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An Unusual Evolutionary Strategy: The Origins, Genetic Repertoire, and Implications of Doubly Uniparental Inheritance of Mitochondrial DNA in Bivalves

Abstract

Mitochondrial DNA (mtDNA) is typically passed on to progeny only by the female parent. The phenomenon of “doubly uniparental inheritance” (DUI) of mtDNA in many bivalve species is a fascinating exception to the paradigm of strict maternal inheritance of mtDNA. In this review, we survey the current state of knowledge of DUI and discuss several active areas of research in this field. Topics/questions covered include: the number of times DUI evolved (once or multiple origins), the link between DUI and sex determination, the role(s) of mtDNA-encoded non-oxidative phosphorylation genes (i.e. ORFan/orf genes) in freshwater mussels, the function of conserved sequence motifs and sperm transmission elements in mtDNA of marine mussels, the challenges of annotating mtDNA genomes of DUI species, the presence of unorthodox features in venerid mtDNA, whether or not orf DNA sequences are useful in species-level identification of freshwater mussel, and finally, whether or not there are obvious benefits of DUI. For each topic, we also highlight important avenues for future research within this fascinating field of mitochondrial evolutionary biology.

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References

  • Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJ, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–465

    CAS  CrossRef  Google Scholar 

  • Allen JF (1996) Separate sexes and the mitochondrial theory of ageing. J Theor Biol 180:135–140

    CAS  CrossRef  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402

    CAS  CrossRef  Google Scholar 

  • Bauer G (1987) Reproductive strategy of the freshwater pearl mussel Margaritifera margaritifera. J Anim Ecol 56:691–704

    Google Scholar 

  • Bayrer JR, Zhang W, Weiss MA (2005) Dimerization of doublesex is mediated by a cryptic ubiquitin-associated domain fold: implications for sex-specific gene regulation. J Biol Chem 280:32989–32996

    CAS  CrossRef  Google Scholar 

  • Bettinazzi S, Plazzi F, Passamonti M (2016) The complete female-and male-transmitted mitochondrial genome of Meretrix lamarckii. PloS one 11

    Google Scholar 

  • Bettinazzi S, Rodríguez E, Milani L, Blier PU, Breton S (2019) Metabolic remodelling associated with mtDNA: insights into the adaptive value of doubly uniparental inheritance of mitochondria. Proc Roy Soc B 286:20182708

    CAS  CrossRef  Google Scholar 

  • Bettinazzi S, Nadarajah S, Dalpé A, Milani L, Blier PU, Breton S (2020) Linking paternally inherited mtDNA variants and sperm performance. Phil Trans Roy Soc B 375:20190177

    CAS  CrossRef  Google Scholar 

  • Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27:1767–1780

    CAS  CrossRef  Google Scholar 

  • Boore JL, Medina M, Rosenberg LA (2004) Complete sequences of the highly rearranged molluscan mitochondrial genomes of the scaphopod Graptacme eborea and the bivalve Mytilus edulis. Mol Biol Evol 21:1492–1503

    CAS  CrossRef  Google Scholar 

  • Breton S, Burger G, Stewart DT, Blier PU (2006) Comparative analysis of gender-associated complete mitochondrial genomes in marine mussels (Mytilus spp.). Genetics 172:1107–1119

    CAS  CrossRef  Google Scholar 

  • Breton S, Beaupre HD, Stewart DT, Hoeh WR, Blier PU (2007) The unusual system of doubly uniparental inheritance of mtDNA: isn’t one enough? Trends Genet 23:465–474

    CAS  CrossRef  Google Scholar 

  • Breton S, Beaupré HD, Stewart DT, Piontkivska H, Karmakar M, Bogan AE, Blier PU, Hoeh WR (2009a) Comparative mitochondrial genomics of freshwater mussels (Bivalvia: Unionoida) with doubly uniparental inheritance of mtDNA: gender-specific open reading frames and putative origins of replication. Genetics 183:1575–1589

