Abstract
Bivalved mollusks have an unusual system of mitochondrial DNA transmission referred to as “Doubly Uniparental Inheritance” or DUI. Species with DUI are characterized by the presence of two gender-associated mitochondrial DNA lineages that are inherited through males (male-transmitted or M types) or females (female-transmitted or F types), respectively. In marine mussels (Mytiloida), an M type and an F type occasionally recombine. Complete mtDNA genome sequencing studies have demonstrated that new, recombinant M types are occasionally produced that are primarily composed of an F type protein coding genes, rRNA genes, tRNA genes, F type control region and, significantly, an M type control region. We have studied various properties of one of these novel recombinant M types (i.e., a “recently masculinized male-transmitted genome or RM type”) and compared its performance with an evolutionary older “standard” M type (i.e., an SM type) and found evidence for faster swimming speed and more efficient mitochondrially-encoded enzyme activity of the RM type. These studies lead us to a model to explain the evolutionary dynamics and phylogenetic relationships of the various male and female-transmitted mtDNA genomes found in marine mussels (Mytiloida).
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
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
Breton S, Doucet Beaupré H, Stewart DT, Hoeh WR, Blier PU (2007) The unusual system of doubly uniparental inheritance of mtDNA: Isn't one enough? TIG 23:464–475
Breton S, Stewart DT, Blier PU (2009) Role-reversal of gender-associated mitochondrial DNA affects mitochondrial function in Mytilus edulis (Bivalvia: Mytilidae). J Exp Zool B (Mol Dev Evol) 312B:108–117
Burt A, Trivers RL (2006) Genes in conflict. Belknap Press of Harvard University Press, Boston, MA
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
Burzyński A, Zbawicka M, Skibinski DOF, Wenne R (2006) Doubly uniparental inheritance is associated with high polymorphism for rearranged and recombinant control region haplotypes in Baltic Mytilus trossulus. Genetics 174:1081–1094
Cao LQ, Kenchington E, Zouros E, Rodakis GC (2004) 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
Chakrabarti R, Walker JM, Chapman EG, Shepardson SP, Trdan RJ, Curole JP, Watters GT, Stewart DT, Vijayaraghavan 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
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
Dalziel AC, Stewart DT (2002) Tissue-specific expression of male-transmitted mitochondrial DNA and its implications for rates of molecular evolution in Mytilus mussels (Bivalvia: Mytilidae). Genome 45:348–355
Dalziel AC, Moore SE, Moyes CD (2005) Mitochondrial enzyme content in the muscles of high performance fish: Evolution and variation among fiber types. Am J Physiol Regul Integr Comp Physiol 288:R163–R172
Everett EM, Williams P, Gibson G, Stewart DT (2004) Mitochondrial DNA polymorphisms and sperm motility in Mytilus edulis (Bivalvia: Mytilidae). J Exp A (Comp Exp Biol) 301A:906–910
Garrido-Ramos MA, Stewart DT, Sutherland BW, Zouros E (1998) The distribution of male-transmitted and female-transmitted mitochondrial DNA types in somatic tissues of blue mussels: Implications for the operation of doubly uniparental inheritance of mitochondrial DNA. Genome 41:818–824
Hoeh WR, Stewart DT, Sutherland BW, Zouros E (1996) Multiple origins of gender-associated mitochondrial DNA lineages in bivalves (Mollusca: Bivalvia). Evolution 50:2276–2286
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
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
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
Knock E, Petersen SD, Stewart DT (2005) Differential display reverse transcription PCR applied to male Mytilus edulis mussels with two distinct mitochondrial DNA types. Biochem Syst Ecol 33:715–724
Levitan DR. (2000) Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegatus. Proc R Soc Lond B Biol Sci 267:531–534.
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
Obata M, Kamiya K, Kawamura K, Komaru A (2006) Sperm mitochondrial DNA transmission to both male and female offspring in the blue mussel Mytilus galloprovincialis. Dev Growth Differ 48:253–261
Passamonti M, Scali V (2001) Gender-associated mitochondrial DNA heteroplasmy in the venerid clam Tapes philippinarum (Mollusca Bivalvia). Curr Genetics 39:117–124
Passamonti M (2007) An unusual case of gender-associated mitochondrial DNA heteroplasmy: the mytilid Musculista senhousia (Mollusca Bivalvia). BMC Evol Biol 7(Suppl 2):S7 doi:10.1186/1471-2148-7-S2-S7
Quesada H, Stuckas H, Skibinski DOF (2003) Heteroplasmy suggests paternal co-transmission of multiple genomes and pervasive reversion of maternally into paternally transmitted genomes of mussel (Mytilus) mitochondrial DNA. J Mol Evol 57:S138–S147
Rawson PD (2005) Nonhomologous recombination between the large unassigned region of the male and female mitochondrial genomes in the mussel, Mytilus trossulus. J Mol Evol 61:717–732
Sano N, Obata M, 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. Dev Growth Diff 49:67–72
Stewart DT, Kenchington E, Singh R, Zouros E (1996) Degree of selective constraint as an explanation of the different rates of evolution of gender-specific mitochondrial DNA lineages in the mussel Mytilus. Genetics 143:1349–1357
Theologidis I, Saavedra C, Zouros E (2007) No evidence for absence of paternal mtDNA in male progeny from pair matings of the mussel Mytilus galloprovincialis. Genetics 176:1367–1369
Venetis C, Theologidis I, Zouros E, Rodakis GC (2006) No evidence for presence of maternal mitochondrial DNA in the sperm of Mytilus galloprovincialis males. Proc R Soc Lond B Biol Sci 273:2483–2489
Walker JM, Bogan AE, Garo K, Soliman GN, Hoeh WR (2006) Hermaphroditism in the Iridinidae (Bivalvia: Etherioidea). J Molluscan Stud 72: 216–217
Zeh JA, Zeh DW (2005) Maternal inheritance, sexual conflict and the maladapted male. TIG 21:281–286
Acknowledgments
This work was funded by Discovery grants from the Natural Sciences and Engineering Research Council of Canada (NSERC) to D. Stewart and P. Blier and by a National Science Foundation grant to W.R. Hoeh. S. Breton was funded by an NSERC postgraduate scholarship and is currently funded by an NSERC postdoctoral fellowship. We acknowledge members of the Blier and Stewart labs for assistance with various aspects of this study.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2009 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Stewart, D.T., Breton, S., Blier, P.U., Hoeh, W.R. (2009). Masculinization Events and Doubly Uniparental Inheritance of Mitochondrial DNA: A Model for Understanding the Evolutionary Dynamics of Gender-Associated mtDNA in Mussels. In: Pontarotti, P. (eds) Evolutionary Biology. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-00952-5_9
Download citation
DOI: https://doi.org/10.1007/978-3-642-00952-5_9
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-00951-8
Online ISBN: 978-3-642-00952-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)