Whole genome analysis of a schistosomiasis-transmitting freshwater snail

Adema, Coen M.; Hillier, LaDeana W.; Jones, Catherine S.; Loker, Eric S.; Knight, Matty; Minx, Patrick; Oliveira, Guilherme de; Raghavan, Nithyakalyani; Shedlock, Andrew M.; Amaral, Laurence Rodrigues do; Arican-Goktas, Halime D.; Assis, Juliana de; Baba, Elio H.; Baron, Olga Lucia; Bayne, Christopher J.; Bickham-Wright, Utibe; Biggar, Kyle K.; Blouin, Michael S.; Bonning, Bryony C.; Botka, Chris; Bridger, Joanna M.; Buckley, Katherine M.; Buddenborg, Sarah Kay; Caldeira, Roberta Lima; Carleton, Julia B.; Carvalho, Omar S.; Castillo, Maria G.; Chalmers, Iain W.; Christensens, Mikkel; Clifton, Sandra W.; Cosseau, Céline; Coustau, Christine; Cripps, Richard M.; Cuesta-Astroz, Yesid; Cummins, Scott F.; Stephano, Leon di; Dinguirard, Nathalie; Duval, David Timothy; Emrich, Scott J.; Feschotte, Cédric; Feyereisen, René; Fitzgerald, Peter; Fronick, Catrina C.; Fulton, Lucinda L.; Galinier, Richard; Gava, Sandra Grossi; Geusz, Michael E.; Geyer, Kathrin K.; Giraldo-Calderón, Gloria I.; Gomes, Matheus de Souza; Gordy, Michelle A.; Gourbal, Benjamin; Grunau, Christoph; Hanington, Patrick C.; Hoffmann, Karl F.; Hughes, Daniel; Humphries, Judith E.; Jackson, Daniel J.; Jannotti-Passos, Liana K.; Jeremias, Wander de Jesus; Jobling, Susan; Kamel, Bishoy; Kapusta, Aurélie; Kaur, Satwant; Koene, Joris M.; Kohn, Andrea B.; Lawson, Daniel; Lawton, Scott P; Liang, Di; Limpanont, Yanin; Liu, Sijun; Lockyer, Anne E.; Lovato, TyAnna L.; Ludolf, Fernanda; Magrini, Vincent; McManus, Donald P.; Medina, Mónica; Misra, Milind; Mitta, Guillaume; Mkoji, Gerald M.; Montague, Michæl J.; Montelongo, Cesar; Moroz, Leonid L.; Muñoz-Torres, Monica; Niazi, Umar; Noble, Leslie R.; Oliveira, Francislon Silva de; Pais, Fabiano Sviatopolk-Mirsky; Papenfuss, Anthony T.; Peace, Rob; Peña, Janeth J.; Pila, Emmanuel A.; Quelais, Titouan; Raney, Brian J.; Rast, Jonathan P.; Rollinson, David; Rosse, Izinara Cruz; Rotgans, Bronwyn; Routledge, Edwin J.; Ryan, Kathryn M.; Scholte, Larissa Lopes Silva; Storey, Kenneth B.; Swain, Martin; Tennessen, Jacob A.; Tomlinson, Chad; Trujillo, Damian L.; Volpi, Emanuela V.; Walker, Anthony J.; Wang, Tianfang; Ittiprasert, Wannaporn; Warren, Wesley C.; Wu, Xiao-Jun; Yoshino, Timothy P.; Yusuf, Mohammed; Zhang, Si-Ming; Zhao, Min; Wilson, Richard K.

doi:10.1038/ncomms15451

Cited by 219 publications

(362 citation statements)

References 54 publications

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“…LD, linkage disequilibrium.aLarson et al (2014).bMitta et al (2005).cAdema et al (2017).dPila et al (2016b).eZhang and Coultas (2011).fBaričević et al (2015).gLéonard et al (2001).hTennessen et al (2015b).iPeña and Adema (2016).jTennessen et al (2015a).kAllan et al (2017).lPila et al (2016a).mGoodall et al (2006).nBlouin et al (2013).oGalinier et al (2013).pHannington et al (2012).qKnight et al (1999).…”

Section: Resultsmentioning

confidence: 99%

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

Tennessen

Bollmann

Blouin

2017

G3 Genes|Genomes|Genetics

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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.

