Section: Evolutionary Biology
Topic: Evolution, Genetics/Genomics, Population biology

Substantial genetic mixing among sexual and androgenetic lineages within the clam genus Corbicula

10.24072/pcjournal.180 - Peer Community Journal, Volume 2 (2022), article no. e73.

Get full text PDF Peer reviewed and recommended by PCI

“Occasional” sexuality occurs when a species combines clonal reproduction and genetic mixing. This strategy is predicted to combine the advantages of both asexuality and sexuality, but its actual consequences on the genetic diversity and species longevity are poorly understood. Androgenesis, a reproductive mode in which the offspring inherits its entire nuclear genome from the father, is often reported as a strictly clonal reproductive mode. Androgenesis is the predominant reproductive mode within the hermaphroditic, invasive lineages of the mollusk genus Corbicula. Their ability to reproduce clonally through androgenesis has been determinant in their invasive success, having colonized during the 20th century American and European freshwater systems, where they became notorious invaders with a widespread, global distribution. However, in androgenetic Corbicula clams, occasional genetic mixing between distinct lineages has also been observed when the sperm of one lineage fertilizes the oocyte of another one. Because of these occasional introgressions, the genetic relationships between Corbicula species remained unclear, and the biogeographic origins of the invasive androgenetic lineages have been challenging to identify. To address these issues, we analyzed the patterns of allele sharing for several nuclear and mitochondrial molecular markers among Corbicula individuals collected across both the native and invasive range. Our results show the occurrence of an allelic pool encompassing all Corbicula freshwater species worldwide, including sexual and androgenetic ones, which highlights the substantial genetic mixing within this genus. However, the differences in allele sharing patterns between invasive lineages, and the low diversity within each lineage, suggest recent, distinct biogeographic origins of invasive Corbicula androgenetic lineages. Finally, the polyploidy, high heterozygosity, and hybrid phenotypes and genotypes found in our study probably originated from hybridization events following egg parasitism between distinct Corbicula lineages. This extensive cross-lineage mixing found in Corbicula may generate nuclear diversity in an otherwise asexually reproducing species.

Published online:
DOI: 10.24072/pcjournal.180
Type: Research article
Vastrade, Martin 1; Etoundi, Emilie 1; Bournonville, Thibaut 2; Colinet, Mathilde 1; Debortoli, Nicolas 1, 2; Hedtke, Shannon M. 3; Nicolas, Emilien 4; Pigneur, Lise-Marie 5; Virgo, Julie 1; Flot, Jean-François 6, 7; Marescaux, Jonathan 1, 2; Van Doninck, Karine 1, 4

