The detection of sex-linked heteroplasmy inPseudocardium sachalinense(Bivalvia: Mactridae) and its implications for the distribution of doubly uniparental inheritance of mitochondrial DNA

Abstract

Although mitochondrial inheritance in metazoans is typically strictly maternal, doubly uniparental inheritance (DUI) is probably the major exception to this widespread rule. DUI has been found in many species of bivalve molluscs, belonging to several different families. Based on current understanding, the detection of DUI generally relies on the detection of two distinct mitochondrial DNA lineages: a female-transmitted one, that dominates somatic tissues in males and females and eggs, and a male-transmitted one, that dominates the male germline and sperm. When a new species with DUI is identified, novel data are available to make a better inference on the evolution of this phenomenon within the Bivalvia. In this study, mitochondrial heteroplasmy in Pseudocardium sachalinense (Schrenck, 1862) is described. This species belongs to the family of Mactridae, in which DUI has not been previously demonstrated: this finding allowed to upgrade the present knowledge about the distribution of DUI.

Doubly uniparental inheritance and highly divergent mitochondrial genomes of the freshwater mussel Unio tumidus (Bivalvia: Unionidae)

“…The strong correlation between local AT-skew and the direction of translation has been noted previously (Soroka & Burzyński, 2010, 2015 and seems to be characteristic for all Unionidae mitochondrial genomes, with possible exception of MORF gene (Fig. 1).…”

“…Currently, DUI has been confirmed in several bivalve families (Mytilidae, Unionidae, Margaritiferidae, Hyriidae, Veneridae, Donacidae, Nuculanidae, Mactridae, Arcticidae, and Solenidae), suggesting widespread occurrence of the phenomenon in 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, 2002;Curole & Kocher, 2005;Walker et al, 2006;Soroka, 2008;Theologidis et al, 2008;Boyle & Etter, 2013;Huang et al, 2013;Plazzi, 2015;Soroka & Burzyński, 2015Dégletagne et al, 2016). Under DUI, two types of mitochondrial DNA are present: haplotype F (female genome)-inherited according to SMI and haplotype M (male genome)-inherited from fathers to sons.…”

Pursuing the quest for better understanding the taxonomic distribution of the system of doubly uniparental inheritance of mtDNA

“…Genetic distances and phylogenetic analyses provide evidence for sex-associated mitochondrial heteroplasmy in Scrobicularia plana (Bivalvia: Semelidae) and Yoldia hyperborea (Bivalvia: Yoldiidae), raising the total of bivalve families in which DUI has been discovered to 12 (Hoeh, Stewart & Guttman, 2002; Theologidis et al, 2008; Boyle & Etter, 2013; Plazzi, 2015; Dégletagne, Abele & Held, 2016). …”

“…To date, the vast majority of species with DUI that have been reported belong to the freshwater bivalve order Unionoida (families Hyriidae, Margaritiferidae, Unionidae) mostly because the PCR-based method used to detect DUI in this group, which is based on amplifying the cox2 extension specific to unionoid male mtDNAs (Curole & Kocher, 2002), is simple and effective (Walker et al, 2006). The other groups in which species with DUI have been found are the orders Mytiloida (family Mytilidae) (Hoeh, Blakley & Brown, 1991; Skibinski, Gallagher & Beynon, 1994; Zouros et al, 1994a; Zouros et al, 1994b; Passamonti, 2007), Veneroida (families Arcticidae, Donacidae, Mactridae, Solenidae, Veneridae) (Theologidis et al, 2008; Plazzi, 2015; Dégletagne, Abele & Held, 2016), and Nuculanoida (family Nuculanidae), an order belonging to the most basal protobranch bivalve lineage (Boyle & Etter, 2013). It is still unsettled whether DUI has a single origin followed by its loss in several bivalve lineages or whether it has multiple and independent origins (Hoeh et al, 1996; Theologidis et al, 2008; Zouros, 2013; Milani et al, 2014).…”

“…Such an approach has already been successfully implemented in several previous DUI studies (e.g., Passamonti & Scali, 2001; Theologidis et al, 2008; Boyle & Etter, 2013; Plazzi, Cassano & Passamonti, 2015; Plazzi, 2015; Vargas et al, 2015; Dégletagne, Abele & Held, 2016). In the present study, we use this approach to test for the presence of DUI in two bivalve species, i.e., the nuculanoid Yoldia hyperborea (Gould, 1841) and the veneroid Scrobicularia plana (Da Costa, 1778), and we observe sex-linked heteroplasmy (thus the possible presence of DUI) in both of them, increasing the number of families in which DUI has been found by two.…”