    CAS  CrossRef  Google Scholar 

  • Breton S, Stewart DT, Blier PU (2009b) Role-reversal of gender-associated mitochondrial DNA affects mitochondrial function in Mytilus edulis (Bivalvia: Mytilidae). J Exp Zool B 312:108–117

    CrossRef  CAS  Google Scholar 

  • Breton S, Stewart DT, Hoeh WR (2010) Characterization of a mitochondrial ORF from the gender-associated mtDNAs of Mytilus spp. (Bivalvia: Mytilidae): identification of the “missing” ATPase 8 gene. Mar Genomics 3:11–18

    CrossRef  Google Scholar 

  • Breton S, Stewart DT, Shepardson S, Trdan RJ, Bogan AE, Chapman EG, Ruminas AJ, Piontkivska H, Hoeh WR (2011a) Novel protein genes in animal mtDNA: a new sex determination system in freshwater mussels (Bivalvia: Unionoida)? Mol Biol Evol 28:1645–1659

    CAS  CrossRef  Google Scholar 

  • Breton S, Ghiselli F, Passamonti M, Milani L, Stewart DT, Hoeh WR (2011b) Evidence for a fourteenth mtDNA-encoded protein in the female-transmitted mtDNA of marine mussels (Bivalvia: Mytilidae). PLoS ONE 6:e19365

    CAS  CrossRef  Google Scholar 

  • Breton S, Milani L, Ghiselli F, Guerra D, Stewart DT, Passamonti M (2014) A resourceful genome: updating the functional repertoire and evolutionary role of animal mitochondrial DNAs. Trends Genet 30:555–564

    CAS  CrossRef  Google Scholar 

  • Burt A, Trivers R (2006) Selfish mitochondrial DNA. Genes in Conflict: the biology of selfish genetic elements. Belknap Press of Harvard University, Cambridge, MA

    Google Scholar 

  • Burzyński A, Zbawicka M, Skibinski DOF, Wenne R (2003) Evidence for recombination of mtDNA in the marine mussel Mytilus trossulus from the Baltic. Mol Biol Evol 20:388–392

    CrossRef  Google Scholar 

  • Cao L, Kenchington E, Zouros E (2004a) Differential segregation patterns of sperm mitochondria in embryos of the blue mussel (Mytilus edulis). Genetics 166:883–894

    CrossRef  Google Scholar 

  • Cao L, Kenchington E, Zouros E, Rodakis GC (2004b) Evidence that the large noncoding sequence is the main control region of maternally and paternally transmitted mitochondrial genomes of the marine mussel (Mytilus spp.). Genetics 167:835–850

    CAS  CrossRef  Google Scholar 

  • Cao L, Ort BS, Mizi A, Pogson G, Kenchington E, Zouros E, Rodakis GC (2009) The control region of maternally and paternally inherited mitochondrial genomes of three species of the sea mussel genus Mytilus. Genetics 181:1045–1056

    CAS  CrossRef  Google Scholar 

  • Capt C, Renaut S, Ghiselli F, Milani L, Johnson NA, Sietman BE, Stewart DT, Breton S (2018) Deciphering the link between doubly uniparental inheritance of mtDNA and sex determination in bivalves: clues from comparative transcriptomics. Genome Biol Evol 10:577–590

    CAS  CrossRef  Google Scholar 

  • Capt C, Renaut S, Stewart DT, Johnson NA, Breton S (2019) Putative mitochondrial sex determination in the Bivalvia: insights from a hybrid transcriptome assembly in freshwater mussels. Frontiers Genet 10:840

    CAS  CrossRef  Google Scholar 

  • Capt C, Bouvet K, Guerra D, Robicheau BM, Stewart DT, Pante E, Breton S (2020) Unorthodox features in two venerid bivalves with doubly uniparental inheritance of mitochondria. Sci Reports 10:1–3

    Google Scholar 

  • Chakrabarti R, Walker JM, Stewart DT, Trdan RJ, Vijayaraghavana S, Curole JP, Hoeh WR (2006) Presence of a unique male-specific extension of C-terminus to the cytochrome c oxidase subunit II protein coded by the male-transmitted mitochondrial genome of Venustaconcha ellipsiformis (Bivalvia: Unionoidea). FEBS Lett 580:862–866

