In humans and other animals, cancer cells divide excessively, forming tumours or flooding the blood, but they rarely spread to other individuals. However, some animals, including dogs, Tasmanian devils and bivalve molluscs like clams, cockles and mussels, can develop cancers that are transmitted from one individual to another. Despite these cancers being contagious, each one originates in a single animal, meaning that even when the cancer has spread to many individuals, its origins can be traced through its DNA.

Cancer contagion is rare, but transmissible cancers seem to be particularly common in the oceans. In fact, 7 types of contagious cancer have been described in bivalve species so far. These cancers are known as ‘hemic neoplasias’, and are characterized by the uncontrolled division of blood-like cells, which can be released by the host they developed in, and survive in ocean water. When these cells encounter individuals from the same species, they can infect them, causing them to develop hemic neoplasia too

There are still many unanswered questions about contagious cancers in bivalves. For example, how many species do the cancers affect, and which species do the cancers originate in? To address these questions, Garcia-Souto, Bruzos, Díaz et al. gathered over 400 specimens of a species of clam called the warty venus clam from the coastlines of Europe and examined them for signs of cancer. Clams collected in two regions of Spain showed signs of hemic neoplasia: one of the populations was from the Balearic Islands in the Mediterranean Sea, while the other came from the Atlantic coast of northwestern Spain.

Analyzing the genomes of the tumours from each population showed that the cancer cells from both regions had likely originated in the same animal, indicating that the cancer is contagious and had spread through different populations. The analysis also revealed that the cancer did not originally develop in warty venus clams: the cancer cells contained DNA from both warty venus clams and another species called striped venus clams. These two species live close together in the Mediterranean Sea, suggesting that the cancer started in a striped venus clam and then spread to a warty venus clam. To determine whether the cancer still affected both species, Garcia-Souto, Bruzos, Díaz et al. screened 200 striped venus clams from the same areas, but no signs of cancer were found in these clams. This suggests that currently the cancer only affects the warty venus clam.

These findings confirm that contagious cancers can jump between clam species, which could be threat to the marine environment. The fact that the cancer was so similar in clams from the Atlantic coast and from the Mediterranean Sea, however, suggests that it may have emerged very recently, or that human activity helped it to spread from one place to another. If the latter is the case, it may be possible to prevent further spread of these sea-borne cancers through human intervention.

Cancers are clonal cell lineages that arise due to somatic changes that promote cell proliferation and survival (Stratton et al., 2009). Although natural selection operating on cancers favours the outgrowth of malignant clones with replicative immortality, the continued survival of a cancer is generally restricted by the lifespan of its host. However, clonally transmissible cancers – from now on, transmissible cancers – are somatic cell lineages that are transmitted between individuals via the transfer of living cancer cells, meaning that they can survive beyond the death of their hosts (Murchison, 2008). Naturally occurring transmissible cancers have been identified in dogs (Murgia et al., 2006; Murchison et al., 2014; Baez-Ortega et al., 2019), Tasmanian devils (Murchison et al., 2012; Pye et al., 2016) and, more recently, in marine bivalves (Metzger et al., 2015; Metzger et al., 2016; Yonemitsu et al., 2019).

Hemic neoplasia (HN), also called disseminated neoplasia, is a type of leukaemia cancer found in multiple species of bivalves, including oysters, mussels, cockles, and clams (Carballal et al., 2015). Although these leukaemias represent different diseases across bivalve species, they have been classically grouped under the same term because neoplastic cells share morphological features (Carballal et al., 2015). Some HNs have been proven to have a clonal transmissible behaviour (Metzger et al., 2015), in which neoplastic cells, most likely haemocytes (i.e. the cells that populate the haemolymph and play a role in the immune response), are likely to be transmitted through marine water. In late stages of the disease, leukaemic cells invade the surrounding tissues and, generally, animals die because of the infection (Carballal et al., 2015), although remissions have also been described (Burioli et al., 2019). Despite the observation that leukaemic cells are typically transmitted between individuals from the same species, on occasion they can infect and propagate across populations from a second, different bivalve species (Metzger et al., 2016; Yonemitsu et al., 2019). Hence, these cancers represent a potential threat for the ecology of the marine environment, which argues for the necessity of their identification and characterization for their monitoring and prevention.

Here, we use multiplatform next-generation genome sequencing technologies, including Illumina short reads and Oxford Nanopore long reads, together with cytogenetics, electron microscopy, and cytohistological approaches to identify, characterize, and decipher the evolutionary origin of a new marine leukaemia that is transmitted between two different clam species that inhabit the Seas of Southern Europe, namely warty venus (Venus verrucosa) and striped venus (Chamelea gallina).

