Ancient Sex-Specific Extension of the Cytochrome c Oxidase II Gene in Bivalves and the Fidelity of Doubly-Uniparental Inheritance

Abstract

Bivalves of the families Mytilidae and Unionidae show a unique mode of mitochondrial DNA inheritance called doubly uniparental inheritance. In addition to receiving the maternally transmitted mtDNA lineage, males receive a separate mtDNA genome from their fathers. This system is sometimes compromised, in that female genomes are occasionally recruited into the male cycle of inheritance. These masculinization events are common in the Mytilidae but have not been reported in the Unionidae. In order to estimate the age of the male and the female lineages in the Unionidae and to look for evidence of masculinization, we sequenced the junction between the cytochrome c oxidase II gene and the cytochrome c oxidase I gene. The unionid male and female lineages diverged approximately 450 MYA. There is no evidence for masculinization during this period, suggesting that there are taxon-specific differences in the rate of masculinization. Coincidentally, a 200-codon extension of the COII gene is present in the male genome of the Unionidae and may be responsible for the absence of masculinization.

Congruence and Conflict Between Molecular and Reproductive Characters When Assessing Biological Diversity in the Western Fanshell Cyprogenia aberti (Bivalvia, Unionidae)1

“…Complementary DNA was quantified and used in subsequent PCR to amplify the male mitotype copy of CO1. A 550-bp region of the male copy of CO1 was amplified and sequenced using primers UNIOMCOIF (Curole, 2005) and HCO2198, by means of the following thermal cycling conditions for 34 cycles: denaturing at 94uC for 40 seconds, annealing at 45uC for 60 seconds, and extension at 72uC for 90 seconds.…”

Maternal inheritance, sexual conflict and the maladapted male

“…This phenomenon, termed masculinization or gender switching, has occurred at least five times in the evolution of Mytiloida [58]. By contrast, in freshwater mussels (Unionoida), there is no evidence of evolutionary loss of paternalmtDNA transmission over the past 200 million years [59]. The stability of DUI in unionoids is associated with the presence of a 185-codon extension of the cytochrome c oxidase II (MTCO2) gene, although whether this is a cause or a consequence of increased DUI fidelity is unknown.…”

Comparative Mitochondrial Genomics of Freshwater Mussels (Bivalvia: Unionoida) With Doubly Uniparental Inheritance of mtDNA: Gender-Specific Open Reading Frames and Putative Origins of Replication

“…This has led to the proposition that an M-type control region, particularly its most variable domain called VD1 by Cao et al (2004a), might be necessary to confer the paternal role on genomes that are otherwise F-like (Burzyń ski et al 2003;Breton et al 2006;Venetis et al 2007). Alternatively, the absence of masculinization or role-reversal events in freshwater bivalves coincides with the presence of a unique M genome-specific 39 extension of the cytochrome c oxidase subunit 2 gene (Mcox2e; Curole and Kocher 2002) that could facilitate the transmission of the M genomes in freshwater bivalves (Breton et al 2007;Chakrabarti et al 2007;Chapman et al 2008). To date, the control region has not been confirmed in unionoid bivalves (see Serb and Lydeard 2003).…”