DOUBLY UNIPARENTAL INHERITANCE (DUI) OF MITOCHONDRIAL DNA INDONAX TRUNCULUS(BIVALVIA: DONACIDAE) AND THE PROBLEM OF ITS SPORADIC DETECTION IN BIVALVIA

Abstract

Mitochondrial DNA is transmitted maternally in metazoan species. This rule does not hold in several species of bivalves that have two mtDNA types, one that is transmitted maternally and the other paternally. This system of mitochondrial DNA transmission is known as doubly uniparental inheritance (DUI). Here we present evidence of DUI in the clam Donax trunculus making Donacidae the sixth bivalve family in which the phenomenon has been found. In addition, we present the taxonomic affiliation of all species in which DUI is currently known to occur and construct a phylogeny of the maternal and paternal genomes of these species.We use this information to address the question of a single or multiple origins of DUI and to discuss whether failed attempts to demonstrate the presence of DUI in several bivalve species might be due to problems of detection or to genuine absence of the phenomenon.KEY WORDS: Biparental inheritance, bivalve mitochondrial DNA, origin of DUI, reversal of transmission route, Tellinoidea.

Population genetic structure of Calanoides natalis (Copepoda, Calanoida) in the eastern Atlantic Ocean and Benguela upwelling system

“…Typically, identical copies of mtDNA sequences in animals (known as homoplasmy) (Birky, 2001) serve as a crucial assumption in population genetic studies based on mtDNA, even though mitochondrial heteroplasmy and recombination may be more common than previously thought (Rokas et al, 2003;Barr et al, 2005). One mechanism leading to heteroplasmy, doubly uniparental inheritance has been found in many bivalves (Saavedra et al, 1997;Breton et al, 2007;Theologidis et al, 2008;Dégletagne et al, 2016) where genetically distinct male and female mitochondrial lineages exist. However, a strict separation of genderspecific lineages does not seem to be common in C. natalis, as males were found to have similar haplotypes as females in this study.…”

Characteristics of mitochondrial DNA of unionid bivalves (Mollusca: Bivalvia: Unionidae). I. Detection and characteristics of doubly uniparental inheritance (DUI) of unionid mitochondrial DNA

“…The presence of both F and M forms in male gonads was observed in the mytilid Geukensia demissa and a unionid Fusconia flava (HOEH et al 1996a, b). Difficulty to detect both mtDNA genomes in various species may also result from their great divergence; in such a case the DNA primers used may reveal only one, most often female haplotype (THEOLOGIDIS et al 2008). Less variable female genomes offer a greater chance of obtaining similar sequences in many taxa with the use of the same PCR primers.…”

“…Three main subfamilies are distinguished within Unionidae: Ambleminae, Anodontinae and Unioninae, the last two being more closely related , GRAF 2002, HUANG et al 2002 and occurring in Europe. Phylogenetic analyses conducted independently for all analysed mitochondrial genes of European unionids grouped sequences of F and M haplotypes in separate clades according to the literature data (HOEH et al 1996a, 2002a, CUROLE & KOCHER 2002, SOROKA 2008a, b, THEOLOGIDIS et al 2008. This suggests that the origin of DUI precedes speciation.…”

“…Sex-dependent heteroplasmy with two different forms of mtDNA transmitted to the next generations both maternally and paternally was first described in marine bivalves of the genus Mytilus in 1990 and called DUI, doubly uniparental inheritance (FISHER & SKIBINSKI 1990). Besides three species of Mytilus, DUI was detected in a few species representing six bivalve families, and is the most frequent in Unionidae, which have recently been intensely studied in this respect (HOEH et al 1996a, b, LIU et al 1996, PASSAMONTI & SCALI 2001, CUROLE & KOCHER 2002, KREBS 2004, MOCK et al 2004, WALKER et al 2006a, CHAKRABARTI et al 2006, THEOLOGIDIS et al 2008, SOROKA 2008a, b, BRETON et al 2009, DOUCET-BEAUPRÉ et al 2010). …”

“…The two mitochondrial genomes in bivalves are of similar size, close to that in birds and mammals, but evolve faster, and M type evolves faster than F type (STEWART et al 1995, HOEH et al 1996b, ZOUROS 2000. The presence of DUI in seven phylogenetically remote families (Mytilidae, Unionidae, Margaritiferidae, Hyriidae, Veneridae, Donacidae and Solenidae) suggests that the phenomenon may be widespread among bivalves (SKIBINSKI et al 1994, ZOUROS et al 1994, RAWSON & HILBISH 1995, HOEH et al 1996a, LIU et al 1996, PASSAMONTI & SCALI 2001, HOEH et al 2002b, CUROLE & KOCHER 2005, WALKER et al 2006b, THEOLOGIDIS et al 2008, SOROKA 2008a. Though this unusual way of mtDNA inheritance (DUI) occurs mainly in marine and freshwater bivalves, the two groups show marked differences in the characteristics and fidelity of transfer of the two mitochondrial genomes.…”