We investigated the prevalence of HN in the warty venus clam (V. verrucosa), a saltwater bivalve found in the Atlantic Coast of Europe and the Mediterranean Sea. We collected 345 clam specimens from six sampling regions in the Atlantic and the Mediterranean coasts of Europe across five different countries, including Spain, Portugal, France, Ireland, and Croatia (Figure 1a; Supplementary file 1). Cytohistological examination identified HN-like tumours in eight specimens from two sampling points in Spain (Figure 1b–e; Figure 1—figure supplement 1). Three HN-positive specimens (ERVV17-2995, ERVV17-2997, and ERVV17-3193) were collected in Galicia, northwest of the Iberian Peninsula in the Atlantic Ocean, and another five specimens (EMVV18-373, EMVV18-376, EMVV18-391, EMVV18-395, and EMVV18-400) were collected in the Balearic Islands, bathed by the Mediterranean Sea (Figure 1a; Supplementary file 1). Four of these specimens (ERVV17-2995, ERVV17-3193, EMVV18-391, and EMVV18-395) showed a severe form of the disease – classified as N3 stage – which is characterized by high levels of neoplastic cells infiltrating the gills, different levels of infiltration of the digestive gland and gonad, and low/very low infiltration of the mantle and foot (Figure 1d,e; Figure 1—figure supplement 1); one specimen (EMVV18-400) was found that was affected with an intermediate form of the disease – N2 stage – characterized by low levels of neoplastic cells infiltrating the gill vessels, digestive gland, and gonad, but not the foot (Figure 1—figure supplement 1); and three specimens (ERVV17-2997, EMVV18-373, and EMVV18-376) were diagnosed with a light form of the disease – N1 stage – characterized by low levels of neoplastic cells infiltrating the gills vessels only, and no infiltration in the remaining tissues (Figure 1—figure supplement 1). Electron microscopy analysis through gill’s ultrathin sections from two neoplastic warty venus specimens (ERVV17-2995 and ERVV17-3193) revealed tumour cells with a round shape and a pleomorphic nucleus, which are morphological features that generally characterize bivalves’ HN (Figure 1f; Figure 1—figure supplement 2). Finally, one additional neoplastic warty venus specimen (EVVV11-02) was included in the study. The animal, which was sampled in 2011 in Galicia and came from a private collection, showed abnormal metaphases in the gills that were suggestive of HN. Although the species typically shows a 2n = 38 karyotype with metacentric chromosomes that are homogeneous in size (García-Souto et al., 2015), the tumoural metaphases from this individual showed around 100 chromosomes that were variable in size and shape (Figure 1g).

Figure 1 with 2 supplements see all

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To obtain some biological insights into the clonal dynamics of this cancer, we carried out whole-genome sequencing with Illumina paired-ends in DNA samples isolated from the tumoural haemolymph from eight out of nine neoplastic specimens mentioned above (Table 1). Their feet were also sequenced, as foot typically represents the tissue with lower infiltration of neoplastic cells, making it a good candidate tissue to act as ‘matched-normal’ (i.e. host tissue). As for the animal with an abnormal karyotype (EVVV11-02) that was compatible with HN, we sequenced the only tissue available, which were gills (Table 1). Only one neoplastic specimen (EMVV18-373) that had a very low proportion of tumour cells in its haemolymph was excluded from the sequencing. Then, we mapped the paired-end reads onto a dataset containing non-redundant mitochondrial Cytochrome C Oxidase subunit 1 (Cox1) gene references from 118 Venerid clam species. In six out of eight sequenced neoplastic specimens, the results revealed an overrepresentation (>99%) of reads in the sequenced tissues mapping to Cox1 DNA sequences that exclusively identified two different clam species (Figure 2a): the expected one, warty venus clam (V. verrucosa), and a second, unexpected one, the striped venus (C. gallina), a clam that inhabits the Mediterranean Sea (Figure 2b). Preliminary analysis by PCR and capillary sequencing of Cox1 in the haemolymph of two neoplastic specimens, EMVV18-373 and EVVV11-02, revealed an electropherogram with overlapping peaks apparently containing two different haplotypes that match the reference Cox1 sequences for warty and striped venus (Figure 2c).

