First description of a widespread Mytilus trossulus-derived bivalve transmissible cancer lineage in M. trossulus itself
1.
Murchison, E. P. Clonally transmissible cancers in dogs and Tasmanian devils. Oncogene 27, S19–S30 (2008).
CAS PubMed Article PubMed Central Google Scholar
2.
Metzger, M. J. et al. Widespread transmission of independent cancer lineages within multiple bivalve species. Nature 534, 705–709 (2016).
ADS CAS PubMed PubMed Central Article Google Scholar
3.
Storfer, A. et al. The devil is in the details: Genomics of transmissible cancers in Tasmanian devils. PLoS Pathog. 14, 1–7 (2018).
Article CAS Google Scholar
4.
Nowinsky, M. A. Zur Frage über die Impfung der krebsigen Geschwülste. Zentralbl Med Wissensch. 14, 790–791 (1876).
Google Scholar
5.
Murgia, C., Pritchard, J. K., Kim, S. Y., Fassati, A. & Weiss, R. A. Clonal origin and evolution of a transmissible cancer. Cell 126, 477–487 (2006).
CAS PubMed PubMed Central Article Google Scholar
6.
Pearse, A. M. & Swift, K. Allograft theory: transmission of devil facial-tumour disease. Nature 439, 549 (2006).
ADS CAS PubMed Article PubMed Central Google Scholar
7.
Siddle, H. V. et al. Transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial. Proc. Natl. Acad. Sci. USA 104, 16221–16226 (2007).
ADS CAS PubMed Article PubMed Central Google Scholar
8.
Metzger, M. J. J., Reinisch, C., Sherry, J. & Goff, S. P. P. Horizontal transmission of clonal cancer cells causes leukemia in soft-shell clams. Cell 161, 255–263 (2015).
CAS PubMed PubMed Central Article Google Scholar
9.
Riquet, F., Simon, A. & Bierne, N. Weird genotypes? Don’t discard them, transmissible cancer could be an explanation. Evol. Appl. 10, 140–145 (2017).
CAS PubMed Article PubMed Central Google Scholar
10.
Yonemitsu, M. A. et al. A single clonal lineage of transmissible cancer identified in two marine mussel species in South America and Europe. Elife 8, 1–21 (2019).
Article Google Scholar
11.
Woods, G. M., Bruce Lyons, A. & Bettiol, S. S. A devil of a transmissible cancer. Trop. Med. Infect. Dis. 5, 1–10 (2020).
Google Scholar
12.
Ganguly, B., Das, U. & Das, A. K. Canine transmissible venereal tumour: a review. Vet. Comp. Oncol. 14, 1–12 (2016).
CAS PubMed Article Google Scholar
13.
Paynter, A. N., Metzger, M. J., Sessa, J. A. & Siddall, M. E. Evidence of horizontal transmission of the cancer-associated Steamer retrotransposon among ecological cohort bivalve species. Dis. Aquat. Organ. https://doi.org/10.3354/dao03113 (2017).
Article PubMed Google Scholar
14.
Barber, B. J. Neoplastic diseases of commercially important marine bivalves. Aquat. Living Resour. 17, 449–466 (2004).
Article Google Scholar
15.
Farley, C. A. Sarcomatoid proliferative disease in a wild population of blue mussels (Mytilus edulis). J. Natl. Cancer Inst. 43, 509–516 (1969).
CAS PubMed PubMed Central Google Scholar
16.
Sparks, A. K. Synopsis of Invertebrate Pathology Exclusive of Insects (Elsevier, 1985).
Google Scholar
17.
Muttray, A. F. & Vassilenko, K. Mollusca: disseminated neoplasia in bivalves and the p53 protein family. Adv. Comp. Immunol. https://doi.org/10.1007/978-3-319-76768-0 (1969).
Article Google Scholar
18.
Bihari, N., Mičić, M., Batel, R. & Zahn, R. K. Flow cytometric detection of DNA cell cycle alterations in hemocytes of mussels (Mytilus galloprovincialis) off the Adriatic coast Croatia. Aquat. Toxicol. 64, 121–129 (2003).