1 Laboratory of Evolutionary Genetics and Ecology; Research Unit in Environmental and Evolutionary Biology; Institute of Life, Earth and Environment (ILEE); University of Namur, 5000 Namur, Belgium
2 e-biom SA, 5/7 Rue Godefroid, 5000 Namur, Belgium
3 Department of Environment and Genetics, School of Agriculture, Biomedicine and Environment, La Trobe University, Bundoora, Victoria, 3086, Australia
4 Université libre de Bruxelles (ULB), Molecular Biology and Evolution, C.P. 160/16, Avenue F.D. Roosevelt 50, 1050 Brussels, Belgium
5 Université de Liège, Conservation Genetics Laboratory, Chemin de la vallée 4, 4000 Liège, Belgium
6 Université libre de Bruxelles (ULB), Evolutionary Biology and Ecology, C.P. 160/12, Avenue F.D. Roosevelt 50, 1050 Brussels, Belgium
7 Interuniversity Institute of Bioinformatics in Brussels – (IB)2, Brussels, Belgium
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
@article{10_24072_pcjournal_180,
     author = {Vastrade, Martin and Etoundi, Emilie and Bournonville, Thibaut and Colinet, Mathilde and Debortoli, Nicolas and Hedtke, Shannon M. and Nicolas, Emilien and Pigneur, Lise-Marie and Virgo, Julie and Flot, Jean-Fran\c{c}ois and Marescaux, Jonathan and Van Doninck, Karine},
     title = {Substantial genetic mixing among sexual and androgenetic lineages within the clam genus {\protect\emph{Corbicula}}},
     journal = {Peer Community Journal},
     eid = {e73},
     publisher = {Peer Community In},
     volume = {2},
     year = {2022},
     doi = {10.24072/pcjournal.180},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.180/}
}
TY  - JOUR
AU  - Vastrade, Martin
AU  - Etoundi, Emilie
AU  - Bournonville, Thibaut
AU  - Colinet, Mathilde
AU  - Debortoli, Nicolas
AU  - Hedtke, Shannon M.
AU  - Nicolas, Emilien
AU  - Pigneur, Lise-Marie
AU  - Virgo, Julie
AU  - Flot, Jean-François
AU  - Marescaux, Jonathan
AU  - Van Doninck, Karine
TI  - Substantial genetic mixing among sexual and androgenetic lineages within the clam genus Corbicula
JO  - Peer Community Journal
PY  - 2022
VL  - 2
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.180/
DO  - 10.24072/pcjournal.180
ID  - 10_24072_pcjournal_180
ER  - 
%0 Journal Article
%A Vastrade, Martin
%A Etoundi, Emilie
%A Bournonville, Thibaut
%A Colinet, Mathilde
%A Debortoli, Nicolas
%A Hedtke, Shannon M.
%A Nicolas, Emilien
%A Pigneur, Lise-Marie
%A Virgo, Julie
%A Flot, Jean-François
%A Marescaux, Jonathan
%A Van Doninck, Karine
%T Substantial genetic mixing among sexual and androgenetic lineages within the clam genus Corbicula
%J Peer Community Journal
%D 2022
%V 2
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.180/
%R 10.24072/pcjournal.180
%F 10_24072_pcjournal_180
Vastrade, Martin; Etoundi, Emilie; Bournonville, Thibaut; Colinet, Mathilde; Debortoli, Nicolas; Hedtke, Shannon M.; Nicolas, Emilien; Pigneur, Lise-Marie; Virgo, Julie; Flot, Jean-François; Marescaux, Jonathan; Van Doninck, Karine. Substantial genetic mixing among sexual and androgenetic lineages within the clam genus Corbicula. Peer Community Journal, Volume 2 (2022), article  no. e73. doi : 10.24072/pcjournal.180. https://peercommunityjournal.org/articles/10.24072/pcjournal.180/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100137

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Araujo, R.; Moreno, D.; Ramos, M. The Asiatic clam Corbicula fluminea (Müller, 1974) (Bivalvia: Corbiculidae) in Europe, American Malacological Bulletin, Volume 10 (1993)

[2] Bah, T. Inkscape. Guide to a vector drawing program, 4th edition. Prentice Hall, 2011 (https://inkscape.org/)

[3] Barton, N. H. Why Sex and Recombination?, Cold Spring Harbor Symposia on Quantitative Biology, Volume 74 (2009), pp. 187-195 | DOI

[4] Bast, J.; Parker, D. J.; Dumas, Z.; Jalvingh, K. M.; Tran Van, P.; Jaron, K. S.; Figuet, E.; Brandt, A.; Galtier, N.; Schwander, T. Consequences of Asexuality in Natural Populations: Insights from Stick Insects, Molecular Biology and Evolution, Volume 35 (2018) no. 7, pp. 1668-1677 | DOI

[5] Birky, C. W.; Adams, J.; Gemmel, M.; Perry, J. Using Population Genetic Theory and DNA Sequences for Species Detection and Identification in Asexual Organisms, PLoS ONE, Volume 5 (2010) no. 5 | DOI

[6] Birky, C. W. Species Detection and Identification in Sexual Organisms Using Population Genetic Theory and DNA Sequences, PLoS ONE, Volume 8 (2013) no. 1 | DOI

[7] Birky, C. W.; Maughan, H. Evolutionary Genetic Species Detected in Prokaryotes by Applying the K/θ Ratio to DNA Sequences, bioRxiv, 2021 | DOI

[8] Bespalaya, Y. V.; Bolotov, I. N.; Aksenova, O. V.; Kondakov, A. V.; Gofarov, M. Y.; Laenko, T. M.; Sokolova, S. E.; Shevchenko, A. R.; Travina, O. V. Aliens are moving to the Arctic frontiers: an integrative approach reveals selective expansion of androgenic hybrid Corbicula lineages towards the North of Russia, Biological Invasions, Volume 20 (2018) no. 8, pp. 2227-2243 | DOI