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These results suggested cancer contagion between the two clam species of the family Veneridae. Hence, to decipher the origins of this clam neoplasia, we further analysed the mitochondrial DNA (mtDNA) from the two species involved and the tumours. Firstly, we performed multiplatform genome sequencing, including Illumina short reads and Oxford Nanopore long reads, on canonical individuals from the two species to obtain a preliminary assembly of the mitogenomes of V. verrucosa and C. gallina. These reconstructions resulted in 18,092- and 17,618-bp long mtDNA genomes for the warty venus and the striped venus clam, respectively (Figure 2—figure supplement 1). The comparative analysis of the nucleotide sequences from both mitogenomes confirms that, although both species are relatively close within the subfamily Venerinae (Canapa et al., 1996), they represent distinct sister species, showing a Kimura’s two-parameter nucleotide distance (K2P) equal to 21.13%. Then, we mapped the paired-end sequencing data from the six neoplastic specimens with evidence of interspecies cancer transmission onto the two reconstructed species-specific mtDNA genomes. This approach confirmed the coexistence of two different mtDNA haplotypes in the six examined neoplastic samples, matching the canonical mtDNA genomes from the two clam species. For example, in a N2-stage specimen (EMVV18-400), this analysis revealed different proportion of tumour and host mtDNA molecules in the two tissue types sequenced (Figure 2d). Here, the striped venus mtDNA results the most abundant in the haemolymph, in which tumour cells are dominant over the remaining cell types, and the lower in the matched-normal tissue (i.e. infiltrated foot), where tumour cells represent a minor fraction of the total. Similar results were obtained for the remaining five neoplastic individuals (Figure 2—figure supplement 2).

To further investigate the evolutionary origins and geographic spread of this cancer, we sequenced with Illumina paired-ends an additional set of eight healthy (i.e. non-neoplastic) clams from three different Veneridae species, including five more warty venus specimens (EMVV18-385, IGVV19-666, FGVV18-183, CSVV18-1052, and PLVV18-2249) from five different countries, two striped venus specimens (IMCG15-69 and ECCG15-201) from two countries, and one specimen (EVCS14-09) from its sibling species Chamelea striatula, a type of striped venus clam that inhabits the Atlantic Ocean from Norway to the Gulf of Cadiz in Spain. This made a total of 16 Veneridae specimens sequenced, all listed in Table 1 (see also Supplementary file 1). The complete mitochondrial genomes from all tumoural and healthy V. verrucosa specimens (13 individuals), 2 C. gallina, and 1 from its sibling species C. striatula, were individually de novo assembled from the sequencing reads. As expected, this approach reconstructed two different haplotypes in six out eight sequenced neoplastic animals, supporting the presence of mtDNA from two different species. Despite the high sequencing coverage obtained for these individuals (Table 1), we did not find foreign reads in the N1 tumours (ERVV17-2997 and EMVV18-373), most likely due to a low proportion of neoplastic cells in the haemolymph and the matched-normal tissue. Then, we performed a phylogenetic analysis based on the alignment of these mitochondrial genomes (13 coding and 2 RNA gene sequences, altogether encompassing ~14 kb). The results show that tumour and non-tumour sequences from neoplastic warty venus specimens define two well-differentiated clades, and that tumoural warty venus sequences are all identical and closer to striped venus mtDNA than to its own (warty venus) (Figure 2e). Overall, these data support the existence of a single cancer clone originated in the striped venus clam C. gallina that was transmitted to V. verrucosa.

Transmissible cancers are known to occasionally acquire mitochondria from transient hosts (Strakova et al., 2016; Strakova et al., 2020), which can lead to misinterpretation of their evolutionary history. Thus, we looked for nuclear markers to confirm the striped venus origin of this cancer lineage. We performed a preliminary draft assembly of the warty venus and the striped venus nuclear ‘reference’ genomes, using the paired-end sequencing data from two non-neoplastic animals. Then, we used bioinformatic approaches to find single copy nuclear genes that were homologous between the two species, identifying two confident candidate genomic regions (see Methods): a 2.9-kb long region from DEAH12, a gene that encodes for an ATP-dependent RNA helicase, and a 2.2-kb long fragment from the Transcription Factor II Human-like gene, TFIIH. With the idea of finding differentially fixed single-nucleotide variants (SNVs) between both species, we performed PCR amplification and capillary sequencing on a 441 bp fragment from the DEAH12, and a 559 bp fragment from TFIIH, in 2 cohorts of non-neoplastic warty venus specimens (12 for DEAH12 and 15 for TFIIH), 2 cohorts of non-neoplastic striped venus (9 for DEAH12 and 12 for TFIIH), and 1 specimen of its sister species C. striatula. This analysis provided 14 and 15 sites, respectively, for the DEAH12 and the TFIIH loci, with fixed SNVs (allele frequency >95%) that allowed to discriminate between the 3 relevant species and the tumour (Figure 3a). These variants were employed to identify the Illumina reads from each sequenced warty venus neoplastic specimens that were specific for either warty venus or striped venus, which allowed to obtain the consensus sequences that corresponded to the tumour tissue and the non-affected tissue from each neoplastic individual. At the end of this process, we performed Maximum Likelihood phylogenetic reconstructions from these individual nuclear consensus sequences. On the one hand, the phylogeny for the DEAH12 locus confirmed both the monophyly of the tumoural sequences and their closer relationship to C. gallina than to the host species (Figure 3b), which were also observed in the mtDNA analysis. However, the phylogeny derived from the TFIIH locus showed that, although the tumours remained monophyletic, they were positioned in a basal branch relative to C. gallina and V. verrucosa (Figure 3b). Hence, to resolve these differences we also obtained a multilocus species tree based on the alignment of both the mtDNA and the two nuclear genes. This new phylogeny confirmed that warty venus tumours are closer to striped venus specimens than to non-neoplastic warty venus sequences from the same diseased specimens, while the non-neoplastic sequences conformed a more distant warty venus lineage (Figure 3c).