CAS PubMed Article PubMed Central Google Scholar
19.
Vassilenko, E. & Baldwin, S. A. Using flow cytometry to detect haemic neoplasia in mussels (Mytilus trossulus) from the Pacific Coast of Southern British Columbia Canada. J. Invertebr. Pathol. 117, 68–72 (2014).
PubMed Article PubMed Central Google Scholar
20.
Moore, J. D., Elston, R. A., Drum, A. S. & Wilkinson, M. T. Alternate pathogenesis of systemic neoplasia in the bivalve mollusc Mytilus. J. Invertebr. Pathol. 58, 231–243 (1991).
CAS PubMed Article Google Scholar
21.
Benabdelmouna, A., Saunier, A., Ledu, C., Travers, M. A. & Morga, B. Genomic abnormalities affecting mussels (Mytilus edulis-galloprovincialis) in France are related to ongoing neoplastic processes, evidenced by dual flow cytometry and cell monolayer analyses. J. Invertebr. Pathol. 157, 45–52 (2018).
Article CAS Google Scholar
22.
Burioli, E. A. V. et al. Implementation of various approaches to study the prevalence, incidence and progression of disseminated neoplasia in mussel stocks. J. Invertebr. Pathol. 168, 107271 (2019).
CAS PubMed Article Google Scholar
23.
Moore, C. A., Beckmann, N. & Patricia Morse, M. Cytoskeletal structure of diseased and normal hemocytes of Mya arenaria. J. Invertebr. Pathol. 60, 141–147 (1992).
Article Google Scholar
24.
Carballal, M. J., Barber, B. J., Iglesias, D. & Villalba, A. Neoplastic diseases of marine bivalves. J. Invertebr. Pathol. https://doi.org/10.1016/j.jip.2015.06.004 (2015).
Article PubMed Google Scholar
25.
Odintsova, N. A. Leukemia-like cancer in bivalves. Russ. J. Mar. Biol. 46, 59–67 (2020).
Article Google Scholar
26.
Smolarz, K., Renault, T. & Wołowicz, M. Ultrastructural study of neoplastic cells in Macoma balthica (Bivalvia) from the Gulf of Gdansk (Poland). J. Invertebr. Pathol. 92, 79–84 (2006).
PubMed Article Google Scholar
27.
Carella, F. et al. Nuclear morphometry and ploidy of normal and neoplastic haemocytes in mussels. PLoS ONE 12, e0173219 (2017).
PubMed PubMed Central Article CAS Google Scholar
28.
Smolowitz, R. M. & Reinisch, C. L. Indirect peroxidase staining using monoclonal antibodies specific for Mya arenaria neoplastic cells. J. Invertebr. Pathol. 48, 139–145 (1986).
CAS PubMed Article Google Scholar
29.
Carella, F., Figueras, A., Novoa, B. & De Vico, G. Cytomorphology and PCNA expression pattern in bivalves Mytilus galloprovincialis and Cerastoderma edule with haemic neoplasia. Dis. Aquat. Organ. 105, 81–87 (2013).
PubMed Article Google Scholar
30.
McDonald, J. H., Seed, R. & Koehn, R. K. Allozymes and morphometric characters of three species of Mytilus in the Northern and Southern Hemispheres. Mar. Biol. 111, 323–333 (1991).
Article Google Scholar
31.
Larraín, M. A., Zbawicka, M., Araneda, C., Gardner, J. P. A. & Wenne, R. Native and invasive taxa on the Pacific coast of South America: impacts on aquaculture, traceability and biodiversity of blue mussels (Mytilus spp.). Evol. Appl. 11, 298–311 (2018).
Article CAS Google Scholar
32.
Pye, R. J. et al. A second transmissible cancer in Tasmanian devils. Proc. Natl. Acad. Sci. USA 113, 374–379 (2016).
ADS CAS PubMed Article PubMed Central Google Scholar
33.
Strakova, A. et al. Mitochondrial genetic diversity, selection and recombination in a canine transmissible cancer. Elife 5, 1–25 (2016).
Article Google Scholar
34.
