Phenotypic data related to genetic architecture of transmission stage production and virulence in schistosome parasites

These data were generated related to the study of the Genetic architecture of transmission stage production and virulence in schistosome parasites.

Abstract: Both theory and experimental data from multiple pathogens suggest that the production of transmission stages should be strongly associated with virulence, but the genetic bases of parasite transmission/virulence traits are poorly understood. In the blood fluke Schistosoma mansoni, parasite genotypes show extensive variation in numbers of cercariae larvae shed from infected snails. Furthermore, high shedding parasites cause high mortality to snails while low shedding parasites cause low mortality, consistent with expected trade-offs between parasite transmission and virulence. To understand the genetic basis of transmission stage production/virulence, we conducted reciprocal crosses between schistosomes from two laboratory populations that differ 8-fold in cercarial shedding and in their virulence to inbred snail hosts. Each parasite generation, we determined four-week cercarial shedding profiles in inbred Biomphalaria glabrata snails infected with single parasite larvae. We sequenced the whole genome of the F0 parents and the exome of the F1 progeny and 188 F2 progeny from each cross, and used linkage mapping to reveal quantitative trait loci (QTLs) underlying transmission stage production. Cercarial production is polygenic: we found three major QTLs on chromosome 1, 3 and 5 (Log-of-the-odds (LOD) = 5.61, 8.19, 6.25) and two minor QTLs on chromosome 2 and 4. These QTLs act additively and explained 28.56% of the phenotypic variation in cercarial shedding. Alleles inherited from the high and low shedding parents were co-dominant at all QTLs, except for chr. 1 and chr. 4 where the “high cercarial shedding” allele is recessive. These results demonstrate that the genetic architecture of key traits directly relevant to schistosome ecology can be dissected using classical linkage mapping approaches, and set the stage for fine mapping and functional validation of the genes involved using the growing armory of functional and cell biology tools available for this parasite.

This dataset is made of 4 tables:

F0_parental_populations.csv

F1.csv

F2.csv

sex.tsv

F0_parental_populations.csv

This table contains the number of cercariae produced by each individual Biomphalaria glabrata Bg26 snails infected with single genotypes of Schistosoma mansoni parasite. We have compared the transmission stage production between two different populations of S. mansoni parasite. This dataset was originally published in Le Clec'h et al., 2019 (Striking differences in virulence, transmission and sporocyst growth dynamics between two schistosome populations. Parasites and Vectors. 2019 Oct 16;12(1):485. doi: 10.1186/s13071-019-3741-z).

This table is made of 9 columns:

id: the unique identifier of each sample.

schistosoma_population: the population of schistosome used for the infection of the snail. Each snail was infected with a single parasite genotype. We have used SmLE (high shedder/highly virulent population) and SmBRE (low shedding/low virulent population).

Shed.1: the number of cercariae produced by each parasite genotype at the first shedding week (4 weeks after exposure to parasite).

Shed.2: the number of cercariae produced by each parasite genotype at the second shedding week (5 weeks after exposure to parasite).

Shed.3: the number of cercariae produced by each parasite genotype at the third shedding week (6 weeks after exposure to parasite).

Shed.4: the number of cercariae produced by each parasite genotype at the fourth shedding week (7 weeks after exposure to parasite).

sum: the sum of the cercariae produced by each parasite genotype over the 4 weeks of shedding (Shed.1 + Shed.2 + Shed.3 + Shed.4).

average: the average number of cercariae produced by each parasite genotype over the 4 weeks of shedding.

sex: the sex of each parasite genotype determined by PCR 1.

F1.csv

This table contains the number of cercariae produced by each individual Biomphalaria glabrata Bg26 snails infected with single genotypes of F1 progeny from the cross SmLE x SmBRE (see the manuscript for details).

This table is made of 11 columns:

id: the unique identifier of each sample.

cross: F1A or F1B cross. Each snail was infected with a single parasite genotype from either F1A or F1B progeny.

Shed.1: the number of cercariae produced by each parasite genotype at the first shedding week (4 weeks after exposure to parasite).

Shed.2: the number of cercariae produced by each parasite genotype at the second shedding week (5 weeks after exposure to parasite).

Shed.3: the number of cercariae produced by each parasite genotype at the third shedding week (6 weeks after exposure to parasite).

Shed.4: the number of cercariae produced by each parasite genotype at the fourth shedding week (7 weeks after exposure to parasite).

sum: the sum of the cercariae produced by each parasite genotype over the 4 weeks of shedding (Shed.1 + Shed.2 + Shed.3 + Shed.4).

average: the average number of cercariae produced by each parasite genotype over the 4 weeks of shedding.

PO: the total phenoloxidase activity in infected snail hemolymph, measured at 7.5 weeks post-exposure 2.

Hb: the hemoglobin rate in infected snail hemolymph, measured at 7.5 weeks post-exposure 3.

sex: the sex of each parasite genotype determined by PCR 1.

