Discordant population structure inferred from male- and female-type mtDNAs from Macoma balthica, a bivalve species characterized by doubly uniparental inheritance of mitochondria

Abstract

Doubly Uniparental Inheritance (DUI) of mitochondria is a remarkable exception to the Strictly Maternal Inheritance (SMI) in metazoans. In species characterized by DUI --almost exclusively gonochoric bivalve mollusks--, females (F) transmit mitochondria to offspring of both sexes, while males (M) pass on their mitochondria exclusively to their sons. Under DUI, males are heteroplasmic, somatic tissues containing F-transmitted mtDNA and gametic cells containing M-transmitted mtDNAs. The aforementioned transmission routes make M- and F-transmitted mtDNA interesting as sex-specific markers which can differ in their effective population sizes, mutation rates, and selective constraints. For these reasons, looking at both markers can provide significant insight into the genetic structure of populations and investigate its determinants. In this study, we document differences in genetic diversity, divergence, inter-populational genetic differentiation and biogeographic structure between M- and F-type cox1 mt genes in the Baltic tellin (Limecola balthica) to test whether cox1m and cox1f genes bear the marks of similar phylogeographic histories. Both markers were sequenced for 313 male individuals sampled from the Baltic Sea to the Gironde Estuary (Southern France). Haplotype diversity and net divergence were over twice higher in cox1m compared to cox1f. A strong southward decrease in nucleotide diversity was observed only at cox1m. Genetic differentiation between northern and southern populations was nearly 3 times higher at cox1m compared to cox1f (global phiST = 0.447 and 0.126 respectively) and the geographic localization of the strongest genetic break significantly differed between the markers (Finistere Peninsula at cox1f; Cotentin Peninsula at cox1m). A higher mutation rate, relaxed negative selective pressure and differences in effective population sizes (depending on locations) at cox1m could explain differences in population genetic structure. As both F- and M-type mtDNAs interact with nuclear genes for oxidative phosphorylation and ATP production, geographical discordances in genetic clines could be linked to mito-nuclear genetic incompatibilities in this system.

LAMP‐based molecular sexing in a gonochoric marine bivalve (Macoma balthica rubra) with divergent sex‐specific mitochondrial genomes

“…To detect the potential occurrence of DUI disruption in Macoma balthica rubra , individuals were sampled on both sides of the French hybrid zone that spans between the Finistère and the Cotentin peninsulas (Becquet et al, 2012 ; Le Cam et al, 2022 ). Northeast of this region, we sampled specimens in Somme Bay (Le Crotoy, abbreviated ‘CRO’).…”

“…As for PCR primers, we checked that primers would be compatible with the range of genetic variation within M. balthica rubra . For that, primers were aligned to all the unique haplotypes of cox1m recorded in the distributional range of the focal species, that is from Aytré (France) to Lomma (Sweden; Le Cam et al, 2022 ; Figure S1 ). The region amplified by the LAMP primers ranged from the positions 535 to 747 of the entire cox1 gene (Genbank accession number MH 285592.1).…”

“…The stretch of coast located between the Finistère and Cotentin Peninsulas harbours a transition zone between spatially separated genetic stocks (called thereafter ‘hybrid zone’ Figure 2 ; Becquet et al, 2012 ; their Figures 1 and 3). This area is characterized by strong population differentiation ( F ST = 0.48 at F‐type cox1 , F ST = 0.58 at M‐type cox1 , Le Cam et al, 2022 ; nuclear coding SNP F ST up to 1, Pante et al, 2012 and microsatellites F ST = 0.021–0.035, Becquet et al, 2012 ) and geographically‐discordant genetic clines, with F‐type mtDNA being structured around the Finistère Peninsula, while the M‐type mtDNA is structured around the Cotentin Peninsula (Le Cam et al, 2022 ). To our knowledge, DUI disruption had not yet been investigated in intra‐specific hybrid zones.…”

“…Intra‐individual divergence between the M and the F mitotype can reach 54% at nad6 , with an overall divergence level of 41% at the scale of the mitogenome (Capt et al, 2020 ). This species is broadly distributed along the coasts of the northern hemisphere, with populations in the eastern Atlantic spreading from the north of Russia (Hummel et al, 1997 ) to the Arcachon Basin (Hily, 2013 ; Le Cam et al, 2022 ). The northeastern Atlantic populations correspond to the sub‐species M. balthica rubra (Väinölä, 2003 ).…”

“…Study sites are depicted as blue dots. The location of the intra‐specific hybridization zone described in Becquet et al ( 2012 ) and Le Cam et al ( 2022 ) is represented as a thick gray line, and spans, based on current knowledge, from Saint‐Brieuc to Mont‐Saint‐Michel Bay.…”