Artigo Revisado por pares

Sex-biased mitochondrial DNA heteroplasmy in the marine mussel Mytilus

1990; Royal Society; Volume: 242; Issue: 1305 Linguagem: Inglês

10.1098/rspb.1990.0118

ISSN

1471-2954

Autores

Cynthia L. Fisher, D. O. F. Skibinski,

Tópico(s)

Marine Bivalve and Aquaculture Studies

Resumo

Restricted accessMoreSectionsView PDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmail Cite this article Fisher C. and Skibinski David O. F. 1990Sex-biased mitochondrial DNA heteroplasmy in the marine mussel MytilusProc. R. Soc. Lond. B.242149–156http://doi.org/10.1098/rspb.1990.0118SectionRestricted accessArticleSex-biased mitochondrial DNA heteroplasmy in the marine mussel Mytilus C. Fisher Google Scholar Find this author on PubMed Search for more papers by this author and David O. F. Skibinski Google Scholar Find this author on PubMed Search for more papers by this author C. Fisher Google Scholar Find this author on PubMed and David O. F. Skibinski Google Scholar Find this author on PubMed Published:22 December 1990https://doi.org/10.1098/rspb.1990.0118AbstractIndividuals heteroplasmic for mitochondrial DNA were observed in seven Mytilus populations at frequencies varying between 7 and 38%. The majority of heteroplasmic individuals possessed two genomes, referred to as the F and M genomes, which appear to exhibit base sequence divergence estimated to be about 10%. All homoplasmic individuals examined possessed the F genome. A large sex difference in the incidence of heteroplasmy was observed with 37% of males but only 5% of females possessing the M genome. Analysis of mtDNA extracted from different tissues provided evidence that the F genome predominates in female gonads and the M genome predominates in male gonads. Biparental transmission of mtDNA is considered as an explanation of these results but is not supported by a statistical analysis of the association of genotypes within heteroplasmic individuals. Because the F genome predominates in the gonads of most females, it is suggested that the M genome must have a replicative advantage to be detected in large quantity within individuals.FootnotesThis text was harvested from a scanned image of the original document using optical character recognition (OCR) software. As such, it may contain errors. Please contact the Royal Society if you find an error you would like to see corrected. Mathematical notations produced through Infty OCR. Previous ArticleNext Article VIEW FULL TEXT DOWNLOAD PDF FiguresRelatedReferencesDetailsCited by Soroka M, Wasowicz B and Zając K (2021) Conservation status and a novel restoration of the endangered freshwater mussel Unio crassus Philipsson, 1788: Poland case , Knowledge & Management of Aquatic Ecosystems, 10.1051/kmae/2021003:422, (3), . Stewart D, Breton S, Chase E, Robicheau B, Bettinazzi S, Pante E, Youssef N and Garrido-Ramos M (2020) An Unusual Evolutionary Strategy: The Origins, Genetic Repertoire, and Implications of Doubly Uniparental Inheritance of Mitochondrial DNA in Bivalves Evolutionary Biology—A Transdisciplinary Approach, 10.1007/978-3-030-57246-4_12, (301-323), . Soroka M (2020) Doubly uniparental inheritance of mitochondrial DNA in freshwater mussels: History and status of the European species, Journal of Zoological Systematics and Evolutionary Research, 10.1111/jzs.12381, 58:2, (598-614), Online publication date: 1-May-2020. Wang G, Wu C, Ge J, Chen Y, Han Z, Guo P and Li J (2019) Identification of complete F-type mitochondrial genome in Lamprotula scripta and