A Targeted Capture Linkage Map Anchors the Genome of the Schistosomiasis Vector Snail, Biomphalaria glabrata

Abstract

The aquatic planorbid snail Biomphalaria glabrata is one of the most intensively-studied mollusks due to its role in the transmission of schistosomiasis. Its 916 Mb genome has recently been sequenced and annotated, but it remains poorly assembled. Here, we used targeted capture markers to map over 10,000 B. glabrata scaffolds in a linkage cross of 94 F1 offspring, generating 24 linkage groups (LGs). We added additional scaffolds to these LGs based on linkage disequilibrium (LD) analysis of targeted capture and whole-genome sequences of 96 unrelated snails. Our final linkage map consists of 18,613 scaffolds comprising 515 Mb, representing 56% of the genome and 75% of genic and nonrepetitive regions. There are 18 large (> 10 Mb) LGs, likely representing the expected 18 haploid chromosomes, and > 50% of the genome has been assigned to LGs of at least 17 Mb. Comparisons with other gastropod genomes reveal patterns of synteny and chromosomal rearrangements. Linkage relationships of key immune-relevant genes may help clarify snail–schistosome interactions. By focusing on linkage among genic and nonrepetitive regions, we have generated a useful resource for associating snail phenotypes with causal genes, even in the absence of a complete genome assembly. A similar approach could potentially improve numerous poorly-assembled genomes in other taxa. This map will facilitate future work on this host of a serious human parasite.

Linkage Disequilibrium Estimation in Low Coverage High-Throughput Sequencing Data

“…, Pernaci et al 2014 ) or ordering scaffolds, such as in the Locus Ordering by Dis-Equilibrium procedure ( Khatkar et al 2010 ). This application of LD is perhaps less well known but is particularly useful for sequencing data, since assemblies are often fragmented or not existent, and has already been used in a study by Tennessen et al (2017) . One powerful application is combining LD estimates from GUS-LD with the software package LDna ( Kemppainen et al 2015 ) to explore genome-wide LD and investigate the evolutionary forces acting on a population.…”

Sequence and structural variation in the genome of the Biomphalaria glabrata embryonic (Bge) cell line

“…Furthermore, a linkage map has been constructed to arrange many of the original genomic scaffolds to linkage groups that likely represent the 18 haploid chromosomes characteristic of B. glabrata [10]. These resources will enable the development and utilization of new genetic tools in this system.…”

Gene buddies: linked balanced polymorphisms reinforce each other even in the absence of epistasis

“…There are several cases where two or more closely-linked loci all show signatures of balancing selection, often with little evidence for epistasis. Some of these are complexes of structurally and functionally related genes, such as immune gene complexes ( Takahata & Nei, 1990 ; Takahata, Satta & Klein, 1992 ; Makino & McLysaght, 2008 ; Tennessen et al, 2015 ; Tennessen, Bollmann & Blouin, 2017a ) or plant R-gene complexes ( Alcázar et al, 2014 ). In other cases, linked genes appear to have unrelated roles.…”