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Analysis of Blood Fluke Genomes Indicates Parasite Arrived in New World With Slave Trade

NEW YORK (GenomeWeb) – By resequencing the Schistosoma mansoni genome, researchers in the UK were able to trace the human parasite's population history, finding that it likely migrated to the New World with the Atlantic slave trade.

Imperial College London's Joanne Webster and her colleagues amassed whole genome resequencing data for 10 S. mansoni isolates from across Africa and the New World as well as from one S. rodhaini isolate, a related fluke that infects rodents. By comparing the various isolates, the researchers traced the S. mansoni speciation event to the emergence of fishing in Africa some 100,000 years to 150,000 years ago. They further found that West African and Caribbean flukes diverged during the time of the Atlantic slave trade, as the researchers reported this week in Scientific Reports.

"Comparing the S. mansoni genomes suggests that flukes in West Africa split from their Caribbean counterparts at some point between 1117 AD and 1742 AD, which overlaps with the time of the 16th [century to] 19th century Atlantic slave trade," Webster said in a statement. "During this period more than 22,000 African people were transported from West Africa to Guadeloupe by French slave ships, and the fluke was carried with them."

To this day, the blood fluke S. mansoni infects more than 250 million people across the globe, leading to more than 11,000 deaths a year, according to the Wellcome Trust Sanger Institute.

Webster and her colleagues sequenced the genomes of 10 S. mansoni samples — including the NMRI laboratory strain that was used to generate a reference genome in 2009 — and one S. rodhaini isolate to a median 46X coverage, and mapped that sequence data against the S. mansoni reference.

They uncovered between 2 million SNPs in Ugandan isolates and less than a million SNPs in the New World and Senegalese isolates.

Using these SNPs, the researchers sketched out the broad population genetic structure of S. mansoni. Using S. rodhaini as an outgroup, they constructed a maximum likelihood phylogenetic tree that contains a deep split among the S. mansoni isolates. This split separates the Ugandan isolates from the others, while another branch separates out the Cameroon samples. The rest, the researchers noted, fell within a broad clade that included the Senegalese, coastal Kenyan, and all the New World samples.

Then based on a number of population genetics models, Webster and her colleagues traced the S. mansoni and S. rodhaini split back some 126,500 years. This, they noted, indicates that S. mansoni is much younger than was previously thought.

Prior to speciation, they estimated that the ancestor of S. mansoni and S. rodhaini had an effective population size of 425,000, much larger than the present population sizes of either S. mansoni or S. rodhaini.

As the Ugandan isolates are the earliest diverging ones on the maximum likelihood tree and as the isolates from Lake Victoria and Lake Albert harbored the highest number of variants, the researchers suggested that this speciation event likely took place in East Africa.

It also, they noted, corresponds with the adoption of fishing.

"The timing of the separation of the two species coincidences with the first archaeological evidence of fishing in Africa," first author Thomas Crellen from Imperial College London added in a statement. "The parasite develops in freshwater and infects people by burrowing through their skin. The introduction of fishing would have meant that people spent more time in the water, greatly increasing their chances of being infected."

Then, some 5,920 years ago, the Ugandan and Cameroon S. mansoni samples diverged, and the Ugandan and Senegalese samples themselves split about 1,520 years ago, coinciding with a sharp population decline. This movement of S. mansoni across Africa likely reflects human migrations, such as the Bantu expansion, throughout the continent, the researchers said.

Webster and her colleagues also modeled the split between the New World Guadeloupe and West African Senegalese and Cameroon samples to find that they diverged 543 years ago. As the Guadeloupe samples were collected in the field in 1983, that places the split at 1440 AD, with a confidence interval ranging from 1118 AD to 1743 AD — a range that overlaps with the Atlantic slave trade.

Webster and her colleagues also uncovered genes under selection within the S. mansoni genome that appear to have helped it adapt to a human host. By comparing the S. mansoni and S. rodhaini genomes, they uncovered differences in their VAL21 and elastase genes.

"VAL genes produce proteins that cause allergic responses, so it is possible that the variation in VAL21 helps the fluke to hide from our immune systems. The elastase gene helps the parasite to burrow in to the body by breaking down elastin — a major component of human skin," said the Sanger Institute's James Cotton in a statement.