A Distinct Mitochondrial Genome with DUI-Like Inheritance in the Ocean QuahogArctica islandica

Abstract

Mitochondrial DNA (mtDNA) is strictly maternally inherited in metazoans. The major exception to this rule has been found in many bivalve species which allow the presence of different sex-linked mtDNA molecules. This mechanism, named doubly uniparental inheritance (DUI), is characterized by the presence of two mtDNAs: The female mtDNA is found in somatic tissue and female gonads, whereas the male mtDNA is usually found in male gonads and sperm. In this study we highlight the existence of two divergent mitochondrial haplotypes with a low genetic difference around 6–8% in Arctica islandica, a long-lived clam belonging to the Arcticidae, a sister group to the Veneridae in which DUI has been found. Phylogenetic analysis on cytochrome b and 16S sequences from somatic and gonadic tissues of clams belonging to different populations reveals the presence of the “divergent” type in male gonads only and the “normal” type in somatic tissues and female gonads. This peculiar segregation of divergent mtDNA types speaks for the occurrence of the DUI mechanism in A. islandica. This example also highlights the difficulties to assess the presence of such particular mitochondrial inheritance system and underlines the possible misinterpretations in phylogeographic and phylogenetic studies of bivalve species linked to the presence of two poorly differentiated mitochondrial genomes.

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.…”

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

“…During the last decade, DUI has been described as a phenomenon that occurs in approximately 40 bivalve species (e.g., Walker et al, 2006; Theologidis et al, 2008; Doucet-Beaupré et al, 2010; Dégletagne, Abele & Held, 2016). Considering the great deal of new literature on DUI that has been done in the last few years, a more accurate count of species with DUI is clearly needed.…”

“…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.…”

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

“…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.…”