Rawson, P. D. & Harper, F. M. Colonization of the northwest Atlantic by the blue mussel, Mytilus trossulus postdates the last glacial maximum. Mar. Biol. 156, 1857–1868 (2009).
Article Google Scholar
35.
Wenne, R., Bach, L., Zbawicka, M., Strand, J. & McDonald, J. H. A first report on coexistence and hybridization of Mytilus trossulus and M. edulis mussels in Greenland. Polar Biol. 39, 343–355 (2016).
Article Google Scholar
36.
Laakkonen, H. M., Hardman, M., Strelkov, P. & Väinölä, R. Cycles of trans-Arctic dispersal and vicariance, and diversification of the amphi-boreal marine fauna. J. Evol. Biol. https://doi.org/10.1111/jeb.13674 (2020).
Article PubMed PubMed Central Google Scholar
37.
Zbawicka, M., Wenne, R. & Burzyński, A. Mitogenomics of recombinant mitochondrial genomes of Baltic Sea Mytilus mussels. Mol. Genet. Genom. 289, 1275–1287 (2014).
CAS Article Google Scholar
38.
Śmietanka, B. & Burzyński, A. Disruption of doubly uniparental inheritance of mitochondrial DNA associated with hybridization area of European Mytilus edulis and Mytilus trossulus in Norway. Mar. Biol. https://doi.org/10.1007/s00227-017-3235-5 (2017).
Article PubMed PubMed Central Google Scholar
39.
Sunila, I. Histopathology of mussels (Mytilus edulis L.) from the Tvarminne area, the Gulf of Finland (Baltic Sea). Ann. Zool. Fennici 24, 55–69 (1987).
Google Scholar
40.
Usheva, L. N. & Frolova, L. T. Neoplasia in the connective tissue tumor in the mussel Mytilus trossulus from a polluted region of Nakhodka Bay, the Sea of Japan. Ontogenez 31, 63–70 (2000).
CAS PubMed PubMed Central Google Scholar
41.
Maiorova, M. A. & Odintsova, N. A. β integrin-like protein-mediated adhesion and its disturbances during cell cultivation of the mussel Mytilus trossulus. Cell Tissue Res. 361, 581–592 (2015).
CAS PubMed Article PubMed Central Google Scholar
42.
Marigomez, I., Lekube, X. & Cancio, I. Immunochemical localisation of proliferating cells in mussel digestive gland tissue. Histochem. J. 31, 781–788 (1999).
CAS PubMed Article PubMed Central Google Scholar
43.
Maiorova, M. A. & Odintsova, N. A. Proliferative potential of larval cells of the mussel Mytilus trossulus and their capacity to differentiate into myogenic cells in culture. Russ. J. Mar. Biol. 42, 281–285 (2016).
Article Google Scholar
44.
Voronezhskaya, E. E., Nezlin, L. P., Odintsova, N. A., Plummer, J. T. & Croll, R. P. Neuronal development in larval mussel Mytilus trossulus (Mollusca: Bivalvia). Zoomorphology 127, 97–110 (2008).
Article Google Scholar
45.
Presa, P., Pérez, M., Diz, A. P., Perez, M. & Diz, A. P. Polymorphic microsatellite markers for blue mussels (Mytilus spp.). Conserv. Genet. 3, 441–443 (2002).
CAS Article Google Scholar
46.
Zouros, E. Biparental inheritance through uniparental transmission: the doubly uniparental inheritance (DUI) of mitochondrial DNA. Evol. Biol. 40, 1–31 (2013).
Article Google Scholar
47.
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).
CAS PubMed PubMed Central Article Google Scholar
48.
Paabo, S., Irwin, M. & Wilson, C. DNA damage promotes jumping between templates during enzymatic amplification. J. Biol. Chem. 265, 4718–4721 (1990).
CAS PubMed Article PubMed Central Google Scholar
49.
Bradley, R. D. & Hillis, D. A. Recombinant DNA sequences generated by PCR amplification. Mol. Biol. Evol. 14, 592–593 (1997).
CAS PubMed Article PubMed Central Google Scholar
50.