[9] Bespalaya, Y. V.; Aksenova, O. V.; Gofarov, M. Y.; Kondakov, A. V.; Kropotin, A. V.; Kononov, O. D.; Bolotov, I. N. Who inhabits the world’s deepest crater lake? A taxonomic review of Corbicula (Bivalvia: Cyrenidae) clams from Lake Toba, North Sumatra, Indonesia, Journal of Zoological Systematics and Evolutionary Research, Volume 59 (2020) no. 2, pp. 400-410 | DOI

[10] Bode, S.; Adolfsson, S.; Lamatsch, D.; Martins, M.; Schmit, O.; Vandekerkhove, J.; Mezquita, F.; Namiotko, T.; Rossetti, G.; Schön, I.; Butlin, R.; Martens, K. Exceptional cryptic diversity and multiple origins of parthenogenesis in a freshwater ostracod, Molecular Phylogenetics and Evolution, Volume 54 (2010) no. 2, pp. 542-552 | DOI

[11] Coughlan, N.; Cuthbert, R.; Potts, S.; Cunningham, E.; Crane, K.; Caffrey, J.; Lucy, F.; Davis, E.; Dick, J. Beds Are Burning: eradication and control of invasive Asian clam, Corbicula fluminea, with rapid open-flame burn treatments, Management of Biological Invasions, Volume 10 (2019) no. 3, pp. 486-499 | DOI

[12] Crespo, D.; Dolbeth, M.; Leston, S.; Sousa, R.; Pardal, M. Â. Distribution of Corbicula fluminea (Müller, 1774) in the invaded range: a geographic approach with notes on species traits variability, Biological Invasions, Volume 17 (2015) no. 7, pp. 2087-2101 | DOI

[13] Debortoli, N.; Li, X.; Eyres, I.; Fontaneto, D.; Hespeels, B.; Tang, C. Q.; Flot, J.-F.; Van Doninck, K. Genetic Exchange among Bdelloid Rotifers Is More Likely Due to Horizontal Gene Transfer Than to Meiotic Sex, Current Biology, Volume 26 (2016) no. 6, pp. 723-732 | DOI

[14] Dimijian, G. G. Evolution of Sexuality: Biology and Behavior, Baylor University Medical Center Proceedings, Volume 18 (2005) no. 3, pp. 244-258 | DOI

[15] Dmitriev, D. A.; Rakitov, R. A. Decoding of Superimposed Traces Produced by Direct Sequencing of Heterozygous Indels, PLoS Computational Biology, Volume 4 (2008) no. 7 | DOI

[16] Doyle, J. J. The Irrelevance of Allele Tree Topologies for Species Delimitation, and a Non-Topological Alternative, Systematic Botany, Volume 20 (1995) no. 4 | DOI

[17] Flot, J.-F.; Tillier, A.; Samadi, S.; Tillier, S. Phase determination from direct sequencing of length-variable DNA regions, Molecular Ecology Notes, Volume 6 (2006) no. 3, pp. 627-630 | DOI

[18] Flot, J.-F. champuru 1.0: a computer software for unraveling mixtures of two DNA sequences of unequal lengths, Molecular Ecology Notes, Volume 7 (2007) no. 6, pp. 974-977 | DOI

[19] Flot, J.-F.; Magalon, H.; Cruaud, C.; Couloux, A.; Tillier, S. Patterns of genetic structure among Hawaiian corals of the genus Pocillopora yield clusters of individuals that are compatible with morphology, Comptes Rendus Biologies, Volume 331 (2008) no. 3, pp. 239-247 | DOI

[20] Flot, J. seqPHASE: a web tool for interconverting PHASE input/output files and FASTA sequence alignments, Molecular Ecology Resources, Volume 10 (2010) no. 1, pp. 162-166 | DOI

[21] Flot, J.-F.; Couloux, A.; Tillier, S. Haplowebs as a graphical tool for delimiting species: a revival of Doyle's "field for recombination" approach and its application to the coral genus Pocillopora in Clipperton, BMC Evolutionary Biology, Volume 10 (2010) no. 1 | DOI

