Skip to main content
SpringerLink
Log in

Molluscan genomics: the road so far and the way forward

  • TRENDS IN AQUATIC ECOLOGY III
  • Review Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Love’s feeling is more soft and sensible than are the horns of cockled snails.

Shakespeare, Love’s Labor’s Lost.

Abstract

Mollusca is the second most species-rich phylum within the metazoans, displaying critical economic, ecological and scientific importance. Yet, they are still largely underrepresented with respect to genomic resources. The emergence of next-generation sequencing technologies has revolutionized deep-scale genomic characterization of non-model organisms, and molluscs are slowly entering this transformative era. Here, we provide a historical contextualization of the Genome Revolution in molluscs with a tour de force revision of key research trends observed over the past decade. Omic approaches such as RAD-seq, transcriptome, mitogenome and whole-genome sequencing represent the most significant resources produced for this phylum. Importantly, the molecular mechanisms underscoring multiple biological novelties and adaptations observed in molluscs are starting to be unravelled. In contrast, compared to other metazoan lineages the genomic resources currently available for this lineage still lag far behind. We put forward that to fully grasp the evolutionary and adaptive roads of this tantalizing group of organisms crucially depends on the full embracement of high-throughput sequencing (HTS) technologies in the near future.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adema, C. M., L. W. Hillier, C. S. Jones, E. S. Loker, M. Knight, P. Minx, G. Oliveira, N. Raghavan, A. Shedlock, L. R. do Amaral, H. D. Arican-Goktas, J. G. Assis, E. H. Baba, O. L. Baron, C. J. Bayne, U. Bickham-Wright, K. K. Biggar, M. Blouin, B. C. Bonning, C. Botka, J. M. Bridger, K. M. Buckley, S. K. Buddenborg, R. Lima Caldeira, J. Carleton, O. S. Carvalho, M. G. Castillo, I. W. Chalmers, M. Christensens, S. Clifton, C. Cosseau, C. Coustau, R. M. Cripps, Y. Cuesta-Astroz, S. F. Cummins, L. di Stephano, N. Dinguirard, D. Duval, S. Emrich, C. Feschotte, R. Feyereisen, P. FitzGerald, C. Fronick, L. Fulton, R. Galinier, S. G. Gava, M. Geusz, K. K. Geyer, G. I. Giraldo-Calderón, M. de Souza Gomes, M. A. Gordy, B. Gourbal, C. Grunau, P. C. Hanington, K. F. Hoffmann, D. Hughes, J. Humphries, D. J. Jackson, L. K. Jannotti-Passos, W. de Jesus Jeremias, S. Jobling, B. Kamel, A. Kapusta, S. Kaur, J. M. Koene, A. B. Kohn, D. Lawson, S. P. Lawton, D. Liang, Y. Limpanont, S. Liu, A. E. Lockyer, T. L. Lovato, F. Ludolf, V. Magrini, D. P. McManus, M. Medina, M. Misra, G. Mitta, G. M. Mkoji, M. J. Montague, C. Montelongo, L. L. Moroz, M. C. Munoz-Torres, U. Niazi, L. R. Noble, F. S. Oliveira, F. S. Pais, A. T. Papenfuss, R. Peace, J. J. Pena, E. A. Pila, T. Quelais, B. J. Raney, J. P. Rast, D. Rollinson, I. C. Rosse, B. Rotgans, E. J. Routledge, K. M. Ryan, L. L. S. Scholte, K. B. Storey, M. Swain, J. A. Tennessen, C. Tomlinson, D. L. Trujillo, E. V. Volpi, A. J. Walker, T. Wang, I. Wannaporn, W. C. Warren, X.-J. Wu, T. P. Yoshino, M. Yusuf, S.-M. Zhang, M. Zhao & R. K. Wilson, 2017. Whole genome analysis of a schistosomiasis-transmitting freshwater snail. Nature Communications 8: 15451.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Albertin, C. B., O. Simakov, T. Mitros, Z. Y. Wang, J. R. Pungor, E. Edsinger-Gonzales, S. Brenner, C. W. Ragsdale & D. S. Rokhsar, 2015. The octopus genome and the evolution of cephalopod neural and morphological novelties. Nature 524: 220–224.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Andreson, R., M. Roosaare, L. Kaplinski, S. Laht, T. Kõressaar, M. Lepamets, A. Brauer, V. Kukuškina & M. Remm, 2019. Gene content of the fish-hunting cone snail. Conus Consors. https://doi.org/10.1101/590695.

    Article  Google Scholar 

  • Andrew, R. L., L. Bernatchez, A. Bonin, C. A. Buerkle, B. C. Carstens, B. C. Emerson, D. Garant, T. Giraud, N. C. Kane, S. M. Rogers, J. Slate, H. Smith, V. L. Sork, G. N. Stone, T. H. Vines, L. Waits, A. Widmer & L. H. Rieseberg, 2013. A road map for molecular ecology. Molecular Ecology. https://doi.org/10.1111/mec.12319.

    Article  PubMed  Google Scholar 

  • Arseneau, J. R., R. Steeves & M. Laflamme, 2017. Modified low-salt CTAB extraction of high-quality DNA from contaminant-rich tissues. Molecular Ecology Resources 17: 686–693.

    CAS  PubMed  Google Scholar 

  • Arumugam, R., J. E. Uli & G. Annavi, 2019. A review of the application of next generation sequencing (NGS) in wild terrestrial vertebrate research. Annual Research & Review in Biology. https://doi.org/10.9734/arrb/2019/v31i530061.

    Article  Google Scholar 

  • Atkinson, C. L., C. C. Vaughn, K. J. Forshay & J. T. Cooper, 2013. Aggregated filter-feeding consumers alter nutrient limitation: consequences for ecosystem and community dynamics. Ecology 94: 1359–1369.

    PubMed  Google Scholar 

  • Bailey, C. H., V. F. Castellucci, J. Koester & M. Chen, 1983. Behavioral changes in aging Aplysia: a model system for studying the cellular basis of age-impaired learning, memory, and arousal. Behavioral and Neural Biology 38: 70–81.

    CAS  PubMed  Google Scholar 

  • Bairoch, A. & R. Apweiler, 1999. The SWISS-PROT protein sequence data bank and its supplement TrEMBL in 1999. Nucleic Acids Research. https://doi.org/10.1093/nar/25.1.31.