Letunic, I. & Bork, P. Interactive Tree of Life (iTOL) v4: recent updates and new developments. Nucl. Acids Res. 47, 256–259 (2019).
Article CAS Google Scholar
51.
Martin, D. P., Murrell, B., Golden, M., Khoosal, A. & Muhire, B. RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol. 1, 1–5 (2015).
Article Google Scholar
52.
Breton, S., Burger, G., Stewart, D. T. & Blier, P. U. Comparative analysis of gender-associated complete mitochondrial genomes in marine mussels (Mytilus spp.). Genetics 172, 1107–1119 (2006).
CAS PubMed PubMed Central Article Google Scholar
53.
Marko, P. B. et al. The ‘Expansion-contraction’ model of Pleistocene biogeography: rocky shores suffer a sea change?. Mol. Ecol. 19, 146–169 (2010).
CAS PubMed Article Google Scholar
54.
Crego-Prieto, V., Juanes, F. & Garcia-Vazquez, E. Aquaculture and the spread of introduced mussel genes in British Columbia. Biol. Invasions https://doi.org/10.1007/s10530-015-0853-z (2015).
Article Google Scholar
55.
Chung, J. M. et al. Molecular phylogenetic study of bivalvia from four countries (China, Japan, Russia and Myanmar) using 3 types of primers. Korean J. Malacol. 35, 137–148 (2019).
Google Scholar
56.
Layton, K. K. S., Martel, A. L., Hebert, P. D. N. & Layton, K. K. S. Patterns of DNA barcode variation in Canadian Marine molluscs. PLoS ONE 9, 1–9 (2014).
Article Google Scholar
57.
deWaard, J. R. et al. A reference library for Canadian invertebrates with 1.5 million barcodes, voucher specimens, and DNA samples. Sci. Data 6, 1–12 (2019).
Article CAS Google Scholar
58.
Clement, M., Snell, Q., Walker, P., Posada, D. & Crandall, K. TCS: Estimating Gene Genealogies. Parallel Distrib. Process. Symp. Int. 2, 184 (2002).
59.
Leigh, J. W. & Bryant, D. POPART: full-feature software for haplotype network construction. Methods Ecol. Evol. 6, 1110–1116 (2015).
Article Google Scholar
60.
Kartavtsev, Y. P., Masalkova, N. A. & Katolikova, M. V. Genetic and morphometric variability in settlements of two mussel species (Mytilus ex. Gr. Edulis), Mytilus trossulus and Mytilus galloprovincialis, in the Northwestern Sea of Japan. J. Shellfish Res. 37, 103–119 (2018).
Article Google Scholar
61.
Larraín, M. A., González, P., Pérez, C. & Araneda, C. Comparison between single and multi-locus approaches for specimen identification in Mytilus mussels. Sci. Rep. 9, 1–13 (2019).
Article CAS Google Scholar
62.
Inoue, K., Waite, J. H., Matsuoka, M., Odo, S. & Harayama, S. Interspecific variations in adhesive protein sequences of Mytilus edulis, M. galloprovincialis, and M. trossulus. Biol. Bull. 189, 370–375 (1995).
CAS PubMed Article Google Scholar
63.
Heath, D. D., Rawson, P. D. & Hilbish, T. J. PCR-based nuclear markers identify alien blue mussel Mytilus spp. genotypes on the west coast of Canada. Can. J. Fish. Aquat. Sci. 52, 2621–2627 (1995).
CAS Article Google Scholar
64.
Rawson, P. D., Secor, C. L. & Hilbish, T. J. The effects of natural hybridization on the regulation of doubly uniparental mtDNA inheritance in blue mussels (Mytilus spp.). Genetics 144, 241–248 (1996).
CAS PubMed PubMed Central Article Google Scholar
65.
Rawson, P. D. & Hilbish, T. J. Distribution of male and female mtDNA lineages in populations of blue mussels, Mytilus trossulus and M. galloprovincialis, along the Pacific coast of North America. Mar. Biol. 124, 245–250 (1995).
Article Google Scholar
66.