[22] Glaubrecht, M.; von Rintelen, T.; Korniushin, A. Toward a systematic revision of brooding freshwater Corbiculidae in Southeast Asia (Bilvavia, Veneroida): on shell morphology, anatomy and molecular phylogenetics of endemic taxa from islands in Indonesia, Malacologia, Volume 45 (2003)

[23] Glaubrecht, M.; Fehér, Z.; von Rintelen, T. Brooding in Corbicula madagascariensis (Bivalvia, Corbiculidae) and the repeated evolution of viviparity in corbiculids, Zoologica Scripta, Volume 35 (2006) no. 6, pp. 641-654 | DOI

[24] Gomes, C.; Sousa, R.; Mendes, T.; Borges, R.; Vilares, P.; Vasconcelos, V.; Guilhermino, L.; Antunes, A. Low Genetic Diversity and High Invasion Success of Corbicula fluminea (Bivalvia, Corbiculidae) (Müller, 1774) in Portugal, PLOS ONE, Volume 11 (2016) no. 7 | DOI

[25] Gomes, C.; Mendes, T.; Borges, R.; Guarneri, I.; Marchi, I.; Guilhermino, L.; Vasconcelos, V.; Riccardi, N.; Antunes, A. The genetic diversity of two invasive sympatric bivalves (Corbicula fluminea and Dreissena polymorpha) from Lakes Garda and Maggiore, Northern Italy, Journal of Great Lakes Research, Volume 46 (2020) no. 1, pp. 225-229 | DOI

[26] Hall, T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT, Nucleic Acids Research, Volume 41 (1999)

[27] Haponski, A. E.; Ó Foighil, D. Phylogenomic analyses confirm a novel invasive North American Corbicula (Bivalvia: Cyrenidae) lineage, PeerJ, Volume 7 (2019) | DOI

[28] Hartfield, M.; Keightley, P. D. Current hypotheses for the evolution of sex and recombination, Integrative Zoology, Volume 7 (2012) no. 2, pp. 192-209 | DOI

[29] Hedtke, S. M.; Stanger-Hall, K.; Baker, R. J.; Hillis, D. M. All-male asexuality: origin and maintenance of androgenesis in the asian clam corbicula, Evolution, Volume 62 (2008) no. 5, pp. 1119-1136 | DOI

[30] Hedtke, S. Origin and maintenance of androgenesis: male asexual reproduction in the clam genus Corbicula, Thesis dissertation, University of Texas at Austin (2009), 129 pages

[31] Hedtke, S. M.; Glaubrecht, M.; Hillis, D. M. Rare gene capture in predominantly androgenetic species, Proceedings of the National Academy of Sciences, Volume 108 (2011) no. 23, pp. 9520-9524 | DOI

[32] Hedtke, S. M.; Hillis, D. M. The Potential Role of Androgenesis in Cytoplasmic–Nuclear Phylogenetic Discordance, Systematic Biology, Volume 60 (2011) no. 1, pp. 87-96 | DOI

[33] Hillis, D. M.; Patton, J. C. Morphological and Electrophoretic Evidence for Two Species of Corbicula (Bivalvia: Corbiculidae) in North America, American Midland Naturalist, Volume 108 (1982) no. 1 | DOI

[34] Hotta, M.; Komaru, A. The Process of First Polar Body Formation in Eggs of the Androgenetic Clam Corbicula fluminea, Journal of Shellfish Research, Volume 37 (2018) no. 1, pp. 131-137 | DOI

[35] Houki, S.; Yamada, M.; Honda, T.; Komaru, A. Origin and Possible Role of Males in Hermaphroditic Androgenetic Corbicula Clams, Zoological Science, Volume 28 (2011) no. 7, pp. 526-531 | DOI

[36] Ishibashi, R.; Komaru, A.; Ookubo, K.; Kiyomoto, M. The Second Meiosis Occurs in Cytochalasin D-Treated Eggs of Corbicula leana Even Though It Is Not Observed in Control Androgenetic Eggs because the Maternal Chromosomes and Centrosomes Are Extruded at First Meiosis, Developmental Biology, Volume 244 (2002) no. 1, pp. 37-43 | DOI

[37] Ishibashi, R.; Ookubo, K.; Aoki, M.; Utaki, M.; Komaru, A.; Kawamura, K. Androgenetic Reproduction in a Freshwater Diploid Clam Corbicula fluminea (Bivalvia: Corbiculidae), Zoological Science, Volume 20 (2003) no. 6, pp. 727-732 | DOI

