Skip to main content
SpringerLink
Log in

Evolutionary dynamics of transposable elements during silkworm domestication

  • Research Article
  • Published:
Genes & Genomics Aims and scope Submit manuscript

Abstract

Although there are some documented examples on population dynamics of transposable elements (TEs) in model organisms, the evolutionary dynamics of TEs in domesticated species has not been systematically investigated. The objective of this study is to understand population dynamics of TEs during silkworm domestication. In this work, using transposon-display we examined the polymorphism of seven TE families [they represent about 59% of silkworm (Bombyx mori) total TE content] in four domesticated silkworm populations and one wild silkworm population. Maximum likelihood (ML) was used to estimate selection pressure. Population differentiation and structure were performed by using AMOVA analysis and program DISTRUCT, respectively. The results of transposon-display showed that significant differentiation occurred between the domesticated silkworm and wild silkworm. These TEs have experienced expansions and fixation in the domesticated silkworm but not in wild silkworm. Furthermore, the ML results indicated that purifying selection of TEs in the domesticated silkworm were significantly weaker than that in the wild silkworm. Interestingly, an adaptation insertion induced by BmMITE-2 was found, and this insertion can reduce the polymorphism of the flanking regions of its neighboring COQ7 gene. Our results suggested that TEs expanded and were fixed in the domesticated silkworm might result from demographic effects and artificial selection during domestication. We concluded that the data presented in this study have general implication in animal and crop improvements as well as in domestication of new species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bartolome C, Maside X (2004) The lack of recombination drives the fixation of transposable elements on the fourth chromosome of Drosophila melanogaster. Genet Res 83:91–100

    Article  CAS  PubMed  Google Scholar 

  • Boissinot S, Davis J, Entezam A, Petrov D, Furano AV (2006) Fitness cost of LINE-1 (L1) activity in humans. Proc Natl Acad Sci USA 103:9590–9594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouck A, Peeler R, Arnold ML, Wessler SR (2005) Genetic mapping of species boundaries in Louisiana irises using IRRE retrotransposon display markers. Genetics 171:1289–1303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bourque G (2009) Transposable elements in gene regulation and in the evolution of vertebrate genomes. Curr Opin Genet Dev 19:607–612

    Article  CAS  PubMed  Google Scholar 

  • Britten RJ (1996) Cases of ancient mobile element DNA insertions that now affect gene regulation. Mol Phylogenet Evol 5:13–17

    Article  CAS  PubMed  Google Scholar 

  • Brosius J (2003) The contribution of RNAs and retroposition to evolutionary novelties. Genetica 118:99–116

    Article  CAS  PubMed  Google Scholar 

  • Casa AM et al (2000) The MITE family Heartbreaker (Hbr): molecular markers in maize. Proc Natl Acad Sci USA 97:10083–10089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charlesworth B, Charlesworth D (1983) The population-dynamics of transposable elements. Genet Res 42:1–27

    Article  Google Scholar 

  • Charlesworth D, Charlesworth B (1995) Transposable elements in inbreeding and outbreeding populations. Genetics 140:415–417

    CAS  PubMed  PubMed Central  Google Scholar 

  • Charlesworth B, Langley CH (1989) The population-genetics of drosophila transposable elements. Annu Rev Genet 23:251–287

    Article  CAS  PubMed  Google Scholar 

  • Cornman RS, Arnold ML (2007) Phylogeography of Iris missouriensis (Iridaceae) based on nuclear and chloroplast markers. Mol Ecol 16:4585–4598

    Article  CAS  PubMed  Google Scholar 

  • De Keukeleire P et al (2001) Analysis by transposon display of the behavior of the dTph1 element family during ontogeny and inbreeding of Petunia hybrida. Mol Genet Genomics 265:72–81

    Article  PubMed  Google Scholar 

  • de Koning APJ, Gu WJ, Castoe TA, Batzer MA, Pollock DD (2011) Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet 7:e1002384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Douzery E, Randi E (1997) The mitochondrial control region of Cervidae: evolutionary patterns and phylogenetic content. Mol Biol Evol 14:1154–1166

    Article  CAS  PubMed  Google Scholar 

  • Duret L, Marais G, Biemont C (2000) Transposons but not retrotransposons are located preferentially in regions of high recombination rate in Caenorhabditis elegans. Genetics 156:1661–1669

    CAS  PubMed  PubMed Central  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes—application to human mitochondrial-DNA restriction data. Genetics 131:479–491