Lamprotula caveata and analysis on DUI, Gene, 10.1016/j.gene.2019.04.075, 710, (59-65), Online publication date: 1-Aug-2019. Zouros E and Rodakis G (2019) Doubly Uniparental Inheritance of mtDNA: An Unappreciated Defiance of a General Rule Cellular and Molecular Basis of Mitochondrial Inheritance, 10.1007/102_2018_4, (25-49), . Lim J, Tay T, Lim C, Lee S, Teo S and Tan K (2018) Mytella strigata (Bivalvia: Mytilidae): an alien mussel recently introduced to Singapore and spreading rapidly , Molluscan Research, 10.1080/13235818.2018.1423858, 38:3, (170-186), Online publication date: 3-Jul-2018. Soroka M and Burzyński A (2017) Doubly uniparental inheritance and highly divergent mitochondrial genomes of the freshwater mussel Unio tumidus (Bivalvia: Unionidae), Hydrobiologia, 10.1007/s10750-017-3113-7, 810:1, (239-254), Online publication date: 1-Mar-2018. Robicheau B, Powell A, Del Bel L, Breton S and Stewart D (2016) Evidence for extreme sequence divergence between the male- and female-transmitted mitochondrial genomes in the bivalve mollusc, Modiolus modiolus (Mytilidae) , Journal of Zoological Systematics and Evolutionary Research, 10.1111/jzs.12160, 55:2, (89-97), Online publication date: 1-May-2017. Williams E, Feng X and Place A (2017) Extensive Heteroplasmy and Evidence for Fragmentation in the Callinectes sapidus Mitochondrial Genome , Journal of Shellfish Research, 10.2983/035.036.0129, 36:1, (263-272), Online publication date: 1-Apr-2017. Whelan N and Strong E (2015) Morphology, molecules and taxonomy: extreme incongruence in pleurocerids ( G astropoda, C erithioidea, P leuroceridae) , Zoologica Scripta, 10.1111/zsc.12139, 45:1, (62-87), Online publication date: 1-Jan-2016. Trovant B, Basso N, Orensanz J, Lessa E, Dincao F and Ruzzante D (2016) Scorched mussels ( Brachidontes spp., Bivalvia: Mytilidae) from the tropical and warm‐temperate southwestern Atlantic: the role of the Amazon River in their speciation , Ecology and Evolution, 10.1002/ece3.2016, 6:6, (1778-1798), Online publication date: 1-Mar-2016. Vargas J, Pérez M, Toro J and Astorga M (2015) Presence of two mitochondrial genomes in the mytilid Perumytilus purpuratus: Phylogenetic evidence for doubly uniparental inheritance, Genetics and Molecular Biology, 10.1590/S1415-47573822201420140262, 38:2, (173-181), Online publication date: 1-Jun-2015. Comtet T, Sandionigi A, Viard F and Casiraghi M (2015) DNA (meta)barcoding of biological invasions: a powerful tool to elucidate invasion processes and help managing aliens, Biological Invasions, 10.1007/s10530-015-0854-y, 17:3, (905-922), Online publication date: 1-Mar-2015. Fernández-Álvarez F, García-Jiménez R and Machordom A (2015) Carinina ochracea (Palaeonemertea: Tubulanidae) Reaches Its Southernmost Distribution: New Morphological and Molecular Data , Zoological Science, 10.2108/zs140228, 32:6, (590-595), Online publication date: 1-Dec-2015. Brannock P, Roberts M and Hilbish T (2013) Ubiquitous heteroplasmy in Mytilus spp. resulting from disruption in doubly uniparental inheritance regulation, Marine Ecology Progress Series, 10.3354/meps10228, 480, (131-143), Online publication date: 22-Apr-2013. Boyle E and Etter R (2012) Heteroplasmy in a deep-sea protobranch bivalve suggests an ancient origin of doubly uniparental inheritance of mitochondria in Bivalvia, Marine Biology, 10.1007/s00227-012-2099-y, 160:2, (413-422), Online publication date: 1-Feb-2013. Krebs R, Borden W, Evans N and Doerder F (2013) Differences in population structure estimated within maternally- and