    CAS  CrossRef  Google Scholar 

  • Chakrabarti R, Walker JM, Chapman EG, Shepardson SP, Trdan RJ, Curole JP, Watters GT, Stewart DT, Vijayaraghavana S, Hoeh WR (2007) Reproductive function for a C-terminus extended, male-transmitted cytochrome c oxidase subunit II protein expressed in both spermatozoa and eggs. FEBS Lett 581:5213–5219

    CAS  CrossRef  Google Scholar 

  • Chapman EG, Piontkivska H, Walker JM, Stewart DT, Curole JP, Hoeh WR (2008) Extreme primary and secondary protein structure variability in the chimeric male-transmitted cytochrome c oxidase subunit II protein in freshwater mussels: Evidence for an elevated amino acid substitution rate in the face of domain-specific purifying selection. BMC Evol Biol 8:165

    CrossRef  CAS  Google Scholar 

  • Chase EE, Robicheau BM, Veinot S, Breton S, Stewart DT (2018) The complete mitochondrial genome of the hermaphroditic freshwater mussel Anodonta cygnea (Bivalvia: Unionidae): in silico analyses of sex-specific ORFs across order Unionoida. BMC Genom 19:221

    CAS  CrossRef  Google Scholar 

  • Cogswell AT, Kenchington ELR, Zouros E (2006) Segregation of sperm mitochondria in two- and four-cell embryos of the blue mussel Mytilus edulis: implications for the mechanism of doubly uniparental inheritance of mitochondrial DNA. Genome 49:799–807

    CAS  CrossRef  Google Scholar 

  • Collin R (2013) Phylogenetic patterns and phenotypic plasticity of molluscan sexual systems. Integ Comp Biol 53:723–735

    CrossRef  Google Scholar 

  • Curole JP, Kocher TD (2002) Ancient sex-specific extension of the cytochrome c oxidase II gene in bivalves and the fidelity of doubly-uniparental inheritance. Mol Biol Evol 19:1323–1328

    CAS  CrossRef  Google Scholar 

  • Doucet-Beaupré H, Breton S, Chapman EG, Blier PU, Bogan AE, Stewart DT, Hoeh WR (2010) Mitochondrial phylogenomics of the Bivalvia (Mollusca): searching for the origin and mitogenomic correlates of doubly uniparental inheritance of mtDNA. BMC Evol Biol 10:50

    CrossRef  CAS  Google Scholar 

  • Everett EM, Williams PJ, Gibson G, Stewart DT (2004) Mitochondrial DNA polymorphisms and sperm motility in Mytilus edulis (Bivalvia: Mytilidae). J Exp Zool A 301:906–910

    CrossRef  CAS  Google Scholar 

  • Ferreira-Rodríguez N, Akiyama YB, Aksenova OV, Araujo R, Barnhart MC, Bespalaya YV, Bogan AE, Bolotov IN, Budha PB, Clavijo C, Clearwater SJ (2019) Research priorities for freshwater mussel conservation assessment. Biol Conser 231:77–87

    CrossRef  Google Scholar 

  • Fisher C, Skibinski DOF (1990) Sex-biased mitochondrial DNA heteroplasmy in the marine mussel Mytilus. Proc Roy Soc Lond (B) 242:149–156

    CrossRef  Google Scholar 

  • Fitzpatrick JL, Simmons LW, Evans JP (2012) Complex patterns of multivariate selection on the ejaculate of a broadcast spawning marine invertebrate. Evolution 66:2451–2460

    CrossRef  Google Scholar 

  • Garesse R, Vallejo CG (2001) Animal mitochondrial biogenesis and function: a regulatory cross-talk between two genomes. Gene 263:1–16

    CAS  CrossRef  Google Scholar 

  • Gemmell NJ, Metcalf VJ, Allendorf FW (2004) Mother’s curse: the effect of mtDNA on individual fitness and population viability. Trends Ecol Evol 19:238–244