    Article  PubMed  PubMed Central  Google Scholar 

  • Barghi, N., G. P. Concepcion, B. M. Olivera & A. O. Lluisma, 2016. Structural features of conopeptide genes inferred from partial sequences of the Conus tribblei genome. Molecular Genetics and Genomics 291: 411–422.

    CAS  PubMed  Google Scholar 

  • Bateman, A., M. J. Martin, C. O’Donovan, M. Magrane, R. Apweiler, E. Alpi, R. Antunes, J. Arganiska, B. Bely, M. Bingley, C. Bonilla, R. Britto, B. Bursteinas, G. Chavali, E. Cibrian-Uhalte, A. Da Silva, M. De Giorgi, T. Dogan, F. Fazzini, P. Gane, L. G. Castro, P. Garmiri, E. Hatton-Ellis, R. Hieta, R. Huntley, D. Legge, W. Liu, J. Luo, A. Macdougall, P. Mutowo, A. Nightingale, S. Orchard, K. Pichler, D. Poggioli, S. Pundir, L. Pureza, G. Qi, S. Rosanoff, R. Saidi, T. Sawford, A. Shypitsyna, E. Turner, V. Volynkin, T. Wardell, X. Watkins, H. Zellner, A. Cowley, L. Figueira, W. Li, H. McWilliam, R. Lopez, I. Xenarios, L. Bougueleret, A. Bridge, S. Poux, N. Redaschi, L. Aimo, G. Argoud-Puy, A. Auchincloss, K. Axelsen, P. Bansal, D. Baratin, M. C. Blatter, B. Boeckmann, J. Bolleman, E. Boutet, L. Breuza, C. Casal-Casas, E. De Castro, E. Coudert, B. Cuche, M. Doche, D. Dornevil, S. Duvaud, A. Estreicher, L. Famiglietti, M. Feuermann, E. Gasteiger, S. Gehant, V. Gerritsen, A. Gos, N. Gruaz-Gumowski, U. Hinz, C. Hulo, F. Jungo, G. Keller, V. Lara, P. Lemercier, D. Lieberherr, T. Lombardot, X. Martin, P. Masson, A. Morgat, T. Neto, N. Nouspikel, S. Paesano, I. Pedruzzi, S. Pilbout, M. Pozzato, M. Pruess, C. Rivoire, B. Roechert, M. Schneider, C. Sigrist, K. Sonesson, S. Staehli, A. Stutz, S. Sundaram, M. Tognolli, L. Verbregue, A. L. Veuthey, C. H. Wu, C. N. Arighi, L. Arminski, C. Chen, Y. Chen, J. S. Garavelli, H. Huang, K. Laiho, P. McGarvey, D. A. Natale, B. E. Suzek, C. R. Vinayaka, Q. Wang, Y. Wang, L. S. Yeh, M. S. Yerramalla & J. Zhang, 2015. UniProt: a hub for protein information. Nucleic Acids Research 43: D204–D212.

    Google Scholar 

  • Belcaid, M., G. Casaburi, S. J. McAnulty, H. Schmidbaur, A. M. Suria, S. Moriano-Gutierrez, M. S. Pankey, T. H. Oakley, N. Kremer, E. J. Koch, A. J. Collins, H. Nguyen, S. Lek, I. Goncharenko-Foster, P. Minx, E. Sodergren, G. Weinstock, D. S. Rokhsar, M. McFall-Ngai, O. Simakov, J. S. Foster & S. V. Nyholm, 2019. Symbiotic organs shaped by distinct modes of genome evolution in cephalopods. Proceedings of the National Academy of Sciences of the United States of America 116: 3030–3035.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Besser, J., H. A. Carleton, P. Gerner-Smidt, R. L. Lindsey & E. Trees, 2018. Next-generation sequencing technologies and their application to the study and control of bacterial infections. Clinical Microbiology and Infection 24: 335–341.

    CAS  PubMed  Google Scholar 

  • Boudjelas, S., M. Browne, M. De Poorter & S. Lowe, 2000. 100 of the world’s worst invasive alien species: a selection from the Global Invasive Species Database International Union for Conservation of Nature and Natural Resources. IUCN-ISSG, Auckland.

    Google Scholar 

  • Bradnam, K. R., J. N. Fass, A. Alexandrov, P. Baranay, M. Bechner, I. Birol, S. Boisvert, J. A. Chapman, G. Chapuis, R. Chikhi, H. Chitsaz, W.-C. Chou, J. Corbeil, C. Del Fabbro, T. R. Docking, R. Durbin, D. Earl, S. Emrich, P. Fedotov, N. A. Fonseca, G. Ganapathy, R. A. Gibbs, S. Gnerre, É. Godzaridis, S. Goldstein, M. Haimel, G. Hall, D. Haussler, J. B. Hiatt, I. Y. Ho, J. Howard, M. Hunt, S. D. Jackman, D. B. Jaffe, E. D. Jarvis, H. Jiang, S. Kazakov, P. J. Kersey, J. O. Kitzman, J. R. Knight, S. Koren, T.-W. Lam, D. Lavenier, F. Laviolette, Y. Li, Z. Li, B. Liu, Y. Liu, R. Luo, I. MacCallum, M. D. MacManes, N. Maillet, S. Melnikov, D. Naquin, Z. Ning, T. D. Otto, B. Paten, O. S. Paulo, A. M. Phillippy, F. Pina-Martins, M. Place, D. Przybylski, X. Qin, C. Qu, F. J. Ribeiro, S. Richards, D. S. Rokhsar, J. G. Ruby, S. Scalabrin, M. C. Schatz, D. C. Schwartz, A. Sergushichev, T. Sharpe, T. I. Shaw, J. Shendure, Y. Shi, J. T. Simpson, H. Song, F. Tsarev, F. Vezzi, R. Vicedomini, B. M. Vieira, J. Wang, K. C. Worley, S. Yin, S.-M. Yiu, J. Yuan, G. Zhang, H. Zhang, S. Zhou & I. F. Korf, 2013. Assemblathon 2: evaluating de novo methods of genome assembly in three vertebrate species. GigaScience 2: 10.

    PubMed  PubMed Central  Google Scholar 

  • Brusca, R. C., G. J. Brusca & N. J. Haver, 2003. Invertebrates. Sunderland, MA.