F2.csv

This table contains the number of cercariae produced by each individual Biomphalaria glabrata Bg26 snails infected with single genotypes of F2 progeny from the cross SmLE x SmBRE (see the manuscript for details).

This table is made of 10 columns:

id: the unique identifier of each sample.

cross: F2A or F2B cross. Each snail was infected with a single parasite genotype from either F2A or F2B progeny.

Shed.1: the number of cercariae produced by each parasite genotype at the first shedding week (4 weeks after exposure to parasite).

Shed.2: the number of cercariae produced by each parasite genotype at the second shedding week (5 weeks after exposure to parasite).

Shed.3: the number of cercariae produced by each parasite genotype at the third shedding week (6 weeks after exposure to parasite).

Shed.4: the number of cercariae produced by each parasite genotype at the fourth shedding week (7 weeks after exposure to parasite).

sum: the sum of the cercariae produced by each parasite genotype over the 4 weeks of shedding (Shed.1 + Shed.2 + Shed.3 + Shed.4)

average: the average number of cercariae produced by each parasite genotype over the 4 weeks of shedding.

PO: the total phenoloxidase activity in infected snail hemolymph, measured at 7.5 weeks post-exposure 2.

Hb: the hemoglobin rate in infected snail hemolymph, measured at 7.5 weeks post-exposure 3.

sex.csv

This table contains the in silico sexing of F0 parents, F1 parents and F2 progeny of S. mansoni parasites.

This table is made of 4 columns:

id: the unique identifier of each sample

read_depth: the read depth ratio between the Z-linked and pseudo-autosomal regions.

ratio: computed ratio between the Z-linked and pseudo-autosomal regions.

sex: the sex of each parasite genotype determined in silico: a ratio around 1 corresponds to a male carrying two Z chromosomes while a ratio around 0.5 corresponds to a female carrying only one Z chromosome.

Notes:

1. Le Clec’h W, Chevalier F et al. Real-time PCR for sexing Schistosoma mansoni cercariae. Mol Biochem Parasitol. Jan-Feb 2016; 205(1-2):35-8.doi: 10.1016/j.molbiopara.2016.03.010. Epub 2016 Mar 26.

2. Le Clec’h W et al. Characterization of hemolymph phenoloxidase activity in two Biomphalaria snail species and impact of Schistosoma mansoni infection. Parasit Vectors. 2016 Jan 22; 9:32.doi: 10.1186/s13071-016-1319-6.

3. Le Clec'h et al. Striking differences in virulence, transmission and sporocyst growth dynamics between two schistosome populations. Parasit Vectors. 2019 Oct 16; 12(1):485. doi: 10.1186/s13071-019-3741-z.

本数据集围绕曼氏血吸虫（Schistosoma mansoni）传播阶段产生与毒力的遗传结构研究生成。

摘要：现有理论与多种病原体的实验数据均表明，传播阶段的产生应与毒力紧密相关，但寄生虫传播/毒力性状的遗传基础仍知之甚少。在曼氏血吸虫中，不同寄生虫基因型从感染螺体内排出的尾蚴（cercariae）数量存在显著差异。进一步研究发现，高排尾蚴的寄生虫会导致螺类高死亡率，而低排尾蚴的寄生虫仅引发低死亡率，这与寄生虫传播与毒力间的预期权衡一致。为解析传播阶段产生/毒力的遗传基础，我们对两个曼氏血吸虫实验室种群进行了正反交，这两个种群在尾蚴排出量以及对近交系螺类宿主的毒力上相差8倍。每一代寄生虫，我们均检测了感染单个寄生虫幼虫的近交光滑双脐螺（Biomphalaria glabrata）在4周内的尾蚴排出动态。我们对F0代亲本的全基因组以及每个杂交组合的F1后代和188个F2后代的外显子组进行了测序，并通过连锁作图揭示了控制传播阶段产生的数量性状位点（quantitative trait loci，QTLs）。尾蚴产生属于多基因调控性状：我们在1、3、5号染色体上发现了3个主效QTL（对数似然比Log-of-the-odds，LOD值分别为5.61、8.19、6.25），在2、4号染色体上发现了2个微效QTL。这些QTL以加性方式发挥作用，可解释尾蚴排出量28.56%的表型变异。除1号和4号染色体上的“高尾蚴排出”等位基因为隐性外，所有QTL处的等位基因均为共显性，其遗传自高排和低排亲本。本研究证明，通过经典连锁作图方法即可解析与血吸虫生态学直接相关的关键性状的遗传结构，并为后续利用该寄生虫日益丰富的功能学与细胞生物学研究工具对相关基因进行精细定位和功能验证奠定了基础。

