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. 2019 Feb 12;15(2):e1007900.
doi: 10.1371/journal.pgen.1007900. eCollection 2019 Feb.

Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila

Gabriel E Rech  1 , María Bogaerts-Márquez  1 , Maite G Barrón  1 , Miriam Merenciano  1 , José Luis Villanueva-Cañas  1 , Vivien Horváth  1 , Anna-Sophie Fiston-Lavier  2 , Isabelle Luyten  3 , Sandeep Venkataram  4 , Hadi Quesneville  3 , Dmitri A Petrov  4 , Josefa González  1
Affiliations

Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila

Gabriel E Rech et al. PLoS Genet. .

Abstract

Most of the current knowledge on the genetic basis of adaptive evolution is based on the analysis of single nucleotide polymorphisms (SNPs). Despite increasing evidence for their causal role, the contribution of structural variants to adaptive evolution remains largely unexplored. In this work, we analyzed the population frequencies of 1,615 Transposable Element (TE) insertions annotated in the reference genome of Drosophila melanogaster, in 91 samples from 60 worldwide natural populations. We identified a set of 300 polymorphic TEs that are present at high population frequencies, and located in genomic regions with high recombination rate, where the efficiency of natural selection is high. The age and the length of these 300 TEs are consistent with relatively young and long insertions reaching high frequencies due to the action of positive selection. Besides, we identified a set of 21 fixed TEs also likely to be adaptive. Indeed, we, and others, found evidence of selection for 84 of these reference TE insertions. The analysis of the genes located nearby these 84 candidate adaptive insertions suggested that the functional response to selection is related with the GO categories of response to stimulus, behavior, and development. We further showed that a subset of the candidate adaptive TEs affects expression of nearby genes, and five of them have already been linked to an ecologically relevant phenotypic effect. Our results provide a more complete understanding of the genetic variation and the fitness-related traits relevant for adaptive evolution. Similar studies should help uncover the importance of TE-induced adaptive mutations in other species as well.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Worldwide distribution of D. melanogaster populations used in this study.
Location of the 39 European, 14 North American, five Australian, one Asian, and one African population analyzed in this work. Note that the location of some populations overlap in the map. For more details, see S1 Table. Colors indicate the five major Köppen climate zones [114].
Fig 2
Fig 2. Workflow showing the main steps applied for identifying TEs present at high frequencies in high recombination regions in the D. melanogaster genome.
LRR: TEs located at low recombination rate regions. HRR: TEs located at high recombination rate regions. Fixed: HRR TEs at frequencies > 95% in all populations. LowFreq: low frequency HRR TEs (frequencies < 10% in all samples). HighFreq: high frequency HRR TEs (frequencies < 95% in all samples and at >10% frequency in at least three samples). HighFreq TEs were further classified according to their frequency in African (AF) and/or out-of-Africa (OOA) populations: AF: TEs at high frequency only in the African population; AF-OOA: TEs at high frequency in Africa and out-of-Africa populations; OOA: TEs at high frequency in out-of-Africa populations and low frequency in the African population and NA-AF: TEs present at high frequency in out-of-Africa populations but for which we have no data for the African population.
Fig 3
Fig 3. TE age of the different frequency groups.
A) Top: Boxplots showing the distribution of TE age (terminal branch length) values for each of the categories. Bottom: Zoomed-in version of the boxed area showing the lowest values of the TE age distribution. B) Proportion of young (age < 0.01) and old (age ≥ 0.01) TEs in each category. * p-value < 0.05, *** p-value < 0.001 from Chi-square test.
Fig 4
Fig 4. Number of TEs at different TE length ratios (%).
Bars indicate number of TEs (vertical axis) per bin of TE Length Ratio (%) (horizontal axis) and color shade indicates the proportion of young and old TEs in each bin.
Fig 5
Fig 5. HighFreq TEs with signals of selection.
41 HighFreq TEs showing at least one signal of selection either or both in the selective sweep tests (iHS, H12 or nSL, 36 TEs) or the population differentiation test (FST, 9 TEs). Red and grey circles indicate statistical significance for each TE at each test and population (Significant and No significant, respectively). Empty circles (ND) indicates that the test could not be calculated.
Fig 6
Fig 6. Functional enrichment analysis of genes nearby TEs showing evidence of selection (in this or previous works) and HighFreq TEs.
Bar colors indicates similar biological functions of the DAVID clusters (A) and the fitness-related traits (B): Green: stress response, Red: behavior, Blue: development Yellow: pigmentation. A) Significant gene ontology clusters according to DAVID functional annotation tool (enrichment score > 1.3). For genes nearby HighFreq TEs, only top five clusters are showed. The horizontal axis represent DAVID enrichment score (see S8A and S8B Table for details). B) Significantly overrepresented fitness-related genes according to previous genome association studies. All FDR corrected p-values < 0.05, Chi-square (χ2) test (see S10A and S10B Table for details). The horizontal axis represents the log10(χ2). In both, A) and B), numbers nearby each bar indicate total number of genes in that cluster/category.
Fig 7
Fig 7. Caracteristics of the HighFreq TEs.
A) TE location regarding the nearest gene. B) Location of intragenic TEs. C) TE order. *: p-value < 0.05. ***: p-value < 0.001 (Chi-square test).
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