    Google Scholar 

  • Cai, H., Q. Li, X. Fang, J. Li, N. E. Curtis, A. Altenburger, T. Shibata, M. Feng, T. Maeda, J. A. Schwartz, S. Shigenobu, N. Lundholm, T. Nishiyama, H. Yang, M. Hasebe, S. Li, S. K. Pierce & J. Wang, 2019. A draft genome assembly of the solar-powered sea slug Elysia chlorotica. Scientific Data 6: 190022.

    PubMed  PubMed Central  Google Scholar 

  • Butler, P. G., A. D. Wanamaker, J. D. Scourse, C. A. Richardson & D. J. Reynolds, 2013. Variability of marine climate on the North Icelandic Shelf in a 1357-year proxy archive based on growth increments in the bivalve Arctica islandica. Palaeogeography, Palaeoclimatology, Palaeoecology 373: 141–151. https://doi.org/10.1016/j.palaeo.2012.01.016.

    Article  Google Scholar 

  • Calcino, A. D., A. L. de Oliveira, O. Simakov, T. Schwaha, E. Zieger, T. Wollesen, & A. Wanninger, 2018. The quagga mussel genome and the evolution of freshwater tolerance. bioRxiv. https://doi.org/10.1101/505305.

  • Calisi, R. M. & M. D. MacManes, 2015. RNAseq-ing a more integrative understanding of animal behavior. Current Opinion in Behavioral Sciences 6: 65–68.

    Google Scholar 

  • Capt, C., S. Renaut, F. Ghiselli, L. Milani, N. A. Johnson, B. E. Sietman, D. T. Stewart & S. Breton, 2018. Deciphering the link between doubly uniparental inheritance of mtDNA and sex determination in bivalves: clues from comparative transcriptomics. Genome Biology and Evolution 10: 577–590.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cardoso, P., T. L. Erwin, P. A. V. Borges & T. R. New, 2011. The seven impediments in invertebrate conservation and how to overcome them. Biological Conservation 144: 2647–2655. https://doi.org/10.1016/j.biocon.2011.07.024.

    Article  Google Scholar 

  • Cowie, R. H., 2009. Apple snails (Ampullariidae) as agricultural pests: their biology, impacts and management. In Barker, G. M. (ed.), Molluscs as crop pests. CABI, Wallingford: 145–192.

    Google Scholar 

  • Cuttelod, A., M. Seddon & E. Neubert, 2011. European red list of non-marine molluscs. Publications Office of the European Union, Luxembourg: 108.

    Google Scholar 

  • David, K. T., A. E. Wilson & K. M. Halanych, 2019. Sequencing disparity in the genomic era. Molecular Biology and Evolution 36: 1624–1627.

    CAS  PubMed  Google Scholar 

  • Davies, N., D. Field, L. Amaral-Zettler, M. S. Clark, J. Deck, A. Drummond, D. P. Faith, J. Geller, J. Gilbert, F. O. Glöckner, P. R. Hirsch, J.-A. Leong, C. Meyer, M. Obst, S. Planes, C. Scholin, A. P. Vogler, R. D. Gates, R. Toonen, V. Berteaux-Lecellier, M. Barbier, K. Barker, S. Bertilsson, M. Bicak, M. J. Bietz, J. Bobe, L. Bodrossy, A. Borja, J. Coddington, J. Fuhrman, G. Gerdts, R. Gillespie, K. Goodwin, P. C. Hanson, J.-M. Hero, D. Hoekman, J. Jansson, C. Jeanthon, R. Kao, A. Klindworth, R. Knight, R. Kottmann, M. S. Koo, G. Kotoulas, A. J. Lowe, V. T. Marteinsson, F. Meyer, N. Morrison, D. D. Myrold, E. Pafilis, S. Parker, J. J. Parnell, P. N. Polymenakou, S. Ratnasingham, G. K. Roderick, N. Rodriguez-Ezpeleta, K. Schonrogge, N. Simon, N. J. Valette-Silver, Y. P. Springer, G. N. Stone, S. Stones-Havas, S.-A. Sansone, K. M. Thibault, P. Wecker, A. Wichels, J. C. Wooley, T. Yahara & A. Zingone, 2014. The founding charter of the Genomic Observatories Network. GigaScience 3: 2.

    PubMed  PubMed Central  Google Scholar 

  • Dominguez Del Angel, V., E. Hjerde, L. Sterck, S. Capella-Gutierrez, C. Notredame, O. Vinnere Pettersson, J. Amselem, L. Bouri, S. Bocs, C. Klopp, J.-F. Gibrat, A. Vlasova, B. L. Leskosek, L. Soler, M. Binzer-Panchal & H. Lantz, 2018. Ten steps to get started in Genome Assembly and Annotation. F1000Research 7: 148.

    Google Scholar 

  • Du, X., G. Fan, Y. Jiao, H. Zhang, X. Guo, R. Huang, Z. Zheng, C. Bian, Y. Deng, Q. Wang, Z. Wang, X. Liang, H. Liang, C. Shi, X. Zhao, F. Sun, R. Hao, J. Bai, J. Liu, W. Chen, J. Liang, W. Liu, Z. Xu, Q. Shi, X. Xu, G. Zhang & X. Liu, 2017. The pearl oyster Pinctada fucata martensii genome and multi-omic analyses provide insights into biomineralization. GigaScience 6: 8.

    Google Scholar 

  • Dudchenko, O., M. S. Shamim, S. Batra, N. C. Durand, N. T. Musial, R. Mostofa, M. Pham, B. G. S. Hilaire, W. Yao, E. Stamenova, M. Hoeger, S. K. Nyquist, V. Korchina, K. Pletch, J. P. Flanagan, A. Tomaszewicz, D. McAloose, C. P. Estrada, B. J. Novak, A. D. Omer & E. L. Aiden, 2018. The Juicebox Assembly Tools module facilitates de novo assembly of mammalian genomes with chromosome-length scaffolds for under $1000. bioRxiv. https://doi.org/10.1101/254797.

    Article  Google Scholar 

  • Dunisławska, A., J. Łachmańska, A. Sławińska & M. Siwek, 2017. Next generation sequencing in animal science—a review. Animal Science Papers & Reports 35(3): 205–224.

    Google Scholar 

  • Dunn, C. W. & J. F. Ryan, 2015. The evolution of animal genomes. Current Opinion in Genetics & Development 35: 25–32.

