Divergence at mitochondrial and ribosomal loci indicates the split between Asian and European populations of Trichinella spiralis occurred prior to swine domestication

Authors: Thompson, Peter; BILZKA-ZAJAC, EWA - National Veterinary Research Institute; Zarlenga, Dante; MINGYUAN, LIU - Jilin University; CENCEK, TOMASZ - National Veterinary Research Institute; ROZYICKI, MIROSLAW - National Veterinary Research Institute; Rosenthal, Benjamin

Submitted to: Infection, Genetics and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/2/2021
Publication Date: 1/6/2021
Publication URL: https://handle.nal.usda.gov/10113/7231849
Citation: Thompson, P.C., Bilzka-Zajac, E., Zarlenga, D.S., Mingyuan, L., Cencek, T., Rozyicki, M., Rosenthal, B.M. 2021. Divergence at mitochondrial and ribosomal loci indicates the split between Asian and European populations of Trichinella spiralis occurred prior to swine domestication. Infection, Genetics and Evolution. 88(104705). https://doi.org/10.1016/j.meegid.2021.104705.
DOI: https://doi.org/10.1016/j.meegid.2021.104705

Interpretive Summary: The history of humans and pigs are intertwined, and consequently, so are the parasites that live in pigs. In order to understand whether human domestication of pigs impacted populations of the foodborne parasite Trichinella spiralis, a historical investigation of parasite populations was undertaken. We examined the DNA of Trichinella spiralis from Asia, Europe, and North America for signatures of historical connections. It was found that the most recent connection between Asian and European samples occurred about 500,000 years ago, long before pigs were domesticated from wild boars, while North American isolates are recent descendents of European populations. Thus, previous hypotheses suggesting that European Trichinella spiralis came from Asia along with pigs via trade need to be reevaluated. The current population characteristics of Trichinella spiralis are more dependent on their historical relationship with wild boar than modern agriculture.

Technical Abstract: Available evidence suggests that Trichinella spiralis first originated in Asia and subsequently spread to the rest of the world. Notably limited genetic diversity in European T. spiralis isolates indicates that the parasite went through a dramatic genetic bottleneck at some point in its history. Did this genetic bottleneck result from the transport of a limited number of T. spiralis infected pigs from Asian centers of domestication, or was the parasite resident in Europe far earlier than the domestication of pigs there? In order to explore this hypothesis, we generated complete mitochondrial genomes and ribosomal DNAs from seventeen European T. spiralis isolates, six North American isolates and seven Asian isolates using next generation sequencing. A total of 13,858 base pairs of mitochondrial DNA and 7431 nucleotides of the nuclear ribosomal DNA sequence from each isolate were aligned and subjected to phylogenetic analysis using T. nelsoni and T. patagoniensis as outgroups. We confirmed that North American and European isolates were tightly clustered within a single “western clade” and all Chinese T. spiralis isolates were placed within a well-supported sister clade. These results indicate that European T. spiralis did not directly descend from Chinese parasite populations. Furthermore, the amount of nucleotide divergence between the two clades suggests that they diverged before pigs were domesticated. Over evolutionary time periods, Chinese and European T. spiralis were likely maintained as separate populations. The genetic bottleneck observed in European T. spiralis did not result from a small number of founders introduced with Chinese pigs in the recent past, but derives from an earlier bottleneck in host populations associated with the end of the last glacial maximum.