Hyperdiverse Gene Cluster in Snail Host Conveys Resistance to Human Schistosome Parasites

Type Article
Date 2015-03
Language English
Author(s) Tennessen Jacob A.1, Theron Andre2, Marine Melanie1, Yeh Jan-Ying1, Rognon Anne2, Blouin Michael S.1
Affiliation(s) 1 : Oregon State Univ, Dept Integrat Biol, Corvallis, OR 97331 USA.
2 : Univ Perpignan, CNRS, UMR 5244, Ecol & Evolut Interact 2EI, F-66025 Perpignan, France.
Source Plos Genetics (1553-7404) (Public Library Science), 2015-03 , Vol. 11 , N. 3 , P. e1005067 (21p.)
DOI 10.1371/journal.pgen.1005067
WOS© Times Cited 48

Schistosomiasis, a neglected global pandemic, may be curtailed by blocking transmission of the parasite via its intermediate hosts, aquatic snails. Elucidating the genetic basis of snail-schistosome interaction is a key to this strategy. Here we map a natural parasite-resistance polymorphism from a Caribbean population of the snail Biomphalaria glabrata. In independent experimental evolution lines, RAD genotyping shows that the same genomic region responds to selection for resistance to the parasite Schistosoma mansoni. A dominant allele in this region conveys an 8-fold decrease in the odds of infection. Fine-mapping and RNA-Seq characterization reveal a <1Mb region, the Guadeloupe Resistance Complex (GRC), with 15 coding genes. Seven genes are single-pass transmembrane proteins with putative immunological roles, most of which show strikingly high nonsynonymous divergence (5-10%) among alleles. High linkage disequilibrium among three intermediate-frequency (>25%) haplotypes across the GRC, a significantly non-neutral pattern, suggests that balancing selection maintains diversity at the GRC. Thus, the GRC resembles immune gene complexes seen in other taxa and is likely involved in parasite recognition. The GRC is a potential target for controlling transmission of schistosomiasis, including via genetic manipulation of snails.

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Publisher's official version 21 616 KB Open access
S1 Fig. Expression of genes comprising the Guadeloupe Resistance Complex (GRC) in parasite-unchallenged snails. 1 234 KB Open access
S2 Fig. Expression of genes comprising the Guadeloupe Resistance Complex (GRC) in parasite-challenged snails. 1 266 KB Open access
S1 Table. Selection for parasite resistance. 21 KB Open access
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