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To obtain further evidence on the striped venus origin of this clam’s neoplasia, we performed a comparative screening of tandem repeats in the genomes of C. gallina and V. verrucosa using fluorescence in situ hybridization (FISH) (Figure 3d; Figure 3—figure supplement 1). We focused on two satellite DNA repeats, namely CL4 and CL17. The satellites represent repeats of 332- and 429-bp long monomers, respectively, and were identified in a preliminary bioinformatics screening of the striped venus reference genome (see methods). This FISH approach revealed that the mentioned repeats are very abundant in heterochromatic regions from the genomes of the canonical striped venus and the neoplastic warty venus specimens tested (Figure 3d; Figure 3—figure supplement 1). However, the repeats were absent in the metaphases from all the healthy warty venus individuals (Figure 3d; Figure 3—figure supplement 1). These results suggest that the relevant chromosomes with CL4 and CL17 satellites found in neoplastic warty venus specimens derive from C. gallina, supporting that a tumour originated in C. gallina was transmitted to V. verrucosa.

To find out whether this cancer is present in the clam species where it first arose, we performed a screening for its presence in natural populations of striped venus clams from the species C. gallina (n = 213) and C. striatula (n = 9) at five additional sampling points across two countries (Supplementary file 1), including Spain (n = 115) and Italy (n = 107). Histological analyses did not show any traces of HN in these specimens. The virtual absence of this tumour in natural populations of striped venus clams may suggest that today this leukaemia is being mainly, if not exclusively, transmitted between specimens of the recipient species, warty venus. However, further sampling in other regions across the striped venus area of distribution may be necessary to confirm these findings.

Overall, the results provided here reveal the existence of a transmissible leukaemia originated in a striped venus clam, most likely C. gallina, which was transmitted to a second species, the warty venus clam (V. verrucosa), and among whose specimens it currently propagates. We identified this parasitic cancer in warty venus clams from two sampling points that are more than 1000 nautical miles away in the coasts of Spain, bathed by two different seas, the Atlantic Ocean and the Mediterranean Sea. The analysis of mitochondrial and nuclear gene sequences revealed no nucleotide diversity within the seven tumours sequenced, which supports that all belong to the same neoplastic lineage that spreads between Veneridae clams in the Seas of Southern Europe. Although we ignore the age of this cancer clone, we can confirm it arose before 2011, when the neoplastic warty venus specimen EVVV11-02 was collected. The apparent lack of genetic variation between all tumours, even from distant sampling points, suggests either that this cancer is very recent, or that it may have been unintentionally scattered by the action of man, a way of transmission that has been proposed for other bivalve transmissible cancers (Yonemitsu et al., 2019).

Nucleotide data for the mitochondrial DNA assemblies has been uploaded to GenBank under accession numbers MW662590-MW662611. These correspond to reference healthy animals of Venus verrucosa (MW662590, MW662593, MW662607, MW662608 and MW662610), Chamelea gallina (MW662591 and MW662609), Chamelea striatula (MW662611) and to both normal (MW662592, MW662595, MW662597, MW662599, MW662601, MW662602, MW662604, MW662606) and tumoral (MW662594, MW662596, MW662598, MW662600, MW662603, MW662605) mitochondrial DNAs of neoplastic animals. Genomic data (Illumina paired-end sequencing) from the mitogenomes analysed in this manuscript are allocated in DRYAD (https://doi.org/10.5061/dryad.zcrjdfn9v).