    CrossRef  Google Scholar 

  • Ghiselin MT (1969) The evolution of hermaphroditism among animals. Quart Rev Biol 44:189–208

    CAS  CrossRef  Google Scholar 

  • Ghiselli F, Maurizii MG, Reunov A, Ariño-Bassols H, Cifaldi C, Pecci A, Alexandrova Y, Bettini S, Passamonti M, Franceschini V, Milani L (2019) Natural heteroplasmy and mitochondrial inheritance in bivalve molluscs. Integr Comp Biol 59:1016–1032

    CAS  CrossRef  Google Scholar 

  • Ghiselli F, Milani L, Chang PL et al (2012) De novo assembly of the manila clam Ruditapes philippinarum transcriptome provides new insights into expression bias, mitochondrial doubly uniparental inheritance and sex determination. Mol Biol Evol 29:771–786

    CAS  CrossRef  Google Scholar 

  • Ghiselli F, Milani L, Guerra D, Chang PL, Breton S, Nuzhdin SV, Passamonti M (2013) Structure, transcription, and variability of metazoan mitochondrial genome: perspectives from an unusual mitochondrial inheritance system. Genome Biol Evol 5:1535–1554

    CAS  CrossRef  Google Scholar 

  • Gissi C, Iannelli F, Pesole G (2008) Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species. Heredity 101:301–320

    CAS  CrossRef  Google Scholar 

  • Guerra D, Ghiselli F, Passamonti M (2014) The largest unassigned regions of the male and female-transmitted mitochondrial DNAs in Musculista senhousia (Bivalvia, Mytilidae). Gene 536:316–325

    CAS  CrossRef  Google Scholar 

  • Guerra D, Lopes-Lima M, Froufe E, Gan HM, Ondina P, Amaro R, Klunzinger MW, Callil C, Prié V, Bogan AE, Stewart DT (2019) Variability of mitochondrial ORFans hints at possible differences in the system of doubly uniparental inheritance of mitochondria among families of freshwater mussels (Bivalvia: Unionida). BMC Evol Biol 19

    Google Scholar 

  • Guerra D, Plazzi F, Stewart DT, Bogan AE, Hoeh WR, Breton S (2017) Evolution of sex-dependent mtDNA transmission in freshwater mussels (Bivalvia: Unionida). Sci Rep 7:1551

    CrossRef  CAS  Google Scholar 

  • Gusman A, Lecomte S, Stewart DT, Passamonti M, Breton S (2016) Pursuing the quest for better understanding the taxonomic distribution of the system of doubly uniparental inheritance of mtDNA. PeerJ 4:e2760

    CrossRef  CAS  Google Scholar 

  • Hansen D, Pilgrim D (1999) Sex and the single worm: sex determination in the nematode C. elegans. Mech Dev 83:3–15

    CAS  CrossRef  Google Scholar 

  • Hebert PDN, Gregory TR (2005) The promise of DNA barcoding for taxonomy. Syst Biol 54:852–859

    CrossRef  Google Scholar 

  • Hebert PDN, Ratnasingham S, de Waard JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc Roy Soc B 270:S96–S99

    CAS  Google Scholar 

  • Hodgkin J (1987) A genetic analysis of the sex-determining gene, tra-1, in the nematode Caenorhabditis elegans. Genes Dev 1:731–745

    CAS  CrossRef  Google Scholar 

  • Hoeh WR, Blakley KH, Brown WM (1991) Heteroplasmy suggests limited biparental inheritance of Mytilus mitochondrial DNA. Science 251:1488–1490

    CAS  CrossRef  Google Scholar 

  • Hoeh WR, Stewart DT, Saavedra C, Sutherland BW, Zouros E (1997) Phylogenetic evidence for role-reversals of gender-associated mitochondrial DNA in Mytilus (Bivalvia: Mytilidae). Mol Biol Evol 14:959–967

    CAS  CrossRef  Google Scholar 

  • Hoeh WR, Stewart DT, Guttman SI (2002) High fidelity of mitochondrial genome transmission under the doubly uniparental mode of inheritance in freshwater mussels (Bivalvia: Unionoidea). Evolution 56:2252–2261

