Discordant population structure inferred from male- and female-type mtDNAs from Limecola 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 insights into the genetic structure of populations and investigate its determinants. In this study, we document differences in genetic diversity, divergence, inter-populational differentiation and biogeographic structure between M- and F-type cox1 mt genes in the Baltic tellin (Macoma balthica) to test whether cox1m and cox1f genes bear the marks of similar phylogeographic histories. These markers were sequenced for 302 male individuals sampled from the North Sea to the Gironde Estuary (Southern France) encompassing the intra-subspecific M. b. rubra hybrid zone in the Gulf of Saint Malo. Both genes supported a scenario of cladogenesis of M.b. rubra clades prior to the last glacial maximum. Nucleotide diversity and net divergence were over twice higher in cox1m compared to cox1f. Genetic differentiation between northern and southern populations was nearly 3 times higher at cox1m compared to cox1f (global {Phi}ST = 0.345 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, [~]250 km apart). A higher mutation rate, relaxed negative selection 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 in a context of secondary contact could be linked to mito-nuclear genetic incompatibilities.