paternally-inherited forms of mitochondria in Lampsilis siliquoidea (Bivalvia: Unionidae) , Biological Journal of the Linnean Society, 10.1111/bij.12025, 109:1, (229-240), Online publication date: 1-May-2013. Zouros E (2012) Biparental Inheritance Through Uniparental Transmission: The Doubly Uniparental Inheritance (DUI) of Mitochondrial DNA, Evolutionary Biology, 10.1007/s11692-012-9195-2, 40:1, (1-31), Online publication date: 1-Mar-2013. John J and John B (2013) Sperm Mitochondrial DNA Sperm Chromatin for the Researcher, 10.1007/978-1-4614-8459-2_5, (71-88), . Yusa Y, Breton S and Hoeh W (2013) Population Genetics of Sex Determination in Mytilus Mussels: Reanalyses and a Model, Journal of Heredity, 10.1093/jhered/est014, 104:3, (380-385), Online publication date: 1-May-2013. John J and John B (2011) Sperm Mitochondrial DNA Sperm Chromatin, 10.1007/978-1-4419-6857-9_6, (81-94), . Batista F, Lallias D, Taris N, Guedes-Pinto H and Beaumont A (2010) Relative quantification of the M and F mitochondrial DNA types in the blue mussel Mytilus edulis by real-time PCR, Journal of Molluscan Studies, 10.1093/mollus/eyq031, 77:1, (24-29), Online publication date: 1-Feb-2011., Online publication date: 1-Feb-2011. Sano N, Obata M and Komaru A (2010) Mitochondrial DNA Transmitted from Sperm in the Blue Mussel Mytilus galloprovincialis Showing Doubly Uniparental Inheritance of Mitochondria, Quantified by Real-Time PCR , Zoological Science, 10.2108/zsj.27.611, 27:7, (611-614), Online publication date: 1-Jul-2010. Soroka M (2011) Characteristics of mitochondrial DNA of unionid bivalves (Mollusca: Bivalvia: Unionidae). I. Detection and characteristics of doubly uniparental inheritance (DUI) of unionid mitochondrial DNA, Folia Malacologica, 10.2478/v10125-010-0015-y, 18:4, (147-188), Online publication date: 1-Dec-2010. Gillis N, Walters L, Fernandes F and Hoffman E (2009) Higher genetic diversity in introduced than in native populations of the mussel Mytella charruana : evidence of population admixture at introduction sites , Diversity and Distributions, 10.1111/j.1472-4642.2009.00591.x, 15:5, (784-795), Online publication date: 1-Sep-2009. Filipowicz M, Burzyński A, Śmietanka B and Wenne R (2008) Recombination in Mitochondrial DNA of European Mussels Mytilus, Journal of Molecular Evolution, 10.1007/s00239-008-9157-6, 67:4, (377-388), Online publication date: 1-Oct-2008. Hedtke S, Stanger-Hall K, Baker R and Hillis D (2008) ALL-MALE ASEXUALITY: ORIGIN AND MAINTENANCE OF ANDROGENESIS IN THE ASIAN CLAM CORBICULA, Evolution, 10.1111/j.1558-5646.2008.00344.x, 62:5, (1119-1136), Online publication date: 1-May-2008. Sano N, Obata M and Komaru A (2007) Quantitation of the male and female types of mitochondrial DNA in a blue mussel, Mytilus galloprovincialis, using real-time polymerase chain reaction assay, Development, Growth & Differentiation, 10.1111/j.1440-169X.2007.00904.x, 49:1, (67-72) Ort B and Pogson G (2007) Molecular Population Genetics of the Male and Female Mitochondrial DNA Molecules of the California Sea Mussel, Mytilus californianus , Genetics, 10.1534/genetics.107.072934, 177:2, (1087-1099), Online publication date: 1-Oct-2007. Breton S, Beaupré H, Stewart D, Hoeh W and Blier P (2007) The unusual system of doubly uniparental inheritance of mtDNA: isn't one enough?, Trends in Genetics, 10.1016/j.tig.2007.05.011, 23:9, (465-474), Online publication date: 1-Sep-2007. Obata M, Sano N, Kawamura K and Komaru A (2007) Inheritance of two M type mitochondrial DNA from sperm and unfertilized eggs