    CAS  CrossRef  Google Scholar 

  • Hoffmann RJ, Boore JL, Brown WM (1992) A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics 131:397–412

    CAS  Google Scholar 

  • Huber M (2010) Compendium of bivalves. ConchBooks, Germany

    Google Scholar 

  • Hurst LD, Hoekstra RF (1994) Shellfish gees kept in line. Nature 368:817–818

    CrossRef  Google Scholar 

  • Inoue K, Hayes DM, Harris JL, Christian AD (2013) Phylogenetic and morphometric analyses reveal ecophenotypic plasticity in freshwater mussels Obovaria jacksoniana and Villosa arkansasensis (Bivalvia: Unionidae). Ecol Evol 3:2670–2683

    CrossRef  Google Scholar 

  • Jeratthitikul E, Phuangphong S, Sutcharit C et al (2019) Integrative taxonomy reveals phenotypic plasticity in the freshwater mussel Contradens contradens (Bivalvia: Unionidae) in Thailand, with a description of a new species. Syst Biodiv 17:134–147

    CrossRef  Google Scholar 

  • Jha M, Côté J, Hoeh WR, Blier PU, Stewart DT (2008) Sperm motility in Mytilus edulis in relation to mitochondrial DNA polymorphisms: implications for the evolution of doubly uniparental inheritance in bivalves. Evolution 62:99–106

    CAS  Google Scholar 

  • Kulkarni M, Smith HE (2008) E1 Ubiquitin-activating enzyme UBA-1 plays multiple roles throughout C. elegans development. PLoS Genet 4:e1000131

    Google Scholar 

  • Kyriakou E, Kravariti L, Vasilopoulos T, Zouros E, Rodakis GC (2015) A protein binding site in the M mitochondrial genome of Mytilus galloprovincialis may be responsible for its paternal transmission. Gene 562:83–94

    CAS  CrossRef  Google Scholar 

  • Kyriakou E, Kravariti L, Zouros E, Rodakis GC (2016) No sex-specific protein-binding site in the VD1 of the F mitochondrial genome of the mussel Mytilus galloprovincialis. Gene Rep 5:148–150

    CrossRef  Google Scholar 

  • Levitan Don R (2000) Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegatus. Proc Roy Sc Lond B 267:531–534

    CAS  CrossRef  Google Scholar 

  • Lee Y, Kwak H, Shin J, Kim SC, Kim T, Park JK (2019) A mitochondrial genome phylogeny of Mytilidae (Bivalvia: Mytilida). Mol Phylogenet Evol 139:106533

    CAS  CrossRef  Google Scholar 

  • Liu G, Innes D, Thompson RJ (2011) Quantitative analysis of sperm plane circular movement in the blue mussels Mytilus edulis, M. trossulus and their hybrids. J Exp Zool A 315A:280–290

    CrossRef  Google Scholar 

  • Lopes-Lima M, Burlakova LE, Karatayev AY, Mehler K, Seddon M, Sousa R (2018) Conservation of freshwater bivalves at the global scale: diversity, threats and research needs. Hydrobiologia 810:1–14

    CrossRef  Google Scholar 

  • Lopes-Lima M, Froufe E, Ghamizi M, Mock KE, Kebapçı Ü, Klishko O, Kovitvadhi S, Kovitvadhi U, Paulo OS, Pfeiffer JM III, Raley M (2017) Phylogeny of the most species-rich freshwater bivalve family (Bivalvia: Unionida: Unionidae): Defining modern subfamilies and tribes. Mol Phylogen Evol 106:174–191

    CrossRef  Google Scholar 

  • Lopes-Lima M, Teixeira A, Froufe E, Lopes A, Varandas S, Sousa R (2014) Biology and conservation of freshwater bivalves: past, present and future perspectives. Hydrobiologia 735(1):1–3

    Google Scholar 

  • Lubośny M, Przyłucka A, Śmietanka B, Breton S, Burzyński A (2018) Actively transcribed and expressed atp8 gene in Mytilus edulis mussels. PeerJ 6:e4897