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Section: Resultsmentioning

confidence: 99%

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

Tennessen

Bollmann

Blouin

2017

G3 Genes|Genomes|Genetics

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“…In summary, these results provide evidence for a common phylogenetic signal that is indicative of an ovipostatin-like effect in multiple species, but also suggests that other factors may be involved in determining egg size. The possibility that ovipostatin may be involved is supported by the recent report that sequences matching the gene that encodes this accessory gland protein were found in the genome of B. glabrata (Adema et al, 2017).…”

Section: Discussionmentioning

confidence: 95%

The effect of mating on female reproduction across hermaphroditic freshwater snails

Swart

Starkloff

Ypenburg

et al. 2020

Invertebrate Biology

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Sexual conflicts often arise between mating partners because each sex tries to maximize its own reproductive success. One major male strategy to influence a partner's resource allocation is the transfer of accessory gland proteins. This has been shown to occur in simultaneous hermaphrodites as well as in organisms with separate sexes. Although accessory gland proteins affect the investment of resources in both male and female function, we here specifically focus on female investment. In the great pond snail, Lymnaea stagnalis, previous studies found that the accessory gland protein ovipostatin reduced female fecundity by suppressing egg laying in the partner in the short term (days). To investigate whether this reduction in egg laying is a commonly found effect of mating in freshwater snails, we compared egg output for evidence of suppression in isolated and paired snails of eight pulmonate species. Furthermore, we determined whether the suppression of egg laying caused a shift in resource allocation to the eggs. We found that in five of the eight species egg laying was suppressed, with fewer and lighter egg masses being laid when they had access to a mating partner. In mated pairs of L. stagnalis and Biomphalaria alexandrina, allocation of resources to the eggs was altered in opposite ways: individuals of L. stagnalis laid fewer but larger and heavier eggs; individuals of B. alexandrina laid smaller and lighter eggs, with no change in egg numbers. Such changes in the female function are most likely the result of combined effects of receiving accessory gland proteins, and the cost of mating in both male and female roles. Thus, effects of the maternal environment, including the receipt of accessory gland proteins, on offspring investment are not restricted to species with separate sexes.

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“…Alongside the emerging patterns of molluscan phenotypic evolution based on morphogenetic and palaeontological data, significant insights have been gained concerning the molecular mechanisms that govern their development (Wanninger & Wollesen, ). Thereby, the release of the genomes of various gastropods including the Pacific abalone Haliotis discus hannai (Nam et al, ), the freshwater snail Biomphalaria glabrata (Adema et al, ), and the basally branching owl limpet Lottia gigantea (Simakov et al, ) together with several bivalves [e.g. Crassostrea gigas (Thunberg, 1793) (Zhang et al, ), Patinopecten yessoensis (Jay, 1857) (Wang et al, ), and other scallop, oyster, and mussel species (Takeuchi et al, ; Du et al, ; Li et al, , ; Sun et al, )] and the California two‐spot octopus Octopus bimaculoides Pickford & McConnaughey, 1949 (Albertin et al, ) provided an important framework for studies into key developmental regulators such as Hox and ParaHox genes as well as signalling molecules involved in dorso‐ventral axis patterning (bone morphogenetic protein (BMP)/decapentaplegic (Dpp) pathway) and left/right determination (Nodal pathway).…”

Section: Evodevo Genomes and The Diversification Of Molluscsmentioning

confidence: 99%

The evolution of molluscs

2018

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Molluscs are extremely diverse invertebrate animals with a rich fossil record, highly divergent life cycles, and considerable economical and ecological importance. Key representatives include worm-like aplacophorans, armoured groups (e.g. polyplacophorans, gastropods, bivalves) and the highly complex cephalopods. Molluscan origins and evolution of their different phenotypes have largely remained unresolved, but significant progress has been made over recent years. Phylogenomic studies revealed a dichotomy of the phylum, resulting in Aculifera (shell-less aplacophorans and multi-shelled polyplacophorans) and Conchifera (all other, primarily uni-shelled groups). This challenged traditional hypotheses that proposed that molluscs gradually evolved complex phenotypes from simple, worm-like animals, a view that is corroborated by developmental studies that showed that aplacophorans are secondarily simplified. Gene expression data indicate that key regulators involved in anterior-posterior patterning (the homeobox-containing Hox genes) lost this function and were co-opted into the evolution of taxon-specific novelties in conchiferans. While the bone morphogenetic protein (BMP)/decapentaplegic (Dpp) signalling pathway, that mediates dorso-ventral axis formation, and molecular components that establish chirality appear to be more conserved between molluscs and other metazoans, variations from the common scheme occur within molluscan sublineages. The deviation of various molluscs from developmental pathways that otherwise appear widely conserved among metazoans provides novel hypotheses on molluscan evolution that can be tested with genome editing tools such as the CRISPR/Cas9 (clustered regularly interspaced short palindromic repeats/clustered regularly interspaced short palindromic repeats-associated protein9) system.

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Whole genome analysis of a schistosomiasis-transmitting freshwater snail

Cited by 219 publications

References 54 publications

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

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

The effect of mating on female reproduction across hermaphroditic freshwater snails

The evolution of molluscs

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