    CAS  PubMed  PubMed Central  Google Scholar 

  • Feschotte C (2008) Opinion—transposable elements and the evolution of regulatory networks. Nat Rev Genet 9:397–405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gherman A et al (2007) Population bottlenecks as a potential major shaping force of human genome architecture. PLoS Genet 3:1223–1231

    Article  CAS  Google Scholar 

  • Gonzalez J, Lenkov K, Lipatov M, Macpherson JM, Petrov DA (2008) High rate of recent transposable element-induced adaptation in Drosophila melanogaster. PLoS Biol 6:2109–2129

    Article  CAS  Google Scholar 

  • Gonzalez J, Macpherson JM, Messer PW, Petrov DA (2009) Inferring the strength of selection in drosophila under complex demographic models. Mol Biol Evol 26:513–526

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez J, Karasov TL, Messer PW, Petrov DA (2010) Genome-wide patterns of adaptation to temperate environments associated with transposable elements in Drosophila. PLoS Genet 6:e1000905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gray MM, Sutter NB, Ostrander EA, Wayne RK (2010) The IGF1 small dog haplotype is derived from Middle Eastern grey wolves. BMC Biol 8:16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han MJ et al (2010) Burst expansion, distribution and diversification of MITEs in the silkworm genome. BMC Genom 11:520

    Article  CAS  Google Scholar 

  • Kazazian HH Jr (2004) Mobile elements: drivers of genome evolution. Science 303:1626–1632

    Article  CAS  PubMed  Google Scholar 

  • Kwon SJ, Park KC, Kim JH, Lee JK, Kim NS (2005) Rim 2/Hipa CACTA transposon display; a new genetic marker technique in Oryza species. BMC Genet 6:15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le Rouzic A, Deceliere G (2005) Models of the population genetics of transposable elements. Genet Res 85:171–181

    Article  CAS  PubMed  Google Scholar 

  • Le Rouzic A, Boutin TS, Capy P (2007) Long-term evolution of transposable elements. Proc Natl Acad Sci USA 104:19375–19380

    Article  PubMed  PubMed Central  Google Scholar 

  • Lockton S, Gaut BS (2010) The evolution of transposable elements in natural populations of self-fertilizing Arabidopsis thaliana and its outcrossing relative Arabidopsis lyrata. BMC Evol Biol 10:10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lockton S, Ross-Ibarra J, Gaut BS (2008) Demography and weak selection drive patterns of transposable element diversity in natural populations of Arabidopsis lyrata. Proc Natl Acad Sci USA 105:13965–13970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma JX, Devos KM, Bennetzen JL (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 14:860–869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marbois BN, Clarke CF (1996) The COQ7 gene encodes a protein in saccharomyces cerevisiae necessary for ubiquinone biosynthesis. J Biol Chem 271:2995–3004

    Article  CAS  PubMed  Google Scholar 

  • Marino-Ramirez L, Lewis KC, Landsman D, Jordan IK (2005) Transposable elements donate lineage-specific regulatory sequences to host genomes. Cytogenet Genome Res 110:333–341

    Article  CAS  PubMed  Google Scholar 

  • Meyers BC, Tingley SV, Morgante M (2001) Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res 11:1660–1676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mita K et al (2004) The genome sequence of silkworm, Bombyx mori. DNA Res 11:27–35

    Article  CAS  PubMed  Google Scholar 

  • Morgan MT (2001) Transposable element number in mixed mating populations. Genet Res 77:261–275

    Article  CAS  PubMed  Google Scholar 

  • Nagaraja GM, Nagaraju J (1995) Genome fingerprinting of the silkworm, Bombyx mori, using random arbitrary primers. Electrophoresis 16:1633–1638

    Article  CAS  PubMed  Google Scholar 

  • Naito K et al (2006) Dramatic amplification of a rice transposable element during recent domestication. Proc Natl Acad Sci USA 103:17620–17625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neafsey DE, Blumenstiel JP, Hartl DL (2004) Different regulatory mechanisms underlie similar transposable element profiles in pufferfish and fruitflies. Mol Biol Evol 21:2310–2318

    Article  CAS  PubMed  Google Scholar 

  • Nuzhdin SV (1999) Sure facts, speculations, and open questions about the evolution of transposable element copy number. Genetica 107(1–3):129–137

    Article  CAS  PubMed  Google Scholar 

  • Osanai-Futahashi M, Suetsugu Y, Mita K, Fujiwara H (2008) Genome-wide screening and characterization of transposable elements and their distribution analysis in the silkworm, Bombyx mori. Insect Biochem Mol Biol 38:1046–1057

    Article  CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol 6:288–295

    Article  Google Scholar 

  • Petrov DA, Aminetzach YT, Davis JC, Bensasson D, Hirsh AE (2003) Size matters: non-LTR retrotransposable elements and ectopic recombination in Drosophila. Mol Biol Evol 20:880–892

    Article  CAS  PubMed  Google Scholar 

  • Petrov DA, Fiston-Lavier AS, Lipatov M, Lenkov K, Gonzalez J (2011) Population genomics of transposable elements in Drosophila melanogaster. Mol Biol Evol 28:1633–1644

    Article  CAS  PubMed  Google Scholar 

  • Posada D (2006) ModelTest server: a web-based tool for the statistical selection of models of nucleotide substitution online. Nucleic Acids Res 34:W700-W703

    Article  PubMed Central  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol 4:137–138

    Article  Google Scholar 

  • Saccone C, Pesole G, Sbisá E (1991) The main regulatory region of mammalian mitochondrial DNA: structure-function model and evolutionary pattern. J Mol Evol 33:83–91

    Article  CAS  PubMed  Google Scholar 

  • Sakudoh T et al (2007) Carotenoid silk coloration is controlled by a carotenoid-binding protein, a product of the Yellow blood gene. Proc Natl Acad Sci USA 104:8941–8946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanmiguel P, Bennetzen JL (1998) Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Ann Bot 82:37–44

    Article  CAS  Google Scholar 

  • Stenmark P et al (2001) A new member of the family of di-iron carboxylate proteins—Coq7 (clk-1), a membrane-bound hydroxylase involved in ubiquinone biosynthesis. J Biol Chem 276:33297–33300

    Article  CAS  PubMed  Google Scholar 

  • Studer A, Zhao Q, Ross-Ibarra J, Doebley J (2011) Identification of a functional transposon insertion in the maize domestication gene tb1. Nat Genet 43:1160-U1164

    Article  CAS  Google Scholar 

  • Sun W, Shen YH, Han MJ, Cao YF, Zhang Z (2014) An adaptive transposable element insertion in the regulatory region of the EO gene in the domesticated silkworm, Bombyx mori. Mol Biol Evol 31:3302–3313

    Article  CAS  PubMed  Google Scholar 

  • The International Silkworm Genome Consortium (2008) The genome of a lepidopteran model insect, the silkworm Bombyx mori. Insect Biochem Mol Biol 38:1036–1045

    Article  CAS  Google Scholar 

  • Valizadeh P, Crease TJ (2008) The association between breeding system and transposable element dynamics in Daphnia pulex. J Mol Evol 66:643–654

    Article  CAS  PubMed  Google Scholar 

  • Van den Broeck D et al (1998) Transposon display identifies individual transposable elements in high copy number lines. Plant J 13:121–129

    PubMed  Google Scholar 

  • Vicient CM et al (1999) Retrotransposon BARE-1 and its role in genome evolution in the genus Hordeum. Plant Cell 11:1769–1784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vitte C, Panaud O, Quesneville H (2007) LTR retrotransposons in rice (Oryza sativa, L.): recent burst amplifications followed by rapid DNA loss. BMC Genom 8:218

    Article  CAS  Google Scholar 

  • Wright SI, Schoen DJ (1999) Transposon dynamics and the breeding system. Genetica 107:139–148

    Article  CAS  PubMed  Google Scholar 

  • Wright SI, Le QH, Schoen DJ, Bureau TE (2001) Population dynamics of an Ac-like transposable element in self- and cross-pollinating arabidopsis. Genetics 158:1279–1288

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xia Q et al (2004) A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306:1937–1940

    Article  PubMed  Google Scholar 

  • Xu HE et al (2013) BmTEdb: a collective database of transposable elements in the silkworm genome. Database: bat055

  • Yang Q et al (2013) CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize. Proc Natl Acad Sci USA 110:16969–16974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SY, Han MJ, Kang LF, Li ZW, Shen YH, Zhang Z (2014) Demographic history and gene flow during silkworm domestication. BMC Evol Biol 14:185

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Dr. Zhou-He Du for his help in collecting wild silkworm samples and Dr. Fang-Yin Dai for his help in collecting domesticated silkworm samples. This work was supported by Fundamental and Advanced Research Project of Chongqing Municipality (No. cstc2016jcyjA0258 to MJH), the National Natural Science Foundation of China (No. 31401106 to MJH and No. 31560308 and 31700318 to HHZ), the Natural Science Foundation of Jiangxi Province (No. 20171BAB204016 to HHZ), Fundamental Research Funds for the Central Universities (SWU115035 to MJH), the China Postdoctoral Science Foundation (No. 2017M612891 to HHZ) and State Key Laboratory of Silkworm Genome Biology (No. sklsgb161718-8 to HHZ).