    CrossRef  CAS  Google Scholar 

  • Lubośny M, Śmietanka B, Przyłucka A, Burzyński A (2020) Highly divergent mitogenomes of Geukensia demissa (Bivalvia, Mytilidae) with extreme AT content. J Zool Syst Evol Res https://doi.org/10.1111/jzs.12354

  • Lymbery RA, Kennington WJ, Evans JP (2017) Egg chemoattractants moderate intraspecific sperm competition. Evol Lett 1:317–327

    CrossRef  Google Scholar 

  • McCartney MA, Auch B, Kono T, Mallez S, Zhang Y, Obille A, Becker A, Abrahante JE, Garbe J, Badalamenti JP, Herman A (2019) The Genome of the Zebra Mussel, Dreissena polymorpha: A Resource for Invasive Species Research. BioRxiv 1:696732

    Google Scholar 

  • McGinnis S, Madden TL (2004) BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucl Acids Res 32:W20–W25

    CAS  CrossRef  Google Scholar 

  • Milani L (2015) Mitochondrial membrane potential: a trait involved in organelle inheritance? Biol Lett 11(10)

    Google Scholar 

  • Milani L, Ghiselli F (2015) Mitochondrial activity in gametes and transmission of viable mtDNA. Biol Direct 10:22

    CrossRef  CAS  Google Scholar 

  • Milani L, Ghiselli F, Guerra D, Breton S, Passamonti M (2013) A comparative analysis of mitochondrial ORFans: new clues on their origin and role in species with doubly uniparental inheritance of mitochondria. Genome Biol Evol 5:1408–1434

    CrossRef  CAS  Google Scholar 

  • Milani L, Ghiselli F, Maurizii MG, Nuzhdin SV, Passamonti M (2014) Paternally transmitted mitochondria express a new gene of potential viral origin. Gen Biol Evol 6:391–405

    CrossRef  CAS  Google Scholar 

  • Mitchell A, Guerra D, Stewart D, Breton S (2016) In silico analyses of mitochondrial ORFans in freshwater mussels (Bivalvia: Unionoida) provide a framework for future studies of their origin and function. BMC Genom 17:597

    CrossRef  CAS  Google Scholar 

  • Mizi A, Zouros E, Moschonas N, Rodakis GC (2005) The complete maternal and paternal mitochondrial genomes of the Mediterranean mussel Mytilus galloprovincialis: implications for the doubly uniparental inheritance mode of mtDNA. Mol Biol Evol 22:952–967

    Google Scholar 

  • Oliver M, Evans JP (2014) Chemically moderated gamete preferences predict offspring fitness in a broadcast spawning invertebrate. Proc Biol Sci 281:20140148

    Google Scholar 

  • Ouimet P, Kienzle L, Lubosny M, Burzyński A, Angers A, Breton S (2020) The ORF in the control region of the female-transmitted Mytilus mtDNA codes for a protein. Gene 725:144161

    CAS  CrossRef  Google Scholar 

  • Pante E, Poitrimol C, Saunier A, Becquet V, Garcia P (2017) Putative sex-linked heteroplasmy in the tellinid bivalve Limecola balthica (Linnaeus, 1758). J Moll Stud 83:226–228

    Google Scholar 

  • Passamonti M, Ghiselli F (2009) Doubly uniparental inheritance: two mitochondrial genomes, one precious model for organelle DNA inheritance and evolution. DNA Cell Biol 28:79–89

    CAS  CrossRef  Google Scholar 

  • Passamonti M, Ricci A, Milani L, Ghiselli F (2011) Mitochondrial genomes and doubly uniparental inheritance: new insights from Musculista senhousia sex-linked mitochondrial DNAs (Bivalvia Mytilidae). BMC Genom 12:442

    CAS  CrossRef  Google Scholar 

  • Passamonti M, Plazzi F (2020) Doubly Uniparental Inheritance and beyond: the contribution of the Manila clam Ruditapes philippinarum. J Zool Syst Evol Res. https://doi.org/10.1111/jzs.12371