to offspring in Mytilus galloprovincialis, Development, Growth & Differentiation, 10.1111/j.1440-169X.2007.00930.x, 49:4, (335-344) Obata M, Kamiya C, Kawamura K and Komaru A (2006) Sperm mitochondrial DNA transmission to both male and female offspring in the blue mussel Mytilus galloprovincialis, Development, Growth and Differentiation, 10.1111/j.1440-169X.2006.00863.x, 48:4, (253-261), Online publication date: 1-May-2006. Carney S, Formica M, Divatia H, Nelson K, Fisher C and Schaeffer S (2006) Population structure of the mussel "Bathymodiolus" childressi from Gulf of Mexico hydrocarbon seeps, Deep Sea Research Part I: Oceanographic Research Papers, 10.1016/j.dsr.2006.03.002, 53:6, (1061-1072), Online publication date: 1-Jun-2006. Chakrabarti R, Walker J, Stewart D, Trdan R, Vijayaraghavan S, Curole J and Hoeh W (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 Letters, 10.1016/j.febslet.2005.12.104, 580:3, (862-866), Online publication date: 6-Feb-2006. Burzyński A, Zbawicka M, Skibinski D and Wenne R (2006) Doubly Uniparental Inheritance Is Associated With High Polymorphism for Rearranged and Recombinant Control Region Haplotypes in Baltic Mytilus trossulus , Genetics, 10.1534/genetics.106.063180, 174:3, (1081-1094), Online publication date: 1-Nov-2006. Soroka M (2005) Genetic Variability Among Freshwater Mussel Anodonta woodiana (Lea, 1834) (Bivalvia: Unionidae) Populations Recently Introduced in Poland, Zoological Science, 10.2108/zsj.22.1137, 22:10, (1137-1144), Online publication date: 1-Oct-2005. Curole J and Kocher T (2005) Evolution of a Unique Mitotype-Specific Protein-Coding Extension of the Cytochrome c Oxidase II Gene in Freshwater Mussels (Bivalvia: Unionoida), Journal of Molecular Evolution, 10.1007/s00239-004-0192-7, 61:3, (381-389), Online publication date: 1-Sep-2005. Endo K, Noguchi Y, Ueshima R and Jacobs H (2005) Novel Repetitive Structures, Deviant Protein-Encoding Sequences andUnidentified ORFs in the Mitochondrial Genome of the BrachiopodLingula anatina, Journal of Molecular Evolution, 10.1007/s00239-004-0214-5, 61:1, (36-53), Online publication date: 1-Jul-2005. JOHN J, JOKHI R and BARRATT C (2005) The impact of mitochondrial genetics on male infertility, International Journal of Andrology, 10.1111/j.1365-2605.2005.00515.x, 28:2, (65-73), Online publication date: 1-Apr-2005. Kallersjo M, von Proschwitz T, Lundberg S, Eldenas P and Erseus C (2005) Evaluation of ITS rDNA as a complement to mitochondrial gene sequences for phylogenetic studies in freshwater mussels: an example using Unionidae from north-western Europe, Zoologica Scripta, 10.1111/j.1463-6409.2005.00202.x, 34:4, (415-424), Online publication date: 1-Jul-2005. St John J, Lloyd R and El Shourbagy S (2004) The potential risks of abnormal transmission of mtDNA through assisted reproductive technologies, Reproductive BioMedicine Online, 10.1016/S1472-6483(10)60496-8, 8:1, (34-44), Online publication date: 1-Jan-2004. St. John J and Schatten G (2004) Paternal Mitochondrial DNA Transmission During Nonhuman Primate Nuclear Transfer, Genetics, 10.1534/genetics.103.025049, 167:2, (897-905), Online publication date: 1-Jun-2004. Cao L, Kenchington E and Zouros E (2004) Differential Segregation Patterns of Sperm Mitochondria in Embryos of the Blue Mussel ( Mytilus edulis ) , Genetics, 10.1093/genetics/166.2.883, 166:2, (883-894), Online publication date: 1-Feb-2004. St John J, Lloyd R, Bowles E, Thomas E and El Shourbagy S The consequences of nuclear transfer for mammalian foetal development and