    CAS  Google Scholar 

  • Evans, J. D., S. J. Brown, K. J. J. Hackett, G. Robinson, S. Richards, D. Lawson, C. Elsik, J. Coddington, O. Edwards, S. Emrich, T. Gabaldon, M. Goldsmith, G. Hanes, B. Misof, M. Muñoz-Torres, O. Niehuis, A. Papanicolaou, M. Pfrender, M. Poelchau, M. Purcell-Miramontes, H. M. Robertson, O. Ryder, D. Tagu, T. Torres, E. Zdobnov, G. Zhang & X. Zhou, 2013. The i5K initiative: advancing arthropod genomics for knowledge, human health, agriculture, and the environment. Journal of Heredity 104: 595–600.

    Google Scholar 

  • Farrington, J. W., B. W. Tripp, S. Tanabe, A. Subramanian, J. L. Sericano, T. L. Wade & A. H. Knap, 2016. Edward D. Goldberg’s proposal of “the Mussel Watch”: reflections after 40 years. Marine Pollution Bulletin 110: 501–510.

    CAS  PubMed  Google Scholar 

  • Figueras, A., R. Moreira, M. Sendra & B. Novoa, 2019. Genomics and immunity of the Mediterranean mussel Mytilus galloprovincialis in a changing environment. Fish & Shellfish Immunology 90: 440–445.

    CAS  Google Scholar 

  • Gazeau, F., L. M. Parker, S. Comeau, J.-P. Gattuso, W. A. O’Connor, S. Martin, H.-O. Pörtner & P. M. Ross, 2013. Impacts of ocean acidification on marine shelled molluscs. Marine Biology 160: 2207–2245.

    CAS  Google Scholar 

  • Geist, J., 2011. Integrative freshwater ecology and biodiversity conservation. Ecological Indicators. https://doi.org/10.1016/j.ecolind.2011.04.002.

    Article  Google Scholar 

  • Geniza, M. & P. Jaiswal, 2017. Tools for building de novo transcriptome assembly. Current Plant Biology 11–12: 41–45.

    Google Scholar 

  • Ghiselli, F., M. Iannello, G. Puccio, P. L. Chang, F. Plazzi, S. V. Nuzhdin & M. Passamonti, 2018. Comparative transcriptomics in two bivalve species offers different perspectives on the evolution of sex-biased genes. Genome Biology and Evolution 10: 1389–1402.

    PubMed  PubMed Central  Google Scholar 

  • Ghiselli, F., M. G. Maurizii, A. Reunov, H. Ariño-Bassols, C. Cifaldi, A. Pecci, Y. Alexandrova, S. Bettini, M. Passamonti, V. Franceschini, & L. Milani, 2019. Natural heteroplasmy and mitochondrial inheritance in bivalve molluscs. Integrative and Comparative Biology; in press, advance online article. http://dx.doi.org/10.1093/icb/icz061.

  • Ghosh, M., N. Sharma, A. K. Singh, M. Gera, K. K. Pulicherla & D. K. Jeong, 2018. Transformation of animal genomics by next-generation sequencing technologies: a decade of challenges and their impact on genetic architecture. Critical Reviews in Biotechnology 38: 1157–1175.

    CAS  PubMed  Google Scholar 

  • Glanzman, D. L., 2009. Habituation in Aplysia: the Cheshire Cat of neurobiology. Neurobiology of Learning and Memory 92: 147–154.

    CAS  PubMed  Google Scholar 

  • Gómez-Chiarri, M., W. C. Warren, X. Guo & D. Proestou, 2015. Developing tools for the study of molluscan immunity: the sequencing of the genome of the eastern oyster, Crassostrea virginica. Fish & Shellfish Immunology 46: 2–4.

    Google Scholar 

  • Gonzalez, D. R., A. C. Aramendia & A. Davison, 2019. Recombination within the Cepaea nemoralis supergene is confounded by incomplete penetrance and epistasis. Heredity 123: 153–161.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goodwin, S., J. D. McPherson & W. R. McCombie, 2016. Coming of age: ten years of next-generation sequencing technologies. Nature Reviews Genetics. 17: 333–351.

    CAS  PubMed  Google Scholar 

  • Haszprunar, G. & A. Wanninger, 2012. Molluscs. Current Biology 22: R510–R514.

    CAS  PubMed  Google Scholar 

  • Hollenbeck, C. M. & I. A. Johnston, 2018. Genomic tools and selective breeding in molluscs. Frontiers in Genetics 9: 253.

    PubMed  PubMed Central  Google Scholar 

  • Kanehisa, M. & S. Goto, 2000. Yeast biochemical pathways. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28: 27–30.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Karatayev, A. Y., L. E. Burlakova & D. K. Padilla, 2015. Zebra versus quagga mussels: a review of their spread, population dynamics, and ecosystem impacts. Hydrobiologia 746: 97–112.

    CAS  Google Scholar 

  • Kay, E. A., 1995. The conservation biology of molluscs. International Union for Conservation of Nature and Natural Resources, Gland, Switzerland and Cambridge, UK. https://islandpress.org/books/conservation-biology-molluscs.

  • Kenny, N. J., E. K. O. Namigai, F. Marlétaz, J. H. L. Hui & S. M. Shimeld, 2015. Draft genome assemblies and predicted microRNA complements of the intertidal lophotrochozoans Patella vulgata (Mollusca, Patellogastropoda) and Spirobranchus (Pomatoceros) lamarcki (Annelida, Serpulida). Marine Genomics 24: 139–146.

    PubMed  Google Scholar 

  • Kijas, J., M. Hamilton, N. Botwright, H. King, L. McPherson, A. Krsinich & S. McWilliam, 2019. Genome sequencing of Blacklip and Greenlip Abalone for development and validation of a SNP based genotyping tool. Frontiers in Genetics 9: 687.

    PubMed  PubMed Central  Google Scholar 

  • Kim, B. M., S. Kang, D. H. Ahn, S. H. Jung, H. Rhee, J. S. Yoo, J. E. Lee, S. J. Lee, Y. H. Han, K. Bin Ryu, S. J. Cho, H. Park & H. S. An, 2018. The genome of common long-arm octopus Octopus minor. GigaScience 7: 11.

    Google Scholar 

  • Kocot, K. M., 2013. Recent advances and unanswered questions in deep molluscan phylogenetics. American Malacological Bulletin American Malacological Society 31: 195–208. https://doi.org/10.4003/006.031.0112.