1. 1. Garcia-Souto D
   2. Diaz-Costas S
   3. Bruzos A
   4. Rocha S
   5. Roman-Lewis C
   6. Alonso J
   7. Rodriguez R
   8. Jorge R
   9. Villanueva A
   10. Silva L
   11. Valencia J
   12. Annona G
   13. Tarallo A
   14. Ricardo F
   15. Bratos-Cetinic A
   16. Posada D
   17. Pasantes J
   18. Tubio J MC

   (2021) Dryad Digital Repository

   Mitochondrial genome sequencing of marine leukemias reveals cancer contagion between clam species in the Seas of Southern Europe.

   https://doi.org/10.5061/dryad.zcrjdfn9v
2. 1. Garcia-Souto D
   2. Diaz-Costas S
   3. Bruzo AL
   4. Rocha S
   5. Pequeno A
   6. Roman-Lewis CF
   7. Costas D
   8. Rodriguez-Castro J
   9. Villanueva A
   10. Silva L
   11. Valencia JM
   12. Annona G
   13. Tarallo A
   14. Richardo F
   15. Bratos-Centinic A
   16. Posada D
   17. Tubio JM

   (2022) NCBI GenBank

   ID MW662590. Venus verrucosa mitochondrion, complete genome CSVV18_1050 Healthy animal, foot.

   https://www.ncbi.nlm.nih.gov/nuccore/MW662590
3. 1. Garcia-Souto D
   2. Diaz-Costas S
   3. Bruzos AL
   4. Rocha S
   5. Pequeno A
   6. Roman-Lewis CF
   7. Costas D
   8. Rodriguez-Castro J
   9. Villanueva A
   10. Silva L
   11. Valencia JM
   12. Annona G
   13. Tarallo A
   14. Ricardo F
   15. Bratos-Cetinic A
   16. Tubio JM

   (2022) NCBI GenBank

   ID MW662593. Venus verrucosa mitochondrion, complete genome EMVV18_385 Healthy animal, foot.

   https://www.ncbi.nlm.nih.gov/nuccore/MW662593
4. 1. Garcia-Souto D
   2. Diaz-Costas S
   3. Bruzos AL
   4. Rocha S
   5. Pequeno A
   6. Roman-Lewis CF
   7. Costas D
   8. Rodriguez-Castro J
   9. Villanueva A
   10. Silva L
   11. Valencia JM
   12. Tarallo A
   13. Richardo F
   14. Bratos-Cetinic A
   15. Posada D
   16. Tubio JM

   (2022) NCBI GenBank

   ID MW662607. Venus verrucosa mitochondrion, complete genome FGVV18_193 Healthy animal, foot.

   https://www.ncbi.nlm.nih.gov/nuccore/MW662607
5. 1. Garcia-Souto D
   2. Diaz-Costas S
   3. Bruzo AL
   4. Rocha S
   5. Pequeno A
   6. Roman-Lewis CF
   7. Costas D
   8. Rodriguez-Castro J
   9. Villanueva A
   10. Silva L
   11. Valencia JM
   12. Annona G
   13. Tarallo A
   14. Richardo F
   15. Bratos-Cetinic A
   16. Posada D
   17. Tubio JM

   (2022) NCBI GenBank

   ID MW662608. Venus verrucosa mitochondrion, complete genome IGVV19_666 Healthy animal, foot.

   https://www.ncbi.nlm.nih.gov/nuccore/MW662608
6. 1. Garcia-Souto D
   2. Diaz-Costas S
   3. Bruzos AL
   4. Rocha S
   5. Pequeno A
   6. Roman-Lewis CF
   7. Costas D
   8. Rodriguez-Castro J
   9. Villanueva A
   10. Silva L
   11. Valencia JM
   12. Annona G
   13. Tarallo A
   14. Richardo F
   15. Bratos-Cetinic A
   16. Posada D
   17. Tubio JM

   (2022) NCBI GenBank

   ID MW662610. Venus verrucosa mitochondrion, complete genome PLVV18_2249 Healthy animal, foot.

   https://www.ncbi.nlm.nih.gov/nuccore/MW662610
7. 1. Garcia-Souto D
   2. Diaz-Costas S
   3. Bruzos AL
   4. Rocha S
   5. Pequeno A
   6. Roman-Lewis CF
   7. Costas D
   8. Rodriguez-Castro J
   9. Villanueva A
   10. Silva L
   11. Valencia JM
   12. Annona G
   13. Tarallo A
   14. Richardo F
   15. Bratos-Cetinic A
   16. Posada D
   17. Tubio JM

   (2022) NCBI GenBank

   ID MW662591. Chamelea gallina mitochondrion, complete genome ECCG15_201 Healthy animal, foot.

   https://www.ncbi.nlm.nih.gov/nuccore/MW662591
8. 1. Garcia-Souto D
   2. Diaz-Costas S
   3. Bruzo AL
   4. Rocha AL
   5. Pequeno A
   6. Roman-Lewis CF
   7. Costas D
   8. Rodriguez-Castro J
   9. Villanueva A
   10. Silva L
   11. Valencia JM
   12. Annona G
   13. Tarallo A
   14. Richardo F
   15. Bratos-Cetinic A
   16. Posada D
   17. Tubio JM

