Doubly Uniparental Inheritance Is Associated With High Polymorphism for Rearranged and Recombinant Control Region Haplotypes in BalticMytilus trossulus

Abstract

Many bivalve species, including mussels of the genus Mytilus, are unusual in having two mtDNA genomes, one inherited maternally (the F genome) and the other inherited paternally (the M genome). The sequence differences between the genomes are usually great, indicating ancient divergence predating speciation events. However, in Mytilus trossulus from the Baltic, both genomes are similar to the F genome from the closely related M. edulis. This study analyzed the mtDNA control region structure in male and female Baltic M. trossulus mussels. We show that a great diversity of structural rearrangements is present in both sexes. Sperm samples are dominated by recombinant haplotypes with M. edulis M-like control region segments, some having large duplications. By contrast, the rearranged haplotypes that dominate in eggs lack segments from this M genome. The rearrangements can be explained by a combination of tandem duplication, deletion, and intermolecular recombination. An evolutionary pathway leading to the recombinant haplotypes is suggested. The data are also considered in relation to the hypothesis that the M. edulis M-like control region sequence is necessary to confer the paternal role on genomes that are otherwise F-like. S TRICTLY uniparental inheritance of organelle genomes is a rule in nearly all anisogamic organisms. One of the most prominent exceptions is the mitochondrial inheritance system of mussels of the family Mytilidae in which separate maternal (the F genome) and paternal (the M genome) routes of mtDNA inheritance occur (for review, see Skibinski et al.1994a,b; Zouros et al. 1994a,b;Zouros 2000). This system, called doubly uniparental inheritance (DUI) (Zouros et al. 1994a), has also been observed in freshwater mussels of the family Unionidae (Hoeh et al. 1996;Liu et al. 1996) and clams of the family Veneridae (Passamonti and Scali 2001). Phylogenetic analysis indicates that divergence of the F and M genomes can be great, predating speciation events, and that role reversal or masculinization events, whereby the F genome takes on the role of the previous M genome, has occurred repeatedly in the evolution of marine mussels (Hoeh et al. 1996(Hoeh et al. , 1997, but is absent or less frequent in freshwater mussels (Hoeh et al. 2002).A hybrid zone separates Baltic Mytilus trossulus from North Sea M. edulis populations (see Riginos and Cunningham 2005 for review). Although there is little introgression of mtDNA between American M. trossulus and M. edulis (Saavedra et al. 1996;Comesana et al. 1999) in Baltic M. trossulus, the mtDNA in heteroplasmic male individuals is similar to that in the F genome from M. edulis (Quesada et al. 1995(Quesada et al. , 2003Wenne and Skibinski 1995; Zbawicka et al. 2003a,b). It appears that there has been complete asymmetric introgression of M. edulis F mtDNA into Baltic M. trossulus, accompanied by role reversal and masculinization (Rawson and Hilbish 1998;Quesada et al. 1999). These processes might be coupled and associated with cytonuclear incompatibilities that ...

Molecular Population Genetics of the Male and Female Mitochondrial DNA Molecules of the California Sea Mussel,Mytilus californianus

“…Third, unlike a number of recent studies (e.g., Ladoukakis and Zouros 2001;Burzynski et al 2003Burzynski et al , 2006Rawson 2005;Breton et al 2006), no recombination was detected within or between the M and F molecules. Although both genomes of M. californianus failed the four-gamete test (suggesting recombination within both F and M), the finite-sites model implemented by the method of McVean et al (2002) failed to detect significant recombination, suggesting that its apparent signal was caused by homoplasy.…”

Glacial history of the European marine mussels Mytilus, inferred from distribution of mitochondrial DNA lineages

“…This would, however, have been noticed, as also the original F genome sequence would be amplified, resulting in mixed signals in the sequencing reaction. Moreover, the haplotypes having such structures can be detected with repeat-specific PCR (AB16-AB32 primer pair, as described by Burzyń ski et al, 2006). Our survey showed that such genomes are present in a limited set of localities only, such as the Baltic Sea, the Black Sea and, to a much lesser extent, Mediterranean Sea and the Gulf of Biscay (Filipowicz et al, 2008).…”

“…The lengths of the AB15-AB16 products were approximately 900 base pairs (bp) for the F genome and 770 bp for the M genome, so these could easily be distinguished. However, several reports have claimed that recombination is possible, either within the region or in its vicinity (Burzyń ski et al, 2006;Venetis et al, 2007;Filipowicz et al, 2008), possibly changing the transmission route and consequently making the genome evolving faster. Certain precautions had to be taken to ensure that this did not affect our data in an unpredictable way.…”

“…Such events reset the divergence between both lineages (Hoeh et al, 1997). This seems to be the case for Mytilus mussels from the Baltic Sea where the typical M genome is present only at a very low frequency (Śmietanka et al, 2004) and, in most of the male mussels from the Baltic Sea, highly divergent M genome has been replaced by one of the recently masculinized recombinant genomes (Burzyń ski et al, 2006).…”

Sex Determining Mechanisms in Bivalves

“…The divergent M type is referred to as a "standard male" or SM type, whereas the other M type is referred to as a "recently masculinized" or RM type genome ). Sequencing studies have affirmed that Mytilus RM types are recombinant genomes (e.g., Cao et al 2004b; Burzynski et al 2006). These RM types are composed of an F genome protein coding, ribosomal and transfer RNA genes and, significantly, the control region from an SM type genome.…”