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.
Animal and plant species exhibit an astonishing diversity of sexual systems, including environmental and genetic determinants of sex, with the latter including genetic material in the mitochondrial genome. In several hermaphroditic plants for example, sex is determined by an interaction between mitochondrial cytoplasmic male sterility (CMS) genes and nuclear restorer genes. Specifically, CMS involves aberrant mitochondrial genes that prevent pollen development and specific nuclear genes that restore it, leading to a mixture of female (male‐sterile) and hermaphroditic individuals in the population (gynodioecy). Such a mitochondrial‐nuclear sex determination system is thought to be rare outside plants. Here, we present one possible case of CMS in animals. We hypothesize that the only exception to the strict maternal mtDNA inheritance in animals, the doubly uniparental inheritance (DUI) system in bivalves, might have originated as a mitochondrial‐nuclear sex‐determination system. We document and explore similarities that exist between DUI and CMS, and we propose various ways to test our hypothesis.
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