    Article  Google Scholar 

  • Kocot, K. M., J. T. Cannon, C. Todt, M. R. Citarella, A. B. Kohn, A. Meyer, S. R. Santos, C. Schander, L. L. Moroz, B. Lieb & K. M. Halanych, 2011. Phylogenomics reveals deep molluscan relationships. Nature 477: 452–456.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kocot, K. M., N. W. Jeffery, K. Mulligan, K. M. Halanych, T. R. Gregory, 2015. Genome size estimates for Aplacophora, Polyplacophora and Scaphopoda: small solenogasters and sizeable scaphopods. Journal of Molluscan Studies 82: 216–219. https://doi.org/10.1093/mollus/eyv054.

    Article  Google Scholar 

  • Kocot, K. M., F. Aguilera, C. McDougall, D. J. Jackson & B. M. Degnan, 2016. Sea shell diversity and rapidly evolving secretomes: insights into the evolution of biomineralization. Frontiers in Zoology. https://doi.org/10.1186/s12983-016-0155-z.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kocot, K. M., C. Todt, N. T. Mikkelsen & K. M. Halanych, 2019. Phylogenomics of Aplacophora (Mollusca, Aculifera) and a solenogaster without a foot. Proceedings of the Royal Society B: Biological Sciences 286: 20190115.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lewin, H. A., G. E. Robinson, W. J. Kress, W. J. Baker, J. Coddington, K. A. Crandall, R. Durbin, S. V. Edwards, F. Forest, M. T. P. Gilbert, M. M. Goldstein, I. V. Grigoriev, K. J. Hackett, D. Haussler, E. D. Jarvis, W. E. Johnson, A. Patrinos, S. Richards, J. C. Castilla-Rubio, M.-A. van Sluys, P. S. Soltis, X. Xu, H. Yang & G. Zhang, 2018. Earth BioGenome Project: sequencing life for the future of life. Proceedings of the National Academy of Sciences of the United States of America 115: 4325–4333.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li, C., X. Liu, B. Liu, B. Ma, F. Liu, G. Liu, Q. Shi & C. Wang, 2018. Draft genome of the Peruvian scallop Argopecten purpuratus. GigaScience 7: 4.

    Google Scholar 

  • Li, Y., X. Sun, X. Hu, X. Xun, J. Zhang, X. Guo, W. Jiao, L. Zhang, W. Liu, J. Wang, J. Li, Y. Sun, Y. Miao, X. Zhang, T. Cheng, G. Xu, X. Fu, Y. Wang, X. Yu, X. Huang, W. Lu, J. Lv, C. Mu, D. Wang, X. Li, Y. Xia, Y. Li, Z. Yang, F. Wang, L. Zhang, Q. Xing, H. Dou, X. Ning, J. Dou, Y. Li, D. Kong, Y. Liu, Z. Jiang, R. Li, S. Wang & Z. Bao, 2017. Scallop genome reveals molecular adaptations to semi-sessile life and neurotoxins. Nature Communications 8: 1721.

    PubMed  PubMed Central  Google Scholar 

  • Liu, C., Y. Zhang, Y. Ren, H. Wang, S. Li, F. Jiang, L. Yin, X. Qiao, G. Zhang, W. Qian, B. Liu & W. Fan, 2018. The genome of the golden apple snail Pomacea canaliculata provides insight into stress tolerance and invasive adaptation. GigaScience 7: 9.

    CAS  Google Scholar 

  • Lopez, J. V., H. Bracken-Grissom, A. G. Collins, T. Collins, K. Crandall, D. Distel, C. Dunn, G. Giribet, S. Haddock, N. Knowlton, M. Martindale, M. Medina, C. Messing, S. J. O’Brien, G. Paulay, N. Putnam, T. Ravasi, G. W. Rouse, J. F. Ryan, A. Schulze, G. WÃrheide, M. Adamska, X. Bailly, J. Breinholt, W. E. Browne, M. C. Diaz, N. Evans, J. F. Flot, N. Fogarty, M. Johnston, B. Kamel, A. Y. Kawahara, T. Laberge, D. Lavrov, F. Michonneau, L. L. Moroz, T. Oakley, K. Osborne, S. A. Pomponi, A. Rhodes, M. Rodriguez-Lanetty, S. R. Santos, N. Satoh, R. W. Thacker, Y. Van de Peer, C. R. Voolstra, D. M. Welch, J. Winston & X. Zhou, 2014. The Global Invertebrate Genomics Alliance (GIGA): developing community resources to study diverse invertebrate genomes. Journal of Heredity. 105: 1–18.

    CAS  Google Scholar 

  • Lopez, J. V., B. Kamel, M. Medina, T. Collins & I. B. Baums, 2018. Multiple facets of marine invertebrate conservation genomics. Annual Review of Animal Biosciences 7: 473–497.

    PubMed  Google Scholar 

  • Lydeard, C., R. H. Cowie, W. F. Ponder, A. E. Bogan, P. Bouchet, S. A. Clark, K. S. Cummings, T. J. Frest, O. Gargominy, D. G. Herbert, R. Herchler, K. E. Perez, B. Roth, M. Seddon, E. E. Strong & F. G. Thompson, 2004. The global decline of nonmarine mollusks. BioScience 54: 321–330.

    Google Scholar 

  • Masonbrink, R. E., C. M. Purcell, S. E. Boles, A. Whitehead, J. R. Hyde, A. S. Seetharam & A. J. Severin, 2019. An annotated genome for Haliotis rufescens (Red Abalone) and resequenced green, pink, pinto, black, and white abalone species. Genome Biology and Evolution 11: 431–438.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mayjonade, B., J. Gouzy, C. Donnadieu, N. Pouilly, W. Marande, C. Callot, N. Langlade & S. Muños, 2017. Extraction of high-molecular-weight genomic DNA for long-read sequencing of single molecules. BioTechniques 62: xv.

    CAS  Google Scholar 

  • Mikkelsen, N. T., C. Todt, K. M. Kocot, K. M. Halanych & E. Willassen, 2019. Molecular phylogeny of Caudofoveata (Mollusca) challenges traditional views. Molecular Phylogenetics and Evolution 132: 138–150.