   (2022) NCBI GenBank

   ID MW662592. Venus verrucosa mitochondrion, complete genome EMVV18_376 Normal mitochondria from neoplastic animal, foot.

   https://www.ncbi.nlm.nih.gov/nuccore/MW662592
9. 1. Garcia-Souto D
   2. Diaz-Costas S
   3. Bruzos AL
   4. Rocha S
   5. Pequeno A
   6. Roman-Lewis CF
   7. Costas D
   8. Rodriguez-Castro J
   9. Villanueva A
   10. Silva L
   11. Valencia JM
   12. Annona G
   13. Tarallo A
   14. Richardo F
   15. Bratos-Cetinic A
   16. Posada D
   17. Tubio JM

   (2022) NCBI GenBank

   ID MW662595. Venus verrucosa mitochondrion, complete genome EMVV18_391_Normal Normal mitochondria from neoplastic animal, foot.

   https://www.ncbi.nlm.nih.gov/nuccore/MW662595
10. 1. Garcia-Souto D
    2. Diaz-Costas S
    3. Bruzo AL
    4. Rocha A
    5. Roman-Lewis CF
    6. Costas D
    7. Rodriguez-Castro J
    8. Villanueva A
    9. Silva L
    10. Valencia JM
    11. Annona G
    12. Tarallo A
    13. Richardo F
    14. Bratos-Cetinic A
    15. Posada D
    16. Tubio JM
    17. Pequeno A

    (2022) NCBI GenBank

    ID MW662597. Venus verrucosa mitochondrion, complete genome EMVV18_395_Normal Normal mitochondria from neoplastic animal, foot.

    https://www.ncbi.nlm.nih.gov/nuccore/MW662597
11. 1. Garcia-Souto D
    2. Diaz-Costas S
    3. Bruzos AL
    4. Rocha S
    5. Pequeno A
    6. Roman-Lewis CF
    7. Costas D
    8. Rodriguez-Castro J
    9. Villanueva A
    10. Silva L
    11. Valencia JM
    12. Annona G
    13. Tarallo A
    14. Richardo F
    15. Bratos-Cetinic A
    16. Posada D
    17. Tubio JM

    (2022) NCBI GenBank

    ID MW662599. Venus verrucosa mitochondrion, complete genome EMVV18_400_Normal Normal mitochondria from neoplastic animal, foot.

    https://www.ncbi.nlm.nih.gov/nuccore/MW662599
12. 1. Garcia-Souto D
    2. Diaz-Costas S
    3. Bruzos AL
    4. Rocha S
    5. Pequeno A
    6. Roman-Lewis CF
    7. Costas D
    8. Rodriguez-Castro J
    9. Villanueva A
    10. Silva L
    11. Valencia JM
    12. Annona G
    13. Tarallo A
    14. Richardo F
    15. Bratoc-Cetinic A
    16. Posada D
    17. Tubio JM

    (2022) NCBI GenBank

    ID MW662601. Venus verrucosa mitochondrion, complete genome ERVV17_2995_Normal Normal mitochondria from neoplastic animal, foot.

    https://www.ncbi.nlm.nih.gov/nuccore/MW662601
13. 1. Garcia-Souto D
    2. Diaz-Costas S
    3. Bruzos AL
    4. Rocha S
    5. Pequeno A
    6. Roman-Lewis CF
    7. Costas D
    8. Rodriguez-Castro J
    9. Villanueva A
    10. Silva L
    11. Valencia JM
    12. Annona G
    13. Tarallo A
    14. Richardo F
    15. Bratos-Cetinic A
    16. Posada D
    17. Tubio JM

    (2022) NCBI GenBank

    ID MW662602. Venus verrucosa mitochondrion, complete genome ERVV17_2997_Normal Normal mitochondria from neoplastic animal, foot.

    https://www.ncbi.nlm.nih.gov/nuccore/MW662602
14. 1. Garcia-Souto D
    2. Diaz-Costas S
    3. Bruzos AL
    4. Rocha S
    5. Pequeno A
    6. Roman-Lewis CF
    7. Costas D
    8. Rodriguez-Castro J
    9. Villanueva A
    10. Silva L
    11. Valencia JM
    12. Annona G
    13. Tarallo A
    14. Richardo F
    15. Bratos-Cetinic A
    16. Posada D
    17. Tubio JM

    (2022) NCBI GenBank

    ID MW662604. Venus verrucosa mitochondrion, complete genome ERVV17_3193_Normal Normal mitochondria from neoplastic animal, foot.