[38] Ishibashi, R.; Komaru, A. Abortive second meiosis detected in cytochalasin-treated eggs in androgenetic diploid Corbicula fluminea, Development, Growth and Differentiation, Volume 48 (2006) no. 4, pp. 277-282 | DOI

[39] Katoh, K.; Rozewicki, J.; Yamada, K. D. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization, Briefings in Bioinformatics, Volume 20 (2017) no. 4, pp. 1160-1166 | DOI

[40] Komaru, A.; Konishi, K.; Nakayama, I.; Kobayashi, T.; Sakai, H.; Kawamura, K. Hermaphroditic Freshwater Clams in the Genus Corbicula Produce Non-Reductional Spermatozoa With Somatic DNA Content, The Biological Bulletin, Volume 193 (1997) no. 3, pp. 320-323 | DOI

[41] Komaru, A.; Konishi, K. Non-reductional Spermatozoa in Three Shell Color Types of the Freshwater Clam Corbicula fluminea in Taiwan, Zoological Science, Volume 16 (1999) no. 1, pp. 105-108 | DOI

[42] Komaru, A.; Ookubo, K.; Kiyomoto, M. All meiotic chromosomes and both centrosomes at spindle pole in the zygotes discarded as two polar bodies in clam Corbicula leana : unusual polar body formation observed by antitubulin immunofluorescence, Development Genes and Evolution, Volume 210 (2000) no. 5, pp. 263-269 | DOI

[43] Komaru, A.; Kumamoto, A.; Kato, T.; Ishibashi, R.; Obata, M.; Nemoto, T. A Hypothesis of Ploidy Elevation by Formation of a Female Pronucleus in the Androgenetic Clam Corbicula fluminea in the Tone River Estuary, Japan, Zoological Science, Volume 23 (2006) no. 6, pp. 529-532 | DOI

[44] Komaru, A.; Houki, S.; Yamada, M.; Miyake, T.; Obata, M.; Kawamura, K. 28S rDNA haplotypes of males are distinct from those of androgenetic hermaphrodites in the clam Corbicula leana, Development Genes and Evolution, Volume 222 (2012) no. 3, pp. 181-187 | DOI

[45] Komaru, A.; Yamada, M.; Houki, S. Relationship Between Two Androgenetic Clam Species, Corbicula leana and Corbicula fluminea, Inferred from Mitochondrial Cytochrome b and Nuclear 28S rRNA Markers, Zoological Science, Volume 30 (2013) no. 5, pp. 360-365 | DOI

[46] Korniushin, A. V. A revision of some Asian and African freshwater clams assigned to Corbicula fluminalis (Müller, 1774) (Mollusca: Bivalvia: Corbiculidae), with a review of anatomical characters and reproductive features based on museum collections, Hydrobiologia, Volume 529 (2004) no. 1, pp. 255-270 | DOI

[47] Kraemer, L.; Swanson, C.; Galloway, M.; Kraemer, R. Biological basis of behavior in Corbicula fluminea. II. Functional morphology of reproduction and development and review of evidence for self-fertilization, American Malacolical Bulletin Spec. Ed., Volume 2 (1986)

[48] Krzywinski, M.; Schein, J.; Birol, İ.; Connors, J.; Gascoyne, R.; Horsman, D.; Jones, S. J.; Marra, M. A. Circos: An information aesthetic for comparative genomics, Genome Research, Volume 19 (2009) no. 9, pp. 1639-1645 | DOI

[49] Lee, T.; Siripattrawan, S.; Ituarte, C.; Ò Foighil, D. Invasion of the clonal clams: Corbicula lineages in the New World, American Malacological Bulletin, Volume 20 (2005)

[50] Lehtonen, J.; Jennions, M. D.; Kokko, H. The many costs of sex, Trends in Ecology and Evolution, Volume 27 (2012) no. 3, pp. 172-178 | DOI

[51] Lehtonen, J.; Schmidt, D. J.; Heubel, K.; Kokko, H. Evolutionary and ecological implications of sexual parasitism, Trends in Ecology and Evolution, Volume 28 (2013) no. 5, pp. 297-306 | DOI

