Abstract
The Silk Road, which derives its name from the trade of silk produced by the domestic silkworm Bombyx mori, was an important episode in the development and interaction of human civilizations. However, the detailed history behind silkworm domestication remains ambiguous, and little is known about the underlying genetics with respect to important aspects of its domestication. Here, we reconstruct the domestication processes and identify selective sweeps by sequencing 137 representative silkworm strains. The results present an evolutionary scenario in which silkworms may have been initially domesticated in China as trimoulting lines, then subjected to independent spreads along the Silk Road that gave rise to the development of most local strains, and further improved for modern silk production in Japan and China, having descended from diverse ancestral sources. We find that genes with key roles in nitrogen and amino acid metabolism may have contributed to the promotion of silk production, and that circadian-related genes are generally selected for their adaptation. We additionally identify associations between several candidate genes and important breeding traits, thereby advancing the applicable value of our resources.
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References
Larson, G. & Fuller, D. Q. The evolution of animal domestication. Annu. Rev. Ecol. Evol. Syst. 45, 115–136 (2014).
Jensen, P. Behavior genetics and the domestication of animals. Annu. Rev. Anim. Biosci. 2, 85–104 (2014).
Wang, G.-D., Xie, H.-B., Peng, M.-S., Irwin, D. & Zhang, Y.-P. Domestication genomics: evidence from animals. Annu. Rev. Anim. Biosci. 2, 65–84 (2014).
Huang, X. et al. A map of rice genome variation reveals the origin of cultivated rice. Nature 490, 497–501 (2012).
Hufford, M. B. et al. Comparative population genomics of maize domestication and improvement. Nat. Genet. 44, 808–811 (2012).
Qi, J. et al. A genomic variation map provides insights into the genetic basis of cucumber domestication and diversity. Nat. Genet. 45, 1510–1515 (2013).
Zhou, Z. et al. Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nat. Biotechnol. 33, 408–414 (2015).
Mascher, M. et al. Genomic analysis of 6,000-year-old cultivated grain illuminates the domestication history of barley. Nat. Genet. 48, 1089–1093 (2016).
Lin, T. et al. Genomic analyses provide insights into the history of tomato breeding. Nat. Genet. 46, 1220–1226 (2014).
Arunkumar, K. P., Metta, M. & Nagaraju, J. Molecular phylogeny of silkmoths reveals the origin of domesticated silkmoth, Bombyx mori from Chinese Bombyx mandarina and paternal inheritance of Antheraea proylei mitochondrial DNA. Mol. Phylogenet. Evol. 40, 419–427 (2006).
Xia, Q. et al. Complete resequencing of 40 genomes reveals domestication events and genes in silkworm (Bombyx). Science 326, 433–436 (2009).
Peter, B. M. & Slatkin, M. Detecting range expansions from genetic data. Evolution 67, 3274–3289 (2013).
Pickrell, J. K. & Pritchard, J. K. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 8, e1002967 (2012).
Patterson, N. et al. Ancient admixture in human history. Genetics 192, 1065–1093 (2012).
Schiffels, S. & Durbin, R. Inferring human population size and separation history from multiple genome sequences. Nat. Genet. 46, 919–925 (2014).
Hirayama, C. & Nakamura, M. Regulation of glutamine metabolism during the development of Bombyx mori larvae. Biochim. Biophys. Acta 1571, 131–137 (2002).
Osanai, M., Okudaira, M., Naito, J., Demura, M. & Asakura, T. Biosynthesis of l-alanine, a major amino acid of fibroin in Samia cynthia ricini. Insect Biochem. Mol. Biol. 30, 225–232 (2000).
Hirayama, C., Konno, K. & Shinbo, H. The pathway of ammonia assimilation in the silkworm, Bombyx mori. J. Insect Physiol. 43, 959–964 (1997).
Sasaki, T., Kawamura, M. & Ishikawa, H. Nitrogen recycling in the brown planthopper, Nilaparvata lugens: involvement of yeast-like endosymbionts in uric acid metabolism. J. Insect Physiol. 42, 125–129 (1996).
Krall, A. S., Xu, S., Graeber, T. G., Braas, D. & Christofk, H. R. Asparagine promotes cancer cell proliferation through use as an amino acid exchange factor. Nat. Commun. 7, 11457 (2016).
Li, Z. et al. Amino acid deprivation-induced expression of asparagine synthetase regulates the growth and survival of cultured silkworm cells. Arch. Insect Biochem. Physiol. 83, 57–68 (2013).
Tardito, S. et al. Glutamine synthetase activity fuels nucleotide biosynthesis and supports growth of glutamine-restricted glioblastoma. Nat. Cell Biol. 17, 1556–1568 (2015).
Xia, Q., Li, S. & Feng, Q. Advances in silkworm studies accelerated by the genome sequencing of Bombyx mori. Annu. Rev. Entomol. 59, 513–536 (2014).