    https://www.ncbi.nlm.nih.gov/nuccore/MW662604
15. 1. Garcia-Souto D
    2. Diaz-Costas S
    3. Bruzos AL
    4. Rocha S
    5. Pequeno A
    6. Roman-Lewis CF
    7. Costas D
    8. Rodriguez-Castro J
    9. Villanueva A
    10. Silva L
    11. Annona G
    12. Tarallo A
    13. Richardo F
    14. Bratos-Cetinic A
    15. Posada D
    16. Tubio JM
    17. Valencia JM

    (2022) NCBI GenBank

    ID MW662606. Venus verrucosa mitochondrion, complete genome EVVV11_2_Normal Normal mitochondria from neoplastic animal, foot.

    https://www.ncbi.nlm.nih.gov/nuccore/MW662606
16. 1. Garcia-Souto D
    2. Diaz-Costas S
    3. Bruzos AL
    4. Rocha S
    5. Pequeno A
    6. Roman-Lewis CF
    7. Costas D
    8. Rodriguez-Castro J
    9. Villanueva A
    10. Silva L
    11. Valencia JM
    12. Annona G
    13. Tarallo A
    14. Richardo F
    15. Bratos-Cetinic A
    16. Posada D
    17. Tubio JM

    (2022) GenBank

    ID MW662594. Venus verrucosa mitochondrion, complete genome EMVV18_391_Tumour Transmissible neoplasia derived from Chamelea gallina, neoplastic hemocytes.

    https://www.ncbi.nlm.nih.gov/nuccore/MW662594
17. 1. Garcia-Souto D
    2. Diaz-Costas S
    3. Bruzos AL
    4. Rocha S
    5. Pequeno A
    6. Roman-Lewis CF
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    ID MW662596. Venus verrucosa mitochondrion, complete genome EMVV18_395_Tumour Transmissible neoplasia derived from Chamelea gallina, neoplastic hemocytes.

    https://www.ncbi.nlm.nih.gov/nuccore/MW662596
18. 1. Garcia-Souto D
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    ID MW662598. Venus verrucosa mitochondrion, complete genome EMVV18_400_Tumour Transmissible neoplasia derived from Chamelea gallina, neoplastic hemocytes.

    https://www.ncbi.nlm.nih.gov/nuccore/MW662598
19. 1. Garcia-Souto D
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    ID MW662600. Venus verrucosa mitochondrion, complete genome ERVV17_2995_Tumour Transmissible neoplasia derived from Chamelea gallina, neoplastic hemocytes.

    https://www.ncbi.nlm.nih.gov/nuccore/MW662600
20. 1. Garcia-Souto D
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    ID MW662603. Venus verrucosa mitochondrion, complete genome ERVV17_3193_Tumour Transmissible neoplasia derived from Chamelea gallina, neoplastic hemocytes.

    https://www.ncbi.nlm.nih.gov/nuccore/MW662603
21. 1. Garcia-Souto D
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    ID MW662605. Venus verrucosa mitochondrion, complete genome EVVV11_2_Tumour Transmissible neoplasia derived from Chamelea gallina, neoplastic hemocytes.

    https://www.ncbi.nlm.nih.gov/nuccore/MW662605
22. 1. Garcia-Souto D
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    ID MW662609. Chamelea gallina mitochondrion, complete genome IMCG15_69 Healthy animal, foot.

    https://www.ncbi.nlm.nih.gov/nuccore/MW662609
23. 1. Garcia-Souto D
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    https://www.ncbi.nlm.nih.gov/nuccore/MW662611

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Author details

1. Daniel Garcia-Souto

   1. Genomes and Disease, Centre for Research in Molecular Medicine and Chronic Diseases (CIMUS), Universidade de Santiago de Compostela, Santiago de Compostela, Spain
   2. Department of Zoology, Genetics and Physical Anthropology, Universidade de Santiago de Compostela, Santiago de Compostela, Spain
   3. Cancer Ageing and Somatic Mutation Programme, Wellcome Sanger Institute, Cambridge, United Kingdom

   Contribution

   Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Writing – original draft, Writing – review and editing

   Contributed equally with

   Alicia L Bruzos and Seila Diaz

   For correspondence

   daniel.garcia.souto@usc.es

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-0997-8799

2. Alicia L Bruzos

   1. Genomes and Disease, Centre for Research in Molecular Medicine and Chronic Diseases (CIMUS), Universidade de Santiago de Compostela, Santiago de Compostela, Spain
   2. Department of Zoology, Genetics and Physical Anthropology, Universidade de Santiago de Compostela, Santiago de Compostela, Spain

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Validation, Writing – original draft

   Contributed equally with

   Daniel Garcia-Souto and Seila Diaz

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-4362-545X

3. Seila Diaz

   Genomes and Disease, Centre for Research in Molecular Medicine and Chronic Diseases (CIMUS), Universidade de Santiago de Compostela, Santiago de Compostela, Spain