[52] Lenormand, T.; Engelstädter, J.; Johnston, S. E.; Wijnker, E.; Haag, C. R. Evolutionary mysteries in meiosis, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 371 (2016) no. 1706 | DOI

[53] Librado, P.; Rozas, J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data, Bioinformatics, Volume 25 (2009) no. 11, pp. 1451-1452 | DOI

[54] Liegeois, M.; Sartori, M.; Schwander, T. Extremely Widespread Parthenogenesis and a Trade-Off Between Alternative Forms of Reproduction in Mayflies (Ephemeroptera), Journal of Heredity, Volume 112 (2020) no. 1, pp. 45-57 | DOI

[55] Lopez-Soriano, J.; Quiñonero-Salgado, S.; Cappelletti, C.; Faccenda, F.; Ciutti, F. Unraveling the complexity of Corbicula clams invasion in Lake Garda (Italy), Advances in Oceanography and Limnology, Volume 9 (2018) no. 2 | DOI

[56] Mantovani, B.; Passamonti, M.; Scali, V. The Mitochondrial Cytochrome Oxidase II Gene in Bacillus Stick Insects: Ancestry of Hybrids, Androgenesis, and Phylogenetic Relationships, Molecular Phylogenetics and Evolution, Volume 19 (2001) no. 1, pp. 157-163 | DOI

[57] Marescaux, J.; Pigneur, L.-M.; Van Doninck, K. New records of Corbicula clams in French rivers, Aquatic Invasions, Volume 5 (2010) no. Supplement 1 | DOI

[58] McKone, M. J.; Halpern, S. L. The Evolution of Androgenesis, The American Naturalist, Volume 161 (2003) no. 4, pp. 641-656 | DOI

[59] McMahon, R. The occurrence and spread of the introduced Asiatic freshwater clam, Corbicula fluminea (Muller), in North America: 1924-1982, Nautilus, Volume 96 (1982)

[60] Meijer, T.; Preece, R. A review of the occurrence of Corbicula in the Pleistocene of North-West Europe, Netherlands Journal of Geosciences, Volume 79 (2000) no. 2-3, pp. 241-255 | DOI

[61] Milani, L.; Scali, V.; Passamonti, M. Speciation through androgenesis in the stick insect genus Clonopsis (Insecta Phasmatodea), Journal of Zoological Systematics and Evolutionary Research, Volume 53 (2015) no. 2, pp. 116-123 | DOI

[62] Milani, L.; Scali, V.; Punzi, E.; Luchetti, A.; Ghiselli, F. The puzzling taxonomic rank of Pijnackeria hispanica, a chimerical hybrid androgen (Insecta, Phasmida), Organisms Diversity and Evolution, Volume 20 (2020) no. 2, pp. 285-297 | DOI

[63] Minchin, D. The distribution of the Asian clam Corbicula fluminea and its potential to spread in Ireland, Management of Biological Invasions, Volume 5 (2014) no. 2, pp. 165-177 | DOI

[64] Mouthon, J. Sur la présence en France et au Portugal de Corbicula (Bivalvia, Corbiculidae) originaire d'Asie, Basteria, Volume 45 (1981)

[65] Neiman, M.; Hehman, G.; Miller, J. T.; Logsdon, J. M.; Taylor, D. R. Accelerated Mutation Accumulation in Asexual Lineages of a Freshwater Snail, Molecular Biology and Evolution, Volume 27 (2010) no. 4, pp. 954-963 | DOI

[66] Obata, M.; Nishimori, K.; Komaru, A. Change of centrosome attachment site causes androgenesis in the freshwater clam Corbicula fluminea: Comparison with C. sandai. , Venus, Volume 65 (2006)

[67] Okamoto, A.; Arimoto, B. Chromosomes of Corbicula japonica, C. sandai and C. (Corbiculina) leana (Bivalvia: Corbiculidae), Venus Jpn J. Malacol., Volume 45 (1986)

[68] Park, G.; Yong, T.; Im, K.; Chung, E. Karyotypes of three species of Corbicula (Bivalvia: Veneroida) In Korea, Journal of Shellfish Research, Volume 19 (2000)

[69] Park, J. Two Corbicula (Corbiculidae: Bivalvia) mitochondrial lineages are widely distributed in Asian freshwater environment, Molecular Phylogenetics and Evolution, Volume 29 (2003) no. 3, pp. 529-539 | DOI