    PubMed  Google Scholar 

  • Miller, J. R., P. Zhou, J. Mudge, J. Gurtowski, H. Lee, T. Ramaraj, B. P. Walenz, J. Liu, R. M. Stupar, R. Denny, L. Song, N. Singh, L. G. Maron, S. R. McCouch, W. R. McCombie, M. C. Schatz, P. Tiffin, N. D. Young & K. A. T. Silverstein, 2017. Hybrid assembly with long and short reads improves discovery of gene family expansions. BMC Genomics 18: 541.

    PubMed  PubMed Central  Google Scholar 

  • Modica, M. V., F. Lombardo, P. Franchini & M. Oliverio, 2015. The venomous cocktail of the vampire snail Colubraria reticulata (Mollusca, Gastropoda). BMC Genomics 16: 441.

    PubMed  PubMed Central  Google Scholar 

  • Mudge, J. M. & J. Harrow, 2016. The state of play in higher eukaryote gene annotation. Nature Reviews Genetics 17: 758–772.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mun, S., Y.-J. Kim, K. Markkandan, W. Shin, S. Oh, J. Woo, J. Yoo, H. An & K. Han, 2017. The whole-genome and transcriptome of the Manila Clam (Ruditapes philippinarum). Genome Biology and Evolution 9: 1487–1498.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Murgarella, M., D. Puiu, B. Novoa, A. Figueras, D. Posada & C. Canchaya, 2016. Correction: a first insight into the genome of the filter-feeder mussel Mytilus galloprovincialis. PLoS ONE 11: 1–22. https://doi.org/10.1371/journal.pone.0151561.

    Article  CAS  Google Scholar 

  • Nam, B.-H., W. Kwak, Y.-O. Kim, D.-G. Kim, H. J. Kong, W.-J. Kim, J.-H. Kang, J. Y. Park, C. M. An, J.-Y. Moon, C. J. Park, J. W. Yu, J. Yoon, M. Seo, K. Kim, D. K. Kim, S. Lee, S. Sung, C. Lee, Y. Shin, M. Jung, B.-C. Kang, G. Shin, S. Ka, K. Caetano-Anolles, S. Cho & H. Kim, 2017. Genome sequence of pacific abalone (Haliotis discus hannai): the first draft genome in family Haliotidae. GigaScience 6: 5.

    Google Scholar 

  • Nguyen, T. T. T., B. J. Hayes & B. A. Ingram, 2014. Genetic parameters and response to selection in blue mussel (Mytilus galloprovincialis) using a SNP-based pedigree. Aquaculture 420–421: 295–301.

    Google Scholar 

  • Pauls, S. U., M. Alp, M. Bálint, P. Bernabò, F. Čiampor, Z. Čiamporová-Zaťovičová, D. S. Finn, J. Kohout, F. Leese, V. Lencioni, I. Paz-Vinas & M. T. Monaghan, 2014. Integrating molecular tools into freshwater ecology: developments and opportunities. Freshwater Biology 59: 1559–1576.

    Google Scholar 

  • Peñarrubia, L., R.-M. Araguas, C. Pla, N. Sanz, J. Viñas & O. Vidal, 2015a. Identification of 246 microsatellites in the Asiatic clam (Corbicula fluminea). Conservation Genetics Resources 7: 393–395.

    Google Scholar 

  • Peñarrubia, L., N. Sanz, C. Pla, O. Vidal & J. Viñas, 2015b. Using massive parallel sequencing for the development, validation, and application of population genetics markers in the invasive bivalve zebra mussel (Dreissena polymorpha). PLoS ONE 10: e0120732.

    PubMed  PubMed Central  Google Scholar 

  • Ponder, W. F. & D. R. Lindberg, 2008. Phylogeny and evolution of the Mollusca. University of California Press, Oakland.

    Google Scholar 

  • Powell, D., S. Subramanian, S. Suwansa-ard, M. Zhao, W. O’Connor, D. Raftos & A. Elizur, 2018. The genome of the oyster Saccostrea offers insight into the environmental resilience of bivalves. DNA Research 25: 655–665.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pruitt, K. D., T. Tatusova & D. R. Maglott, 2007. NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Research 35: D61–D65.

    CAS  PubMed  Google Scholar 

  • Raghavan, N. & M. Knight, 2006. The snail (Biomphalaria glabrata) genome project. Trends in Parasitology 22: 148–151.

    CAS  PubMed  Google Scholar 

  • Renaut, S., D. Guerra, W. R. Hoeh, D. T. Stewart, A. E. Bogan, F. Ghiselli, L. Milani, M. Passamonti & S. Breton, 2018. Genome survey of the freshwater mussel Venustaconcha ellipsiformis (Bivalvia: Unionida) using a hybrid de novo assembly approach. Genome Biology and Evolution 10: 1637–1646.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Richards, P. M., M. M. Liu, N. Lowe, J. W. Davey, M. L. Blaxter & A. Davison, 2013. RAD-Seq derived markers flank the shell colour and banding loci of the Cepaea nemoralis supergene. Molecular Ecology 22: 3077–3089.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Richards, S., 2015. It’s more than stamp collecting: how genome sequencing can unify biological research. Trends in Genetics 31: 411–421.

    CAS  PubMed  Google Scholar 

  • Sanger, F., S. Nicklen & A. R. Coulson, 1977. DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences of the United States of America 74: 5463–5467.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sanger, F. & A. R. Coulson, 1975. A rapid method for determining sequences in DNA by primed synthesis with DNA polymerase. Journal of Molecular Biology 94: 441–448.

    CAS  PubMed  Google Scholar 

  • Savolainen, O., M. Lascoux & J. Merilä, 2013. Ecological genomics of local adaptation. Nature Reviews Genetics 14: 807–820.

    CAS  PubMed  Google Scholar 

  • Schell, T., B. Feldmeyer, H. Schmidt, B. Greshake, O. Tills, M. Truebano, S. D. Rundle, J. Paule, I. Ebersberger & M. Pfenninger, 2017. An annotated draft genome for Radix auricularia (Gastropoda, Mollusca). Genome Biology and Evolution 9: 585–592.

    CAS  Google Scholar 

  • Schultzhaus, J. N., C. R. Taitt, B. Orihuela, M. Smerchansky, Z. S. Schultzhaus, D. Rittschof, K. J. Wahl & C. M. Spillmann, 2019. Comparison of seven methods for DNA extraction from prosomata of the acorn barnacle, Amphibalanus amphitrite. Analytical Biochemistry 586: 113441.