   Contribution

   Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Writing – original draft

   Contributed equally with

   Daniel Garcia-Souto and Alicia L Bruzos

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-6607-290X

4. Sara Rocha

   Phylogenomics Lab, Universidade de Vigo, Vigo, Spain

   Contribution

   Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-9705-1511

5. Ana Pequeño-Valtierra

   Genomes and Disease, Centre for Research in Molecular Medicine and Chronic Diseases (CIMUS), Universidade de Santiago de Compostela, Santiago de Compostela, Spain

   Contribution

   Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

6. Camila F Roman-Lewis

   CINBIO, Universidade de Vigo, Vigo, Spain

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

7. Juana Alonso

   1. CINBIO, Universidade de Vigo, Vigo, Spain
   2. Galicia Sur Health Research Institute (IIS Galicia Sur), SERGAS-UVIGO, Vigo, Spain

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

8. Rosana Rodriguez

   Centro de Investigación Mariña, Universidade de Vigo, ECIMAT, Vigo, Spain

   Contribution

   Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

9. Damian Costas

   Centro de Investigación Mariña, Universidade de Vigo, ECIMAT, Vigo, Spain

   Contribution

   Methodology, Project administration, Resources

   Competing interests

   No competing interests declared

10. Jorge Rodriguez-Castro

    Genomes and Disease, Centre for Research in Molecular Medicine and Chronic Diseases (CIMUS), Universidade de Santiago de Compostela, Santiago de Compostela, Spain

    Contribution

    Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Writing – original draft, Writing – review and editing

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0003-2912-9601

11. Antonio Villanueva

    Centro de Investigación Mariña, Universidade de Vigo, ECIMAT, Vigo, Spain

    Contribution

    Methodology, Project administration, Resources

    Competing interests

    No competing interests declared

12. Luis Silva

    Instituto Español de Oceanografía (IEO), Centro Oceanográfico de Cádiz, Cádiz, Spain

    Contribution

    Methodology, Project administration, Resources, Writing – review and editing

    Competing interests

    No competing interests declared

13. Jose Maria Valencia

    1. Laboratori d’Investigacions Marines i Aqüicultura, (LIMIA) - Govern de les Illes Balears, Port d'Andratx, Balearic Islands, Spain
    2. Instituto de Investigaciones Agroambientales y de Economía del Agua (INAGEA) (INIA-CAIB-UIB), Palma de Mallorca, Balearic Islands, Spain

    Contribution

    Resources, Writing – review and editing

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0002-1912-1975

14. Giovanni Annona

    Stazione Zoologica Anton Dohrn, Napoli, Italy

    Contribution

    Resources, Writing – review and editing

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0001-7806-6761

15. Andrea Tarallo

    Stazione Zoologica Anton Dohrn, Napoli, Italy

    Contribution

    Resources, Writing – review and editing

    Competing interests

    No competing interests declared

16. Fernando Ricardo

    ECOMARE, Centre for Environmental and Marine Studies (CESAM), Department of Biology, University of Aveiro, Santiago University Campus, Aveiro, Portugal

    Contribution

    Resources, Writing – review and editing

    Competing interests

    No competing interests declared

17. Ana Bratoš Cetinić

    Department of Aquaculture, University of Dubrovnik, Dubrovnik, Croatia

    Contribution

    Resources, Writing – review and editing

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0002-2928-4858

18. David Posada

    1. CINBIO, Universidade de Vigo, Vigo, Spain
    2. Galicia Sur Health Research Institute (IIS Galicia Sur), SERGAS-UVIGO, Vigo, Spain
    3. Department of Biochemistry, Genetics and Immunology, Universidade de Vigo, Vigo, Spain

    Contribution

    Investigation, Methodology, Writing – review and editing

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0003-1407-3406

19. Juan Jose Pasantes

    1. Department of Biochemistry, Genetics and Immunology, Universidade de Vigo, Vigo, Spain
    2. Centro de Investigación Mariña, Universidade de Vigo, Vigo, Spain

    Contribution

    Investigation, Methodology, Resources, Supervision, Writing – review and editing

    Competing interests

    No competing interests declared

20. Jose MC Tubio

    1. Genomes and Disease, Centre for Research in Molecular Medicine and Chronic Diseases (CIMUS), Universidade de Santiago de Compostela, Santiago de Compostela, Spain
    2. Department of Zoology, Genetics and Physical Anthropology, Universidade de Santiago de Compostela, Santiago de Compostela, Spain

    Contribution

    Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Writing – original draft, Writing – review and editing

    For correspondence

    jose.mc.tubio@usc.es

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0003-3540-2459

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