    CrossRef  Google Scholar 

  • Plazzi F, Passamonti M (2019) Footprints of unconventional mitochondrial inheritance in bivalve phylogeny: signatures of positive selection on clades with doubly uniparental inheritance. J Zool Syst Evol Res 57:258–271

    CrossRef  Google Scholar 

  • Plazzi F, Puccio G, Passamonti M (2016) Comparative large-scale mitogenomics evidences clade-specific evolutionary trends in mitochondrial DNAs of bivalvia. Genome Biol Evol 8:2544–2564

    CrossRef  Google Scholar 

  • Plazzi F, Ribani A, Passamonti M (2013) The complete mitochondrial genome of Solemya velum (Mollusca: Bivalvia) and its relationships with Conchifera. BMC Genom 14:409

    CAS  CrossRef  Google Scholar 

  • Pozzi A, Plazzi F, Milani L, Ghiselli F, Passamonti M (2017) SmithRNAs: could mitochondria “bend” nuclear regulation? Mol Biol Evol 34:1960–1973

    CAS  CrossRef  Google Scholar 

  • Régnier C, Fontaine B, Bouchet P (2009) Not knowing, not recording, not listing: numerous unnoticed mollusk extinctions. Cons Biol 23:1214–1221

    CrossRef  Google Scholar 

  • Reis J, Machordom A, Araujo R (2013) Morphological and molecular diversity of Unionidae (Mollusca, Bivalvia) from Portugal. https://doi.org/10.3989/graellsia.2013.v69.075

  • Riccardi N, Froufe E, Bogan AE, Zieritz A, Teixeira A, Vanetti I, Varandas S, Zaccara S, Nagel KO, Lopes-Lima M (2019) Phylogeny of European Anodontini (Bivalvia: Unionidae) with a re-description of Anodonta exulcerata. Zool J Linn Soc. https://doi.org/10.1093/zoolinnean/zlz136

    CrossRef  Google Scholar 

  • Robicheau BM, Breton S, Stewart DT (2017a) Sequence motifs associated with paternal transmission of mitochondrial DNA in the horse mussel, Modiolus modiolus (Bivalvia: Mytilidae). Gene 605:32–42

    CAS  CrossRef  Google Scholar 

  • Robicheau BM, Powell AE, Del Bel L, Breton S, Stewart DT (2017b) Evidence for extreme sequence divergence between the male- and female-transmitted mitochondrial genomes in the bivalve mollusc, Modiolus modiolus (Mytilidae). J Zool Syst Evol Res 55:89–97

    CrossRef  Google Scholar 

  • Robicheau BM, Chase EE, Hoeh WR, Harris JL, Stewart DT, Breton S (2018) Evaluating the utility of the female-specific mitochondrial f-orf gene for population genetic, phylogeographic and systematic studies in freshwater mussels (Bivalvia: Unionida). PeerJ 6:e5007

    CrossRef  CAS  Google Scholar 

  • Sato M, Sato K (2013) Maternal inheritance of mitochondrial DNA by diverse mechanisms to eliminate paternal mitochondrial DNA. Biochim Biophys Acta—Mol Cell Res 1833:1979–1984

    Google Scholar 

  • Shea CP, Peterson JT, Wisniewski JM, Johnson NA (2011) Misidentification of freshwater mussel species (Bivalvia: Unionidae): contributing factors, management implications, and potential solutions. J North Amer Benth Soc 30:446–458

    CrossRef  Google Scholar 

  • Shi J, Hong Y, Sheng J, Peng K, Wang J (2015) De novo transcriptome sequencing to identify the sex-determination genes in Hyriopsis schlegelii. Biosci Biotech Biochem 79:1257–1265

    CAS  CrossRef  Google Scholar 

  • Śmietanka B, Burzyński A, Wenne R (2010) Comparative genomics of marine mussels (Mytilus spp.) gender associated mtDNA: rapidly evolving atp8. J Mol Evol 71:385–400

