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

Abstract

AbstractDoubly 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 genetic 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. Both markers were sequenced for 302 male individuals sampled from the North Sea to the Gironde Estuary (Southern France). Nucleotide 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 ΦST = 0.345 and 0.126 respectively) and the geographic localization of the strongest genetic break significantly differed between the markers (Finistère Peninsula at cox1f; Cotentin Peninsula at cox1m). 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 could be linked to mito-nuclear genetic incompatibilities in this system.