    CAS  PubMed  Google Scholar 

  • Sedlazeck, F. J., H. Lee, C. A. Darby & M. C. Schatz, 2018. Piercing the dark matter: bioinformatics of long-range sequencing and mapping. Nature Reviews Genetics 19: 329–346.

    CAS  PubMed  Google Scholar 

  • Sigwart, J. D. & L. H. Sumner-Rooney, 2015. Mollusca: Caudofoveata. Monoplacophora, Polyplacophora, Scaphopoda, and Solenogastres structure and evolution of invertebrate nervous systems. https://doi.org/10.1093/acprof:oso/9780199682201.003.0018.

    Article  Google Scholar 

  • Simakov, O., F. Marletaz, S.-J. Cho, E. Edsinger-Gonzales, P. Havlak, U. Hellsten, D.-H. Kuo, T. Larsson, J. Lv, D. Arendt, R. Savage, K. Osoegawa, P. de Jong, J. Grimwood, J. A. Chapman, H. Shapiro, A. Aerts, R. P. Otillar, A. Y. Terry, J. L. Boore, I. V. Grigoriev, D. R. Lindberg, E. C. Seaver, D. A. Weisblat, N. H. Putnam & D. S. Rokhsar, 2012. Insights into bilaterian evolution from three spiralian genomes. Nature 493: 526–531.

    PubMed  PubMed Central  Google Scholar 

  • Smith, S. A., N. G. Wilson, F. E. Goetz, C. Feehery, S. C. S. Andrade, G. W. Rouse, G. Giribet & C. W. Dunn, 2011. Resolving the evolutionary relationships of molluscs with phylogenomic tools. Nature 480: 364–367.

    CAS  PubMed  Google Scholar 

  • Sokolov, E. P., 2000. An improved method for DNA isolation from mucopolysaccharide-rich molluscan tissues. Journal of Molluscan Studies 66: 573–575.

    Google Scholar 

  • Sousa, R., C. Antunes & L. Guilhermino, 2008. Ecology of the invasive Asian clam Corbicula fluminea (Müller, 1774) in aquatic ecosystems: an overview. Annales de Limnologie – International Journal of Limnology 44: 85–94.

    Google Scholar 

  • Strack, E., 2015. European freshwater pearls: Part 1 – Russia. The Journal of Gemmology 34: 580–592.

    Google Scholar 

  • Strong, E. E., O. Gargominy, W. F. Ponder & P. Bouchet, 2008. Global diversity of gastropods (Gastropoda; Mollusca) in freshwater. Hydrobiologia. https://doi.org/10.1007/978-1-4020-8259-7_17.

    Article  Google Scholar 

  • Sun, J., H. Mu, J. C. H. Ip, R. Li, T. Xu, A. Accorsi, A. Sánchez Alvarado, E. Ross, Y. Lan, Y. Sun, A. Castro-Vazquez, I. A. Vega, H. Heras, S. Ituarte, B. Van Bocxlaer, K. A. Hayes, R. H. Cowie, Z. Zhao, Y. Zhang, P.-Y. Qian & J.-W. Qiu, 2019. Signatures of divergence, invasiveness, and terrestrialization revealed by four apple snail genomes. Molecular Biology and Evolution 36: 1507–1520.

    PubMed  PubMed Central  Google Scholar 

  • Sun, J., Y. Zhang, T. Xu, Y. Zhang, H. Mu, Y. Zhang, Y. Lan, C. J. Fields, J. H. L. Hui, W. Zhang, R. Li, W. Nong, F. K. M. Cheung, J. W. Qiu & P. Y. Qian, 2017. Adaptation to deep-sea chemosynthetic environments as revealed by mussel genomes. Nature Ecology and Evolution 1: 5.

    Google Scholar 

  • Swart, E. M., A. Davison, J. Ellers, R. R. Filangieri, D. J. Jackson, J. Mariën, I. B. C. van der Ouderaa, D. Roelofs & J. M. Koene, 2019. Temporal expression profile of an accessory-gland protein that is transferred via the seminal fluid of the simultaneous hermaphrodite Lymnaea stagnalis. Journal of Molluscan Studies 85: 177–183.

    Google Scholar 

  • Takeuchi, T., 2017. Molluscan genomics: implications for biology and aquaculture. Current Molecular Biology Reports 3: 297–305.

    Google Scholar 

  • Takeuchi, T., T. Kawashima, R. Koyanagi, F. Gyoja, M. Tanaka, T. Ikuta, E. Shoguchi, M. Fujiwara, C. Shinzato, K. Hisata, M. Fujie, T. Usami, K. Nagai, K. Maeyama, K. Okamoto, H. Aoki, T. Ishikawa, T. Masaoka, A. Fujiwara, K. Endo, H. Endo, H. Nagasawa, S. Kinoshita, S. Asakawa, S. Watabe & N. Satoh, 2012. Draft genome of the pearl oyster Pinctada fucata: a platform for understanding bivalve biology. DNA Research 19: 117–130.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takeuchi, T., R. Koyanagi, F. Gyoja, M. Kanda, K. Hisata, M. Fujie, H. Goto, S. Yamasaki, K. Nagai, Y. Morino, H. Miyamoto, K. Endo, H. Endo, H. Nagasawa, S. Kinoshita, S. Asakawa, S. Watabe, N. Satoh & T. Kawashima, 2016. Bivalve-specific gene expansion in the pearl oyster genome: implications of adaptation to a sessile lifestyle. Zoological Letters 2: 3.

    PubMed  PubMed Central  Google Scholar 

  • Talmage, S. C. & C. J. Gobler, 2010. Effects of past, present, and future ocean carbon dioxide concentrations on the growth and survival of larval shellfish. Proceedings of the National Academy of Sciences of the United States of America 107: 17246–17251. https://doi.org/10.1073/pnas.0913804107.

    Article  PubMed  PubMed Central  Google Scholar 

  • Uliano-Silva, M., F. Dondero, T. Dan Otto, I. Costa, N. C. B. Lima, J. A. Americo, C. J. Mazzoni, F. Prosdocimi & M. F. Rebelo, 2018. A hybrid-hierarchical genome assembly strategy to sequence the invasive golden mussel, Limnoperna fortunei. GigaScience 7: 1–10.