    CrossRef  CAS  Google Scholar 

  • Śmietanka B, Lubośny M, Przyłucka A, Gérard K, Burzyński A (2018) Mitogenomics of Perumytilus purpuratus (Bivalvia: Mytilidae) and its implications for doubly uniparental inheritance of mitochondria. PeerJ 6:e5593

    CrossRef  CAS  Google Scholar 

  • Smith DR (2006) Survey design for detecting rare freshwater mussels. J North Amer Benth Soc 25:701–711

    CrossRef  Google Scholar 

  • Soroka M, Burzyński A (2017) Hermaphroditic freshwater mussel Anodonta cygnea does not have supranumerary open reading frames in the mitogenome. Mitochondrial DNA Part B 2:862–864

    CrossRef  Google Scholar 

  • Stewart DT, Breton S, Blier PU, Hoeh WR (2009) Masculinization events and doubly uniparental inheritance of mitochondrial DNA: a model for understanding the evolutionary dynamics of gender-associated mtDNA in mussels. Evolutionary Biology. Springer, Berlin, Heidelberg, pp 163–173

    CrossRef  Google Scholar 

  • Stewart DT, Jha M, Breton S, Hoeh WR, Blier PU (2012) No effect of sperm interactions or egg homogenate on sperm velocity in the blue mussel, Mytilus edulis (Bivalvia: Mytilidae). Can J Zool 90:1291–1296

    CrossRef  Google Scholar 

  • Vallès Y, Boore JL (2006) Lophotrochozoan mitochondrial genomes. Integr Comp Biol 46:544–557

    CrossRef  Google Scholar 

  • Zbawicka M, Skibinski D, Wenne R (2003) Doubly uniparental transmission of mitochondrial DNA length variants in the mussel Mytilus trossulus. Mar Biol 142:455–460

    CAS  CrossRef  Google Scholar 

  • Zieritz A, Geist J, Gum B (2014) Spatio-temporal distribution patterns of three stream-dwelling freshwater mussel species: towards a strategy for representative surveys. Hydrobiologia 735:123–136

    CAS  CrossRef  Google Scholar 

  • Zieritz A, Hoffman JI, Amos W, Aldridge DC (2010) Phenotypic plasticity and genetic isolation-by-distance in the freshwater mussel Unio pictorum (Mollusca: Unionoida). Evol Ecol 24:923–938

    CrossRef  Google Scholar 

  • Zouros E, Freeman KR, Ball AO, Pogson GH (1992) Direct evidence for extensive paternal mitochondrial DNA inheritance in the marine mussel Mytilus. Nature 359:412–414

    CAS  CrossRef  Google Scholar 

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

    CrossRef  Google Scholar 

  • Zouros E, Rodakis GC (2019) Doubly uniparental inheritance of mtDNA: an unappreciated defiance of a general rule. Cellular and molecular basis of mitochondrial inheritance. Springer, Cham, pp 25–49

    CrossRef  Google Scholar 

  • Zouros E (2020) Doubly uniparental inheritance of mitochondrial DNA: Might it be simpler than we thought? J Zool Syst Evol Res. https://doi.org/10.1111/jzs.12364

    CrossRef  Google Scholar 

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Acknowledgements

DTS and SB were funded by NSERC Discovery grants. EEC was funded by the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No713750, carried out with the financial support of the Regional Council of Provence- Alpes-Côte d’Azur and with the financial support of the A*MIDEX (n° ANR- 11-IDEX-0001-02), funded by the Investissements d’Avenir project funded by the French Government, managed by the French National Research Agency [ANR]). At time of submission, an NSERC CGS-D supported BMR. MAGR was supported by a Harrison McCain Visiting Professorship Award from the Harrison McCain Foundation.

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Stewart, D.T. et al. (2020). An Unusual Evolutionary Strategy: The Origins, Genetic Repertoire, and Implications of Doubly Uniparental Inheritance of Mitochondrial DNA in Bivalves. In: Pontarotti, P. (eds) Evolutionary Biology—A Transdisciplinary Approach. Springer, Cham. https://doi.org/10.1007/978-3-030-57246-4_12

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