本数据集包含4张表格：
F0_parental_populations.csv
F1.csv
F2.csv
sex.tsv

F0_parental_populations.csv
该表格记录了每只感染单个曼氏血吸虫基因型的光滑双脐螺Bg26个体所产生的尾蚴数量。我们比较了两个不同曼氏血吸虫种群的传播阶段产生能力。本数据集最初发表于Le Clec'h等人2019年的研究（Striking differences in virulence, transmission and sporocyst growth dynamics between two schistosome populations. Parasites and Vectors. 2019 Oct 16;12(1):485. doi: 10.1186/s13071-019-3741-z）。
该表格包含9列：
id：每个样本的唯一标识符。
schistosoma_population：用于感染螺类的血吸虫种群。每只螺类仅感染单个寄生虫基因型，本研究使用了SmLE（高排尾蚴/高毒力种群）和SmBRE（低排尾蚴/低毒力种群）。
Shed.1：首次排蚴周（感染寄生虫后第4周）每个寄生虫基因型产生的尾蚴数量。
Shed.2：第二次排蚴周（感染后第5周）的尾蚴数量。
Shed.3：第三次排蚴周（感染后第6周）的尾蚴数量。
Shed.4：第四次排蚴周（感染后第7周）的尾蚴数量。
sum：4周排蚴周期内每个寄生虫基因型产生的尾蚴总数（Shed.1 + Shed.2 + Shed.3 + Shed.4）。
average：4周排蚴周期内每个寄生虫基因型产生的尾蚴平均数量。
sex：通过PCR1确定的每个寄生虫基因型的性别。

F1.csv
该表格记录了每只感染单个SmLE × SmBRE杂交组合F1后代基因型的光滑双脐螺Bg26个体所产生的尾蚴数量（详细信息见论文）。
该表格包含11列：
id：每个样本的唯一标识符。
cross：F1A或F1B杂交组合。每只螺类仅感染单个来自F1A或F1B后代的寄生虫基因型。
Shed.1：首次排蚴周（感染后第4周）的尾蚴数量。
Shed.2：第二次排蚴周（感染后第5周）的尾蚴数量。
Shed.3：第三次排蚴周（感染后第6周）的尾蚴数量。
Shed.4：第四次排蚴周（感染后第7周）的尾蚴数量。
sum：4周排蚴周期内的尾蚴总数。
average：4周排蚴周期内的尾蚴平均数量。
PO：感染后7.5周时检测的感染螺血淋巴中总酚氧化酶活性2。
Hb：感染后7.5周时检测的感染螺血淋巴中血红蛋白水平3。
sex：通过PCR1确定的每个寄生虫基因型的性别。

F2.csv
该表格记录了每只感染单个SmLE × SmBRE杂交组合F2后代基因型的光滑双脐螺Bg26个体所产生的尾蚴数量（详细信息见论文）。
该表格包含10列：
id：每个样本的唯一标识符。
cross：F2A或F2B杂交组合。每只螺类仅感染单个来自F2A或F2B后代的寄生虫基因型。
Shed.1：首次排蚴周（感染后第4周）的尾蚴数量。
Shed.2：第二次排蚴周（感染后第5周）的尾蚴数量。
Shed.3：第三次排蚴周（感染后第6周）的尾蚴数量。
Shed.4：第四次排蚴周（感染后第7周）的尾蚴数量。
sum：4周排蚴周期内的尾蚴总数。
average：4周排蚴周期内的尾蚴平均数量。
PO：感染后7.5周时检测的感染螺血淋巴中总酚氧化酶活性2。
Hb：感染后7.5周时检测的感染螺血淋巴中血红蛋白水平3。

sex.csv
该表格记录了曼氏血吸虫F0代亲本、F1代亲本以及F2代后代的计算机辅助性别分型结果。
该表格包含4列：
id：每个样本的唯一标识符。
read_depth：Z连锁区域与假常染色体区域的测序深度比值。
ratio：Z连锁区域与假常染色体区域的计算比值。
sex：通过计算机辅助确定的每个寄生虫基因型的性别：比值约为1代表携带两条Z染色体的雄性，比值约为0.5代表仅携带一条Z染色体的雌性。

注释：
1. Le Clec’h W, Chevalier F et al. Real-time PCR for sexing Schistosoma mansoni cercariae. Mol Biochem Parasitol. Jan-Feb 2016; 205(1-2):35-8.doi: 10.1016/j.molbiopara.2016.03.010. Epub 2016 Mar 26.
2. Le Clec’h W et al. Characterization of hemolymph phenoloxidase activity in two Biomphalaria snail species and impact of Schistosoma mansoni infection. Parasit Vectors. 2016 Jan 22; 9:32.doi: 10.1186/s13071-016-1319-6.
3. Le Clec'h et al. Striking differences in virulence, transmission and sporocyst growth dynamics between two schistosome populations. Parasit Vectors. 2019 Oct 16; 12(1):485. doi: 10.1186/s13071-019-3741-z.