[70] Patrick, C.; Waters, M.; Golladay, S. The distribution and ecological role of Corbicula fluminea (Müller, 1774) in a large and shallow reservoir, BioInvasions Records, Volume 6 (2017) no. 1, pp. 39-48 | DOI

[71] Peñarrubia, L.; Araguas, R.-M.; Vidal, O.; Pla, C.; Viñas, J.; Sanz, N. Genetic characterization of the Asian clam species complex (Corbicula) invasion in the Iberian Peninsula, Hydrobiologia, Volume 784 (2017) no. 1, pp. 349-365 | DOI

[72] Pfenninger, M.; Reinhardt, F.; Streit, B. Evidence for cryptic hybridization between different evolutionary lineages of the invasive clam genus Corbicula (Veneroida, Bivalvia), Journal of Evolutionary Biology, Volume 15 (2002) no. 5, pp. 818-829 | DOI

[73] Pichot, C.; El Maâtaoui, M.; Raddi, S.; Raddi, P. Surrogate mother for endangered Cupressus, Nature, Volume 412 (2001) no. 6842, p. 39-39 | DOI

[74] Pigneur, L.-M.; Marescaux, J.; Roland, K.; Etoundi, E.; Descy, J.-P.; Van Doninck, K. Phylogeny and androgenesis in the invasive Corbicula clams (Bivalvia, Corbiculidae) in Western Europe, BMC Evolutionary Biology, Volume 11 (2011) no. 1 | DOI

[75] Pigneur, L.; Risterucci, A.; Dauchot, N.; Li, X.; Van Doninck, K. Development of novel microsatellite markers to identify the different invasive lineages in the Corbicula complex and to assess androgenesis, Molecular Ecology Resources, Volume 11 (2011) no. 3, pp. 573-577 | DOI

[76] Pigneur, L.-M.; Hedtke, S. M.; Etoundi, E.; Van Doninck, K. Androgenesis: a review through the study of the selfish shellfish Corbicula spp., Heredity, Volume 108 (2012) no. 6, pp. 581-591 | DOI

[77] Pigneur, L.-M.; Etoundi, E.; Aldridge, D. C.; Marescaux, J.; Yasuda, N.; Van Doninck, K. Genetic uniformity and long-distance clonal dispersal in the invasive androgenetic Corbicula clams, Molecular Ecology, Volume 23 (2014) no. 20, pp. 5102-5116 | DOI

[78] Pilsbury, H.; Bequaert, J. The aquatic molluscs of the Belgian Congo, with a geographical and ecological account of Congo malacology, Bull. Amer. Mus. Nat. Hist., Volume 53 (1927)

[79] Qiu, A.; Shi, A.; Komaru, A. Yellow and brown shell color morphs of Corbicula fluminea (Bivalva: Corbiculidae) from Sichuan Province, China, are triploids and tetraploids, Journal of Shellfish Research, Volume 20 (2001)

[80] Rey, O.; Facon, B.; Foucaud, J.; Loiseau, A.; Estoup, A. Androgenesis is a maternal trait in the invasive ant Wasmannia auropunctata, Proceedings of the Royal Society B: Biological Sciences, Volume 280 (2013) no. 1766 | DOI

[81] Reyna, P.; Nori, J.; Ballesteros, M. L.; Hued, A. C.; Tatián, M. Targeting clams: insights into the invasive potential and current and future distribution of Asian clams, Environmental Conservation, Volume 45 (2018) no. 4, pp. 387-395 | DOI

[82] Sagata, N. Meiotic metaphase arrest in animal oocytes: its mechanisms and biological significance, Trends in Cell Biology, Volume 6 (1996) no. 1, pp. 22-28 | DOI

[83] Sano, N.; Houki, S.; Kodan, A.; Kawamura, K.; Yamada, M.; Komaru, A. Genetic confirmation of “egg parasitism” in androgenetic freshwater Corbicula clams by paternity testing using microsatellite DNA markers, Plankton and Benthos Research, Volume 15 (2020) no. 1, pp. 58-62 | DOI

[84] Simon, J.-C.; Delmotte, F.; Rispe, C.; Crease, T. Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals, Biological Journal of the Linnean Society, Volume 79 (2003) no. 1, pp. 151-163 | DOI