Author information

Author notes

  1. Min-Jin Han and Hong-En Xu have contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Silkworm Genome Biology, Key Laboratory for Sericulture Functional Genomics and Biotechnology of Agricultural Ministry, Southwest University, Chongqing, 400715, China

    Min-Jin Han

  2. Zhengzhou University, Zhengzhou, China

    Hong-En Xu

  3. Clinical Medical College, Jiujiang University, Jiujiang, 332000, China

    Xiao-Min Xiong

  4. College of Pharmacy and Life Science, Jiujiang University, Jiujiang, 332000, China

    Hua-Hao Zhang

Authors
  1. Min-Jin Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hong-En Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiao-Min Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hua-Hao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

HHZ, MJH and HEX designed the study. MJH, HEX, HHZ and XMX performed the experiments. MJH and HEX analyzed the data. HHZ and MJH drafted and revised the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Hua-Hao Zhang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1—The Schematic of TE display and the result of typhoon scanning (PDF 611 KB)

Fig. S2—The graph of Bm1 bands (pooled all 16 adapter primers). (PDF 732 KB)

Fig. S3—The graph of Bmmar1 bands (pooled all 16 adapter primers). (PDF 544 KB)

Fig. S4—The graph of CR1 bands (pooled all 16 adapter primers) (PDF 572 KB)

Fig. S5—The graph of BmMITE-2 bands (pooled all 16 adapter primers). (PDF 720 KB)

Fig. S6—The graph of Jockey bands (pooled all 16 adapter primers) (PDF 639 KB)

Fig. S7—The graph of BmMITE-7 bands (pooled all 16 adapter primers) (PDF 271 KB)

Fig. S8—The graph of Pao bands (pooled all 16 adapter primers) (PDF 254 KB)

Fig. S9—AMOVA ΦPT measures for each TE family of each pairwise population comparison. (PDF 188 KB)

13258_2018_713_MOESM10_ESM.pdf

Fig. S10—Likelihood curves and values of Nes. (A) Likelihood curves of Nes for domesticated silkworm population. Each color curve is representing one domesticated silkworm population. On each curve, the maximum likelihood Nes is showed. (B) Likelihood curves of Nes for wild silkworm population. The maximum likelihood Nes is showed. (C) The maximum likelihood Nes and 95% confidence intervals of each TE family in each population is showed (PDF 376 KB)

13258_2018_713_MOESM11_ESM.pdf

Fig. S11—Gels for detecting strains of BmMITE-2 present or absent in the domesticated silkworm. 1-23 represents DaoZao, ShangSanHuBan, DaoZaoN, FangSi, JiaQiu, DiWuBaiLuan, JianPuZhai, TuZhong-01, 655, ReHei, C108N, LuoSa8,DaXianTuZhong, HuangBo, WenZhouDiFangZhong, XuYiZhong, GaoHua, GaoBai, 872, J115, Fa408, YinDuZhong, Ou18, M represent DNA marker (PDF 417 KB)

13258_2018_713_MOESM12_ESM.pdf

Fig. S12—The phylogenetic tree was reconstructed by Bayesian approach. The phylogenetic tree was reconstructed based on sequences of CR regions for mitochondrial DNA. The red triangles represents strains that the BmMITE-2 present in the 3’UTR of COQ7 gene (NM001099608), others represents strains that the BmMITE-2 absent at this site. (PDF 347 KB)

Table S1—All stains used in this study (DOC 46 KB)

Table S2—TEs composition of silkworm (DOC 46 KB)

Table S3—All primers used in this study (DOC 78 KB)

Table S4—The mean TE allele frequency for each TE in each population (DOC 36 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Han, MJ., Xu, HE., Xiong, XM. et al. Evolutionary dynamics of transposable elements during silkworm domestication. Genes Genom 40, 1041–1051 (2018). https://doi.org/10.1007/s13258-018-0713-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13258-018-0713-1

Keywords

Search

Navigation