Cremonte, F., Vázquez, N. & Silva, M. R. Gonad atrophy caused by disseminated neoplasia in Mytilus chilensis cultured in the Beagle channel, Tierra Del Fuego Province Argentina. J. Shellfish Res. 30, 845–849 (2011).
Article Google Scholar
67.
Ciocan, C. & Sunila, I. Disseminated neoplasia in blue mussels, Mytilus galloprovincialis, from the Black Sea Romania. Mar. Pollut. Bull. 50, 1335–1339 (2005).
CAS PubMed Article Google Scholar
68.
Gombač, M., Sitar, R., Pogačnik, M., Arzul, I. & Jenčič, V. Haemocytic neoplasia in Mediterranean mussels (Mytilus galloprovincialis). Mar. Freshw. Behav. Physiol. 46, 135–143 (2013).
Article Google Scholar
69.
Villalba, A., Mourelle, S. G., Carballal, M. J. & López, C. Symbionts and diseases of farmed mussels Mytilus galloprovincialis throughout the culture process in the Rias of Galicia (NW Spain). Dis. Aquat. Organ. 31, 127–139 (1997).
Article Google Scholar
70.
Cremonte, F., Puebla, C., Tillería, J. & Videla, V. Estudio histopatológico del chorito Mytilus chilensis (Mytilidae) y del culengue Gari solida (Psammobiidae) en el sur de Chile. Lat. Am. J. Aquat. Res. 43, 248–254 (2015).
Article Google Scholar
71.
Vassilenko, E. I., Muttray, A. F., Schulte, P. M. & Baldwin, S. A. Variations in p53-like cDNA sequence are correlated with mussel haemic neoplasia: a potential molecular-level tool for biomonitoring. Mutat. Res. Genet. Toxicol. Environ. Mutagen. https://doi.org/10.1016/j.mrgentox.2010.06.001 (2010).
Article Google Scholar
72.
Caza, F., Bernet, E., Veyrier, F. J., Betoulle, S. & St-Pierre, Y. Hemocytes released in seawater act as Trojan horses for spreading of bacterial infections in mussels. Sci. Rep. 10, 1–12 (2020).
Article CAS Google Scholar
73.
Rebbeck, C. A., Leroi, A. M. & Burt, A. Mitochondrial capture by a transmissible cancer. Science (80-) 331, 303 (2011).
ADS CAS Article Google Scholar
74.
Rawson, P. D. & Hilbish, T. J. Asymmetric introgression of mitochondrial DNA among European populations of Blue Mussels (Mytilus spp.). Evolution (N. Y.) 52, 100–108 (1998).
Google Scholar
75.
Kijewski, A., Zbawicka, M., Väinölä, R. & Wenne, T. K. Introgression and mitochondrial DNA heteroplasmy in the Baltic populations of mussels Mytilus trossulus and M. edulis. Mar. Biol. https://doi.org/10.1007/s00227-006-0316-2 (2006).
Article Google Scholar
76.
Burzyński, A., Zbawicka, M., Skibinski, D. O. F. & Wenne, R. Evidence for recombination of mtDNA in the marine mussel Mytilus trossulus from the Baltic. Mol. Biol. Evol. 20, 388–392 (2003).
PubMed Article PubMed Central Google Scholar
77.
Burzynski, A., Zbawicka, M., Skibinski, D. O. F. & Wenne, R. Doubly uniparental inheritance is associated with high polymorphism for rearranged and recombinant control region haplotypes in Baltic Mytilus trossulus. Genetics 174, 1081–1094 (2006).
CAS PubMed PubMed Central Article Google Scholar
78.
Stuckas, H., Stoof, K., Quesada, H. & Tiedemann, R. Evolutionary implications of discordant clines across the Baltic Mytilus hybrid zone (Mytilus edulis and Mytilus trossulus). Heredity (Edinb). 103, 146–156 (2009).
CAS PubMed Article PubMed Central Google Scholar
79.
Cao, L., Kenchington, E. & Zouros, E. Differential segregation patterns of sperm mitochondria in embryos of the Blue Mussel (Mytilus edulis). Genetics https://doi.org/10.1534/genetics.166.2.883 (2004).
Article PubMed PubMed Central Google Scholar More