offspring survival. A mitochondrial DNA perspective, Reproduction, 10.1530/rep.1.00138, 127:6, (631-641) LEE T and Ó FOIGHIL D (2004) Hidden Floridian biodiversity: mitochondrial and nuclear gene trees reveal four cryptic species within the scorched mussel, Brachidontes exustus, species complex, Molecular Ecology, 10.1111/j.1365-294X.2004.02337.x, 13:11, (3527-3542) Cao L, Kenchington E and Zouros E (2004) Differential Segregation Patterns of Sperm Mitochondria in Embryos of the Blue Mussel ( Mytilus edulis ) , Genetics, 10.1534/genetics.166.2.883, 166:2, (883-894), Online publication date: 1-Feb-2004. Venier P, Pallavicini A, De Nardi B and Lanfranchi G (2003) Towards a catalogue of genes transcribed in multiple tissues of Mytilus galloprovincialis, Gene, 10.1016/S0378-1119(03)00708-X, 314, (29-40), Online publication date: 1-Sep-2003. St. John J (2002) The transmission of mitochondrial DNA following assisted reproductive techniques, Theriogenology, 10.1016/S0093-691X(01)00661-6, 57:1, (109-123), Online publication date: 1-Jan-2002. Ladoukakis E, Saavedra C, Magoulas A and Zouros E (2002) Mitochondrial DNA variation in a species with two mitochondrial genomes: the case of Mytilus galloprovincialis from the Atlantic, the Mediterranean and the Black Sea, Molecular Ecology, 10.1046/j.1365-294X.2002.01473.x, 11:4, (755-769), Online publication date: 1-Apr-2002. Dalziel A and Stewart D (2002) Tissue-specific expression of male-transmitted mitochondrial DNA and its implications for rates of molecular evolution in Mytilus mussels (Bivalvia: Mytilidae) , Genome, 10.1139/g01-159, 45:2, (348-355), Online publication date: 1-Apr-2002. Porter J, Skibinski D, Leamon J and Hayward P (2005) Technique for analysis of bryozoan mitochondrial DNA, Molecular Ecology Notes, 10.1046/j.1471-8278.2000.00018.x, 1:1-2, (103-105), Online publication date: 1-Mar-2001. Apte S and Gardner J (2008) Three polymorphic mitochondrial DNA markers for Perna canaliculus , Animal Genetics, 10.1046/j.1365-2052.2001.0647g.x, 32:1, (47-49), Online publication date: 1-Feb-2001. Ridgway G, Dahle G and Høisœter T (2011) Population genetics of Pecten maximus of the Northeast Atlantic coast , Sarsia, 10.1080/00364827.2000.10414566, 85:2, (167-172), Online publication date: 9-Jun-2000. Silva E and Russo C (2000) Techniques and statistical data analysis in molecular population genetics Marine Genetics, 10.1007/978-94-017-2184-4_13, (119-135), . Noguchi Y, Endo K, Tajima F and Ueshima R (2000) The Mitochondrial Genome of the Brachiopod Laqueus rubellus , Genetics, 10.1093/genetics/155.1.245, 155:1, (245-259), Online publication date: 1-May-2000. Zouros E (2000) The exceptional mitochondrial DNA system of the mussel family Mytilidae, Genes & Genetic Systems, 10.1266/ggs.75.313, 75:6, (313-318), . SKIBINSKI D, GALLAGHER C and QUESADA H (2008) On the roles of selection, mutation and drift in the evolution of mitochondrial DNA diversity in British Mytilus edulis (Mytilidae; Mollusca) populations, Biological Journal of the Linnean Society, 10.1111/j.1095-8312.1999.tb01166.x, 68:1-2, (195-213), Online publication date: 1-Sep-1999. Sutherland B, Stewart D, Kenchington E and Zouros E (1998) The Fate of Paternal Mitochondrial DNA in Developing Female Mussels, Mytilus edulis: Implications for the Mechanism of Doubly Uniparental Inheritance of Mitochondrial DNA, Genetics, 10.1093/genetics/148.1.341, 148:1, (341-347), Online publication date: 1-Jan-1998. Chesser R (1998) Heteroplasmy and Organelle Gene Dynamics, Genetics, 10.1093/genetics/150.3.1309, 