. 4). The standard interpretation of a left-skewed SFS is that purifying selection acts on deleterious variants, limiting their population frequencies. Thus, the skew in A. lyrata relative to A. thaliana is consistent with stronger selection acting on TEs in A. lyrata, as concluded by Wright et al. [42] for Ac elements alone.


The evolution of transposable elements in natural populations of self-fertilizing Arabidopsis thaliana and its outcrossing relative Arabidopsis lyrata.

Lockton S, Gaut BS - BMC Evol. Biol. (2010)

Site Frequency Spectra of all pooled TEs ("Pooled"), and each TE family in species-wide samples of A. thaliana (black bordered bars) and A. lyrata (grey bars with grey borders).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2837042&req=5

Figure 4: Site Frequency Spectra of all pooled TEs ("Pooled"), and each TE family in species-wide samples of A. thaliana (black bordered bars) and A. lyrata (grey bars with grey borders).
Mentions: AMOVA utilizes TE-display bands, but allele frequencies are often more helpful for evaluating evolutionary dynamics. For TE-display data, a band from an inbred species is more likely to represent a homozygous locus than bands in an outcrossing species. We therefore used independent estimates of the inbreeding coefficient (F) to estimate allele frequencies (pTE) from our TE band data (see Methods). This method intrinsically corrects for possibilities that A. lyrata may not always be obligately outcrossing (e.g., [64]) but does assume a constant rate of selfing in A. thaliana. With pTE estimates, we can examine site frequency spectra (SFS), which form the basis for inferring the strength of selection [65,66]. We combined data across populations to construct species-wide samples. Species-wide, and across all TE families, the A. lyrata median pTE was 0.061, but the A. thaliana median pTE of 0.125 was substantially higher (Table 1; Wilcoxon rank sum test, p = 1.28 × 10-6). In addition to lower median frequencies, the A. lyrata SFS showed a skew towards lower frequency insertions in A. lyrata relative to A. thaliana (Fig. 4). This skew is evident not only for the SFS pooled among TE families, but also for most individual TEs (Fig. 4). The standard interpretation of a left-skewed SFS is that purifying selection acts on deleterious variants, limiting their population frequencies. Thus, the skew in A. lyrata relative to A. thaliana is consistent with stronger selection acting on TEs in A. lyrata, as concluded by Wright et al. [42] for Ac elements alone.

Bottom Line: Here, we collected a large TE-display data set in self-fertilizing Arabidopsis thaliana, and compared it to data gathered in outcrossing Arabidopsis lyrata.Across TE families, we estimated higher allele frequencies and lower selection coefficients on A. thaliana TE insertions relative to A. lyrata TE insertions.There are also species-specific differences that could be attributed to the effects of mating system, including higher overall allele frequencies in the selfing lineage and a greater proportion of among population TE diversity in the outcrossing lineage.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine, USA. slockton@gmail.com

ABSTRACT

Background: Transposable Elements (TEs) make up the majority of plant genomes, and thus understanding TE evolutionary dynamics is key to understanding plant genome evolution. Plant reproductive systems are diverse and mating type variation is one factor among many hypothesized to influence TE evolutionary dynamics. Here, we collected a large TE-display data set in self-fertilizing Arabidopsis thaliana, and compared it to data gathered in outcrossing Arabidopsis lyrata. We analyzed seven TE families in four natural populations of each species to tease apart the effects of mating system, demography, transposition, and selection in determining patterns of TE diversity.

Results: Measures of TE band differentiation were largely consistent across TE families. However, patterns of diversity in A. thaliana Ac elements differed significantly from that other TEs, perhaps signaling a lack of recent transposition. Across TE families, we estimated higher allele frequencies and lower selection coefficients on A. thaliana TE insertions relative to A. lyrata TE insertions.

Conclusions: The differences in TE distributions between the two Arabidopsis species represents a synthesis of evolutionary forces that include the transposition dynamics of individual TE families and the demographic histories of populations. There are also species-specific differences that could be attributed to the effects of mating system, including higher overall allele frequencies in the selfing lineage and a greater proportion of among population TE diversity in the outcrossing lineage.

Show MeSH
Related in: MedlinePlus