Evidence of Selection at Melanin Synthesis Pathway Loci during Silkworm Domestication

Abstract

The domesticated silkworm (Bombyx mori) was domesticated from wild silkworm (Bombyx mandarina) more than 5,000 years ago. During domestication, body color between B. mandarina and B. mori changed dramatically. However, the molecular mechanism of the silkworm body color transition is not known. In the present study, we examined within-and between-species nucleotide diversity for eight silkworm melanin synthesis pathway genes, which play a key role in cuticular pigmentation of insects. Our results showed that the genetic diversity of B. mori was significantly lower than that of B. mandarina and 40.7% of the genetic diversity of wild silkworm was lost in domesticated silkworm. We also examined whether position effect exists among melanin synthesis pathway genes in B. mandarina and B. mori. We found that the upstream genes have significantly lower levels of genetic diversity than the downstream genes, supporting a functional constraint hypothesis (FCH) of metabolic pathway, that is, upstream enzymes are under greater selective constraint than downstream enzymes because upstream enzymes participate in biosynthesis of a number of metabolites. We also investigated whether some of the melanin synthesis pathway genes experienced selection during domestication. Neutrality test, coalescent simulation, as well as network and phylogenetic analyses showed that tyrosine hydroxylase (TH) gene was a domestication locus. Sequence analysis further suggested that a putative expression enhancer (Abd-B-binding site) in the intron of TH gene might be disrupted during domestication. TH is the rate-limiting enzyme of melanin synthesis pathway in insects. Real-time polymerase chain reaction assay did show that the relative expression levels of TH gene in B. mori were significantly lower than that in B. mandarina at three different developmental stages, which is consistent with light body color of domesticated silkworm relative to wild silkworm. Therefore, we speculated that expression change of TH gene may contribute to the body color transition from B. mandarina to B. mori. Our results emphasize the exceptional role of gene expression regulation in morphological transition of domesticated animals.

Little gene flow between domestic silkmoth <i>Bombyx mori</i> and its wild relative <i>Bombyx mandarina</i> in Japan, and possible artificial selection on the <i>CAD</i> gene of <i>B. mori</i>

“…Guo et al (2011) demonstrated that a marked decrease in π value of B. mori Def A gene relative to that of Chinese B. mandarina supported that the Def A gene was under artificial selection during domestication. A similar result was presented by Yu et al (2011). The present result is consistent with those of Guo et al (2011) and Yu et al (2011), suggesting that CAD is a candidate gene for silkworm domestication.…”

“…A similar result was presented by Yu et al (2011). The present result is consistent with those of Guo et al (2011) and Yu et al (2011), suggesting that CAD is a candidate gene for silkworm domestication. As described above, the BGIBMGA006816-TA in the Silkworm Genome Database including the CAD gene was not found in the list of genes that represent good candi-dates for domestication genes (Xia et al, 2009) and therefore was considered to be a neutral gene for artificial selection (Xia et al, 2009).…”

“…Based on comparative analysis of B. mori and Chinese and Japanese B. mandarina, we confirmed a significant decrease in genetic variation in the CAD sequence of B. mori. Recently, Yu et al (2011) and Guo et al (2011) reported possible gene targets for silkworm domestication. In these reports, the authors employed the significantly decreased level of genetic variation in B. mori genes or regions compared to those in Chinese B. mandarina as a criterion for the domestication-targeted gene.…”

“…These reports suggest that strong artificial selection occurred during the domestication process because genetic polymorphisms at several loci have been maintained in B. mori (e.g., Kim et al, 2008;Yu et al, 2011). Xia et al (2009) identified possible target genes of silkworm domestication by analyzing 29 B. mori and 11 B. mandarina individuals.…”

Nucleotide sequence variation in mitochondrial COI gene among 147 silkworm (Bombyx mori) strains from Japanese, Chinese, European and moltinism classes

“…When comparing the result with those of nuclear genes, we can use limited amount of information on genetic variation in nuclear genes. For example, Kim et Yu et al (2011) demonstrated that Tyrosine hydroxylase (TH) gene had extremely low amount of nucleotide diversity relative to Chinese B. mandarina. The TH gene was considered to be one of the target genes for silkworm domestication through multiple approaches of population genetic analyses.…”