150:3, (1309-1327), Online publication date: 1-Nov-1998. Quesada H, Warren M and Skibinski D (1998) Nonneutral Evolution and Differential Mutation Rate of Gender-Associated Mitochondrial DNA Lineages in the Marine Mussel Mytilus, Genetics, 10.1093/genetics/149.3.1511, 149:3, (1511-1526), Online publication date: 1-Jul-1998. QUESADA H, GALLAGHER C, SKIBINSKI D and SKIBINSKI D (1998) Patterns of polymorphism and gene flow of gender-associated mitochondrial DNA lineages in European mussel populations, Molecular Ecology, 10.1046/j.1365-294x.1998.00428.x, 7:8, (1041-1051), Online publication date: 1-Aug-1998. Stothard J and Rollinson D (1997) Partial DNA sequences from the mitochondrial cytochrome oxidase subunit I (COI) gene can differentiate the intermediate snail hosts Bulinus globosus and B. nasutus (Gastropoda: Planorbidae) , Journal of Natural History, 10.1080/00222939700770361, 31:5, (727-737), Online publication date: 1-May-1997. Rigaa A, Cellos D and Monnerot M (1997) Mitochondrial DNA from the scallop Pecten maximus: an unusual polymorphism detected by restriction fragment length polymorphism analysis, Heredity, 10.1038/hdy.1997.171, 79:4, (380-387), Online publication date: 1-Oct-1997. Wilding C, Beaumont A and Latchford J (1997) Mitochondrial DNA variation in the scallop Pecten maximus (L.) assessed by a PCR-RFLP method, Heredity, 10.1038/hdy.1997.141, 79:2, (178-189), Online publication date: 1-Aug-1997. Liu H, Mitton J and Wu S (2017) PATERNAL MITOCHONDRIAL DNA DIFFERENTIATION FAR EXCEEDS MATERNAL MITOCHONDRIAL DNA AND ALLOZYME DIFFERENTIATION IN THE FRESHWATER MUSSEL, ANODONTA GRANDIS GRANDIS , Evolution, 10.1111/j.1558-5646.1996.tb03907.x, 50:2, (952-957), Online publication date: 1-Apr-1996. Hoeh W, Stewart D, Sutherland B and Zouros E (2017) MULTIPLE ORIGINS OF GENDER-ASSOCIATED MITOCHONDRIAL DNA LINEAGES IN BIVALVES (MOLLUSCA: BIVALVIA), Evolution, 10.1111/j.1558-5646.1996.tb03616.x, 50:6, (2276-2286), Online publication date: 1-Dec-1996. Quesada H, Skibinski D and Skibinski D (1996) Sex-biased heteroplasmy and mitochondrial DNA inheritance in the musselMytilus galloprovincialis Lmk., Current Genetics, 10.1007/BF02221509, 29:5, (423-426), Online publication date: 1-Apr-1996. Rawson P and Hilbish T (1995) Distribution of male and female mtDNA lineages in populations of blue mussels, Mytilus trossulus and M. galloprovincialis, along the Pacific coast of North America, Marine Biology, 10.1007/BF00347128, 124:2, (245-250), Online publication date: 1-Dec-1995. Craddock C, Hoeh W, Lutz R and Vrijenhoek R (1995) Extensive gene flow among mytilid (Bathymodiolus thermophilus) populations from hydrothermal vents of the eastern Pacific, Marine Biology, 10.1007/BF00349155, 124:1, (137-146), Online publication date: 1-Nov-1995. Wenne R and Skibinski D (1995) Mitochondrial DNA heteroplasmy in European populations of the mussel Mytilus trossulus, Marine Biology, 10.1007/BF00350683, 122:4, (619-624), Online publication date: 1-Jun-1995. Kenchington E, Landry D and Bird C (1995) Comparison of taxa of the mussel Mytilus (Bivalvia) by analysis of the nuclear small-subunit rRNA gene sequence , Canadian Journal of Fisheries and Aquatic Sciences, 10.1139/f95-850, 52:12, (2613-2620), Online publication date: 1-Dec-1995. Hurst L (1997) Cytoplasmic genetics under inbreeding and outbreeding, Proceedings of the Royal Society of London. Series B: Biological Sciences, 258:1353, (287-298), Online publication date: 22-Dec-1994. Hurst L and Hoekstra R (1994) Shellfish genes kept in