    CAS  Google Scholar 

  • Voolstra, C. R., GIGA Community of Scientists (COS), G. Wörheide & J. V. Lopez, 2017. Advancing genomics through the global invertebrate genomics alliance (GIGA). Invertebrate systematics CSIRO PUBLISHING 31: 1–7.

    Google Scholar 

  • Walters, E. T. & L. L. Moroz, 2009. Molluscan memory of injury: evolutionary insights into chronic pain and neurological disorders. Brain, Behavior and Evolution 74: 206–218.

    PubMed  PubMed Central  Google Scholar 

  • Wang, S., J. Zhang, W. Jiao, J. Li, X. Xun, Y. Sun, X. Guo, P. Huan, B. Dong, L. Zhang, X. Hu, X. Sun, J. Wang, C. Zhao, Y. Wang, D. Wang, X. Huang, R. Wang, J. Lv, Y. Li, Z. Zhang, B. Liu, W. Lu, Y. Hui, J. Liang, Z. Zhou, R. Hou, X. Li, Y. Liu, H. Li, X. Ning, Y. Lin, L. Zhao, Q. Xing, J. Dou, Y. Li, J. Mao, H. Guo, H. Dou, T. Li, C. Mu, W. Jiang, Q. Fu, X. Fu, Y. Miao, J. Liu, Q. Yu, R. Li, H. Liao, X. Li, Y. Kong, Z. Jiang, D. Chourrout, R. Li & Z. Bao, 2017. Scallop genome provides insights into evolution of bilaterian karyotype and development. Nature Ecology and Evolution 1: 0120.

    Google Scholar 

  • Wanninger, A. & T. Wollesen, 2019. The evolution of molluscs. Biological Reviews 94: 102–115.

    Google Scholar 

  • Yandell, M. & D. Ence, 2012. A beginner’s guide to eukaryotic genome annotation. Nature Reviews Genetics 13: 329–342. https://doi.org/10.1038/nrg3174.

    Article  CAS  PubMed  Google Scholar 

  • Zarrella, I., K. Herten, G. Maes, S. Tai, M. Yang, E. Seuntjens, E. Ritschard, M. Zach, R. Styfhals, R. Sanges, O. Simakov, G. Ponte & G. Fiorito, 2019. The survey and reference assisted assembly of the Octopus vulgaris genome. Scientific Data 6: 13.

    PubMed  PubMed Central  Google Scholar 

  • Zhang, G., X. Fang, X. Guo, L. Li, R. Luo, F. Xu, P. Yang, L. Zhang, X. Wang, H. Qi, Z. Xiong, H. Que, Y. Xie, P. W. H. Holland, J. Paps, Y. Zhu, F. Wu, Y. Chen, J. Wang, C. Peng, J. Meng, L. Yang, J. Liu, B. Wen, N. Zhang, Z. Huang, Q. Zhu, Y. Feng, A. Mount, D. Hedgecock, Z. Xu, Y. Liu, T. Domazet-Lošo, Y. Du, X. Sun, S. Zhang, B. Liu, P. Cheng, X. Jiang, J. Li, D. Fan, W. Wang, W. Fu, T. Wang, B. Wang, J. Zhang, Z. Peng, Y. Li, N. Li, J. Wang, M. Chen, Y. He, F. Tan, X. Song, Q. Zheng, R. Huang, H. Yang, X. Du, L. Chen, M. Yang, P. M. Gaffney, S. Wang, L. Luo, Z. She, Y. Ming, W. Huang, S. Zhang, B. Huang, Y. Zhang, T. Qu, P. Ni, G. Miao, J. Wang, Q. Wang, C. E. W. Steinberg, H. Wang, N. Li, L. Qian, G. Zhang, Y. Li, H. Yang, X. Liu, J. Wang, Y. Yin & J. Wang, 2012. The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490: 49–54.

    CAS  PubMed  Google Scholar 

  • Zhang, W., J. Chen, Y. Yang, Y. Tang, J. Shang & B. Shen, 2011. A practical comparison of de novo genome assembly software tools for next-generation sequencing technologies. PLoS ONE 6: e17915.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zouros, E., 2013. Biparental inheritance through uniparental transmission: the doubly uniparental inheritance (DUI) of mitochondrial DNA. Evolutionary Biology 40: 1–31.

    Google Scholar 

Download references

Acknowledgements

AGS and MLL were funded by the Portuguese Foundation for Science and Technology (FCT) under grants SFRH/BD/137935/2018 and SFRH/BD/115728/2016, respectively. This research was developed under ConBiomics: the missing approach for the Conservation of freshwater Bivalves Project No NORTE-01-0145-FEDER-030286, co-financed by COMPETE 2020, Portugal 2020 and the European Union through the ERDF, and by FCT through national funds. Additional strategic funding was provided by FCT UID/Multi/04423/2019.

Author information

Authors and Affiliations

  1. CIIMAR/CIMAR – Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Avenida General Norton de Matos, S/N, P 4450-208, Matosinhos, Portugal

    André Gomes-dos-Santos, Manuel Lopes-Lima, L. Filipe C. Castro & Elsa Froufe

  2. Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre, 1021/1055, Porto, Portugal

    André Gomes-dos-Santos & L. Filipe C. Castro

  3. CIBIO/InBIO - Research Center in Biodiversity and Genetic Resources, Universidade do Porto, Campus Agrário de Vairão, Rua Padre Armando Quintas, 4485-661, Vairão, Portugal

    Manuel Lopes-Lima

  4. IUCN SSC Mollusc Specialist Group, c/o IUCN, David Attenborough Building, Pembroke St., Cambridge, England, UK

    Manuel Lopes-Lima

Authors
  1. André Gomes-dos-Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Manuel Lopes-Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L. Filipe C. Castro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elsa Froufe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to André Gomes-dos-Santos or Manuel Lopes-Lima.

Additional information

Guest editors: Koen Martens, Sidinei M. Thomaz, Diego Fontaneto & Luigi Naselli-Flores / Emerging Trends in Aquatic Ecology III

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 207 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gomes-dos-Santos, A., Lopes-Lima, M., Castro, L.F.C. et al. Molluscan genomics: the road so far and the way forward. Hydrobiologia 847, 1705–1726 (2020). https://doi.org/10.1007/s10750-019-04111-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-019-04111-1

Keywords

Search

Navigation