Otto-Ślusarczyk, D., Graboń, W. & Mielczarek-Puta, M. Aspartate aminotransferase—key enzyme in the human systemic metabolism. Postepy Hig. Med. Dosw. (Online) 70, 219–230 (2016).
Muller, N. A. et al. Domestication selected for deceleration of the circadian clock in cultivated tomato. Nat. Genet. 48, 89–93 (2016).
Young, M. W. & Kay, S. A. Time zones: a comparative genetics of circadian clocks. Nat. Rev. Genet. 2, 702–715 (2001).
Denlinger, D. L., Hahn, D. A., Merlin, C., Holzapfel, C. M. & Bradshaw, W. E. Keeping time without a spine: what can the insect clock teach us about seasonal adaptation? Phil. Trans. R. Soc. B 372, 20160257 (2017).
Bodenstein, C., Gosak, M., Schuster, S., Marhl, M. & Perc, M. Modeling the seasonal adaptation of circadian clocks by changes in the network structure of the suprachiasmatic nucleus. PLoS Comput. Biol. 8, e1002697 (2012).
Erion, R. & Sehgal, A. Regulation of insect behavior via the insulin-signaling pathway. Front. Physiol. 4, 353 (2013).
Zhan, S., Merlin, C., Boore, J. L. & Reppert, S. M. The monarch butterfly genome yields insights into long-distance migration. Cell 147, 1171–1185 (2011).
Xu, H.-J. et al. Two insulin receptors determine alternative wing morphs in planthoppers. Nature 519, 464–467 (2015).
Sim, C. & Denlinger, D. L. Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens. Proc. Natl Acad. Sci. USA 105, 6777–6781 (2008).
Sakano, D., Furusawa, T., Sugimura, Y., Storey, J. M. & Storey, K. B. Metabolic shifts in carbohydrate metabolism during embryonic development of non-diapause eggs of the silkworm, Bombyx mori. J. Insect Biotechnol. Sericol. 73, 15–22 (2004).
Chino, H. Carbohydrate metabolism in diapause egg of the silkworm, Bombyx mori. Dev. Growth Differ. 3, 295–316 (1957).
Lee, J. C. et al. Genome-wide association study identifies distinct genetic contributions to prognosis and susceptibility in Crohn’s disease. Nat. Genet. 49, 262–268 (2017).
Yano, K. et al. Genome-wide association study using whole-genome sequencing rapidly identifies new genes influencing agronomic traits in rice. Nat. Genet. 48, 927–934 (2016).
Nicola, N. et al. Genome-wide analysis identifies 12 loci influencing human reproductive behavior. Nat. Genet. 48, 1–7 (2016).
Sakudoh, T. et al. 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 (2007).
Yoda, S. et al. The transcription factor Apontic-like controls diverse colouration pattern in caterpillars. Nat. Commun. 5, 4936 (2014).
Ito, K. et al. Deletion of a gene encoding an amino acid transporter in the midgut membrane causes resistance to a Bombyx parvo-like virus. Proc. Natl Acad. Sci. USA 105, 7523–7527 (2008).
Gupta, T., Kadono-Okuda, K., Ito, K., Trivedy, K. & Ponnuvel, K. M. Densovirus infection in silkworm Bombyx mori and genes associated with disease resistance. Invertebr. Surviv. J. 12, 118–128 (2015).
Sakudoh, T. et al. Diversity in copy number and structure of a silkworm morphogenetic gene as a result of domestication. Genetics 187, 965–976 (2011).
Abiko, T. et al. Changes in nitrogen assimilation, metabolism, and growth in transgenic rice plants expressing a fungal NADP (H)-dependent glutamate dehydrogenase (gdhA). Planta 232, 299–311 (2010).
Zhou, Y. et al. Over-expression of aspartate aminotransferase genes in rice resulted in altered nitrogen metabolism and increased amino acid content in seeds. Theor. Appl. Genet. 118, 1381–1390 (2009).
Lin, T. et al. Genomic analyses provide insights into the history of tomato breeding. Nat. Genet. 46, 1220–1226 (2014).
Rubin, C. J. et al. Whole-genome resequencing reveals loci under selection during chicken domestication. Nature 464, 587–591 (2010).
Wiener, P. & Wilkinson, S. Deciphering the genetic basis of animal domestication. Proc. Biol. Sci. 278, 3161–3170 (2011).
Dong, Y. et al. Sequencing and automated whole-genome optical mapping of the genome of a domestic goat (Capra hircus). Nat. Biotechnol. 31, 135–141 (2013).
Pennisi, E. The biology of genomes. On the trail of brain domestication genes. Science 332, 1030–1031 (2011).
Grimm, D. Animal domestication. The genes that turned wildcats into kitty cats. Science 346, 799 (2014).