line, Nature, 10.1038/368811a0, 368:6474, (811-812), Online publication date: 1-Apr-1994. Geller J, Carlton J and Powers D (1994) PCR-based detection of mtDNA haplotypes of native and invading mussels on the northeastern Pacific coast: latitudinal pattern of invasion, Marine Biology, 10.1007/BF00349563, 119:2, (243-249), Online publication date: 1-May-1994. Zouros E, Ball A, Saavedra C and Freeman K (1994) Mitochondrial DNA inheritance, Nature, 10.1038/368818a0, 368:6474, (818-818), Online publication date: 1-Apr-1994. Hilbish T, Bayne B and Day A (2017) GENETICS OF PHYSIOLOGICAL DIFFERENTIATION WITHIN THE MARINE MUSSEL GENUS MYTILUS , Evolution, 10.1111/j.1558-5646.1994.tb01311.x, 48:2, (267-286), Online publication date: 1-Apr-1994. Skibinski D, Gallagher C and Beynon C (1994) Mitochondrial DNA inheritance, Nature, 10.1038/368817b0, 368:6474, (817-818), Online publication date: 1-Apr-1994. Gardner J (1992) Mytilus Galloprovincialis (Lmk) (Bivalvia, Mollusca): The Taxonomic Status of the Mediterranean Mussel , Ophelia, 10.1080/00785326.1992.10429929, 35:3, (219-243), Online publication date: 1-Jul-1992. Zouros E, Freeman K, Ball A and Pogson G (1992) Direct evidence for extensive paternal mitochondrial DNA inheritance in the marine mussel Mytilus, Nature, 10.1038/359412a0, 359:6394, (412-414), Online publication date: 1-Oct-1992. Karakousis Y and Skibinski D (1992) An analysis of allozyme, mitochondrial DNA and morphological variation in mussel (Mytilus galloprovincialis) populations from Greece, Experientia, 10.1007/BF02118424, 48:9, (878-881), Online publication date: 1-Sep-1992. Hastings I (2009) Population genetic aspects of deleterious cytoplasmic genomes and their effect on the evolution of sexual reproduction, Genetical Research, 10.1017/S0016672300030500, 59:3, (215-225), Online publication date: 1-Jun-1992. McDonald J, Seed R and Koehn R (1991) Allozymes and morphometric characters of three species ofMytilus in the Northern and Southern Hemispheres, Marine Biology, 10.1007/BF01319403, 111:3, (323-333), Online publication date: 1-Oct-1991. Rodríguez-Pena E, Verísimo P, Fernández L, González-Tizón A, Bárcena C, Martínez-Lage A and Qiu G (2020) High incidence of heteroplasmy in the mtDNA of a natural population of the spider crab Maja brachydactyla, PLOS ONE, 10.1371/journal.pone.0230243, 15:3, (e0230243) Stewart D, Robicheau B, Youssef N, Garrido-Ramos M, Chase E and Breton S (2021) Expanding the Search for Sperm Transmission Elements in the Mitochondrial Genomes of Bivalve Mollusks, Genes, 10.3390/genes12081211, 12:8, (1211) Boschen R, Rowden A, Clark M and Gardner J (2015) Limitations in the Use of Archived Vent Mussel Samples to Assess Genetic Connectivity Among Seafloor Massive Sulfide Deposits: A Case Study with Implications for Environmental Management, Frontiers in Marine Science, 10.3389/fmars.2015.00105, 2 Kenchington E, Hamilton L, Cogswell A, Zouros E and Vollmer S (2009) Paternal mtDNA and Maleness Are Co-Inherited but Not Causally Linked in Mytilid Mussels, PLoS ONE, 10.1371/journal.pone.0006976, 4:9, (e6976) This Issue22 December 1990Volume 242Issue 1305 Article InformationDOI:https://doi.org/10.1098/rspb.1990.0118Published by:Royal SocietyPrint ISSN:0962-8452Online ISSN:1471-2954History: Manuscript received08/05/1990Manuscript accepted10/09/1990Published online01/01/1997Published in print22/12/1990 License:Scanned images copyright © 2017, Royal Society Citations and impact Large datasets are available through Proceedings B's partnership with Dryad

Referência(s)