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Genome Sequence Spells Out Lucrative History of Silkworm Domestication

NEW YORK (GenomeWeb) – A team from China has used genome sequencing to explore the evolutionary changes in the once-wild moths that led to the Silk Road — an economically important trade route that boosted interactions between human populations in the East and West.

"The results present an evolutionary scenario in which silkworms may have been initially domesticated in China … 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," corresponding authors Shuai Zhan, Wen Wang, and Anying Xu, at the Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, and Jiangsu University, respectively, wrote with their co-authors.

By resequencing more than 100 domestic silkworm (Bombyx mori) strains and seven wild silkworms from the B. mandarina species, the researchers retraced domestication-related genetic changes and selective sweeps in the silkworm genome, highlighting some of the genes, pathways, and regulatory features contributing to silk production. The telltale changes in the worm genome also helped them gauge some of the directions and dynamics the silk trade took as it spread to different parts of the world.

More broadly, the team's comparative genomic analyses also made it possible to start comparing the sorts of genetic and genomic shifts that contributed to silkworm domestication, relative to documented changes that have taken place in domesticated animals and crop plants.

"As an invertebrate species, the silkworm is unique in its phylogenetic position in the life tree of all domestic species. Correspondingly, we found that linkage disequilibrium decays much more rapidly in silkworms than in other domestic species — both plants and animals — and that the distribution of selective sweeps was fragmented across chromosomes," the authors wrote in their study, which appeared online today in Nature Ecology and Evolution. "Artificial selection may be distributed evenly and the domestication … is more likely to be maintained by a number of loci."

Past research has put the domestication of silkworms at roughly 5,000 years ago, the team noted. But despite some previous sequencing-based efforts to understand the details of this process, the authors noted that "the detailed evolutionary process underlying its domestication has remained unelaborated."

They further explained that "despite broad interest in silkworm domestication, the only well-acknowledged aspect to date is that domesticated silkworms originated form the Chinese wild silkworm Bombyx mandarina."

For their study, the investigators in China and their collaborators at Berry Genomics did paired-end sequencing on 137 domestic silkworm strains and seven wild silkworm representatives using Illumina technology, generating 13-fold coverage of each genome, on average. They then put together a map of variants in the strains, using it to tease out relationships between the strains and ancestral contributions within them.

Along with a distinct phylogenetic split between B. mori and B. mandarina, the investigators saw seven clusters within the domesticated lineage. In China, for example, local silkworm strains were often found at basal phylogenetic positions and fell into three clusters, while improved strains in China and Japan had ancestry differences that appeared to reflect the breeding efforts used to develop them, the team noted.

From still other divergence events, including an early split between strains from China and Europe, the researchers got a glimpse of ancient silk trade interactions. Meanwhile, their analysis of selection pressures in the silkworm genome highlighted hundreds of genes with potential ties to domestication, coming from RNA binding and processing, cell cycle, and other pathways.

In addition to their efforts to follow up on candidate genes with expression profiling, CRISPR-Cas9-based gene knockdown, and other experiments, the team used GWAS to search for SNPs related to specific silkworm phenotypes, particularly variants contributing to disease or insecticide resistance.

"These newly identified loci will not only help strengthen the health of silkworms, but also provide insights into the biological control of lepidopteran pests," the authors wrote.