Li, Y. et al. Domestication of the dog from the wolf was promoted by enhanced excitatory synaptic plasticity: a hypothesis. Genome Biol. Evol. 6, 3115–3121 (2014).
Moon, S. et al. A genome-wide scan for signatures of directional selection in domesticated pigs. BMC Genom. 16, 130 (2015).
Carneiro, M. et al. Rabbit genome analysis reveals a polygenic basis for phenotypic change during domestication. Science 345, 1074–1079 (2014).
Consortium, I. S. G. The genome of a lepidopteran model insect, the silkworm Bombyx mori. Insect Biochem. Mol. Biol. 38, 1036–1045 (2008).
Luo, R. et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1, 18 (2012).
Elsik, C. G. et al. Creating a honey bee consensus gene set. Genome Biol. 8, R13 (2007).
Duan, J. et al. SilkDBv2.0: a platform for silkworm (Bombyx mori) genome biology. Nucleic Acids Res. 38, D453–D456 (2010).
Stanke, M., Tzvetkova, A. & Morgenstern, B. AUGUSTUS at EGASP: using EST, protein and genomic alignments for improved gene prediction in the human genome. Genome Biol. 7, S11.1–S11.8 (2006).
Korf, I. Gene finding in novel genomes. BMC Bioinform. 5, 59 (2004).
Burge, C. & Karlin, S. Prediction of complete gene structures in human genomic DNA. J. Mol. Biol. 268, 78–94 (1997).
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
DePristo, M. A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491–498 (2011).
Patterson, N., Price, A. L. & Reich, D. Population structure and eigenanalysis. PLoS Genet. 2, e190 (2006).
Zhan, S. et al. The genetics of monarch butterfly migration and warning colouration. Nature 514, 317–321 (2014).
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729 (2013).
Tang, H., Peng, J., Wang, P. & Risch, N. J. Estimation of individual admixture: analytical and study design considerations. Genet. Epidemiol. 28, 289–301 (2005).
Keightley, P. D. et al. Estimation of the spontaneous mutation rate in Heliconius melpomene. Mol. Biol. Evol. 32, 239–243 (2014).
Barrett, J. C., Fry, B., Maller, J. & Daly, M. J. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263–265 (2004).
Chen, H., Patterson, N. & Reich, D. Population differentiation as a test for selective sweeps. Genome Res. 20, 393–402 (2010).
Nielsen, R. et al. Genomic scans for selective sweeps using SNP data. Genome Res. 15, 1566–1575 (2005).
Yu, H. S. et al. Evidence of selection at melanin synthesis pathway loci during silkworm domestication. Mol. Biol. Evol. 28, 1785–1799 (2011).
Sun, W., Shen, Y. H., Han, M. J., Cao, Y. F. & Zhang, Z. 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 (2014).
Wang, Y. et al. The CRISPR/Cas system mediates efficient genome engineering in Bombyx mori. Cell Res. 23, 1414–1416 (2013).
Kang, H. M. et al. Variance component model to account for sample structure in genome-wide association studies. Nat. Genet. 42, 348–354 (2010).
Gnerre, S. et al. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc. Natl Acad. Sci. USA 108, 1513–1518 (2011).
Boetzer, M., Henkel, C. V., Jansen, H. J., Butler, D. & Pirovano, W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27, 578–579 (2010).
Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
Acknowledgements
We thank X. Huang, S. Xu and K. Wang for discussion on the evolutionary analyses, X. Hu, W. Wang, A. Wang, H. Liu, Q. Li and J. Lian for early contributions to the wild silkworm genome sequencing, and L. Chen and X. Wang for assistance with DNA preparation. The research was supported by the National Key Basic Research (973) Program in China (grant 2013CB835200), National Science Foundation of China (grants 31522053, 91631103, 31672370, 31501877 and 31371286), Chinese Academy of Sciences programme (grant 173176001000162007) and Thousand Talents Program of China (to S.Z.).
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W.W., S.Z. and H.X. conceived the project. S.Z. and H.X. designed the studies. A.X., H.Q. and M.L. provided silkworm strains. M.L. performed phenotyping. H.X. and L.L. prepared the DNA. S.Z. led the analyses. S.Z., H.X., X.L. and G.F. performed the analyses. H.X. annotated and interpreted the selective sweeps. Y.Z., L.W., L.L., Y.C. and X.L. performed the functional experiments. S.Z., H.X. and X.L. wrote the manuscript. W.W. improved the manuscript. Affiliations are sorted based on the numerical order in the author list.
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Xiang, H., Liu, X., Li, M. et al. The evolutionary road from wild moth to domestic silkworm. Nat Ecol Evol 2, 1268–1279 (2018). https://doi.org/10.1038/s41559-018-0593-4
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DOI: https://doi.org/10.1038/s41559-018-0593-4
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