[85] Schön, I.; Pinto, R. L.; Halse, S.; Smith, A. J.; Martens, K.; Birky, C. W. Cryptic Species in Putative Ancient Asexual Darwinulids (Crustacea, Ostracoda), PLoS ONE, Volume 7 (2012) no. 7 | DOI

[86] Schwander, T.; Crespi, B. J. Multiple direct transitions from sexual reproduction to apomictic parthenogenesis in Timema stick insects, Evolution, Volume 63 (2009) no. 1, pp. 84-103 | DOI

[87] Schwander, T.; Oldroyd, B. P. Androgenesis: where males hijack eggs to clone themselves, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 371 (2016) no. 1706 | DOI

[88] Sequencher® version 4.1.4 DNA sequence analysis software, Gene Codes Corporation, Ann Arbor, MI USA (http://www.genecodes.com)

[89] Siripattrawan, S.; Park, J.-K.; Foighil, D. Ó. Two lineages of the introduced Asian freshwater clam Corbicula occur in North America, Journal of Molluscan Studies, Volume 66 (2000) no. 3, pp. 423-429 | DOI

[90] Skuza, L.; Łabęcka, A. M.; Domagała, J. Cytogenetic and Morphological Characterization of Corbicula fluminalis (O. F. Müller, 1774) (Bivalvia: Veneroida: Corbiculidae): Taxonomic Status Assessment of a Freshwater Clam, Folia Biologica, Volume 57 (2009) no. 3, pp. 177-185 | DOI

[91] Spöri, Y.; Flot, J. HaplowebMaker and CoMa: Two web tools to delimit species using haplowebs and conspecificity matrices, Methods in Ecology and Evolution, Volume 11 (2020) no. 11, pp. 1434-1438 | DOI

[92] Spöri, Y.; Stoch, F.; Dellicour, S.; Birky, C. W.; Flot, J.-F. KoT: an automatic implementation of the K/θ method for species delimitation, bioRxiv, Volume 2021.08.17.454531, 2022 | DOI

[93] Stephens, M.; Smith, N. J.; Donnelly, P. A New Statistical Method for Haplotype Reconstruction from Population Data, The American Journal of Human Genetics, Volume 68 (2001) no. 4, pp. 978-989 | DOI

[94] Tiemann, J.; Haponski, A.; Douglass, S.; Lee, T.; Cummings, K.; Davis, M.; Ó Foighil, D. First record of a putative novel invasive Corbicula lineage discovered in the Illinois River, Illinois, USA, BioInvasions Records, Volume 6 (2017) no. 2, pp. 159-166 | DOI

[95] van der Kooi, C. J.; Schwander, T. On the fate of sexual traits under asexuality, Biological Reviews, Volume 89 (2014) no. 4, pp. 805-819 | DOI

[96] Vastrade, M.; Etoundi, E.; Bournonville, T.; Colinet, M.; Debortoli, N.; Hedtke, S.; Nicolas, E.; Pigneur, L.-M.; Virgo, J.; Flot, J.-F.; Marescaux, J.; Van Doninck, K. Data of Substantial genetic mixing among sexual and androgenetic lineages within the clam genus Corbicula, Zenodo, 2022 | DOI

[97] Voroshilova, I. S.; Pryanichnikova, E. G.; Prokin, A. A.; Sabitova, R. Z.; Karabanov, D. P.; Pavlov, D. D.; Kurina, E. M. Morphological and Genetic Traits of the First Invasive Population of the Asiatic Clam Corbicula fluminea (O.F. Müller, 1774) Naturalized in the Volga River Basin, Russian Journal of Biological Invasions, Volume 12 (2021) no. 1, pp. 36-43 | DOI

[98] Yamada, M.; Ishibashi, R.; Toyoda, K.; Kawamura, K.; Komaru, A. Phylogeography of the Brackish Water Clam Corbicula japonica Around the Japanese Archipelago Inferred from Mitochondrial COII Gene Sequences, Zoological Science, Volume 31 (2014) no. 3, pp. 168-179 | DOI

[99] Zhao, S.; Guo, Y.; Sheng, Q.; Shyr, Y. Advanced Heat Map and Clustering Analysis Using Heatmap3, BioMed Research International (2014) | DOI

Cited by Sources: