The study by Le Cam and colleagues, entitled “Discordant population structure inferred from male- and female-type mtDNAs from Macoma balthica, a bivalve species characterized by doubly uniparental inheritance of mitochondria”, provides a fascinating exploration of the genetic structure and evolutionary dynamics of the Baltic tellin, Macoma balthica, a bivalve species exhibiting doubly uniparental inheritance (DUI) of mitochondria. This work is a significant contribution to the field of evolutionary biology, particularly in understanding how sex-specific mitochondrial inheritance can shape population structure and genetic diversity in marine organisms.

DUI is a remarkable exception to the typical maternal inheritance of mitochondria in metazoans, where both males and females can transmit their mitochondria, but through different routes. In species with DUI, females pass on their mitochondria to all offspring, while males transmit their mitochondria exclusively to their sons. This system results in males being heteroplasmic, carrying both maternal (F-type) and paternal (M-type) mitochondrial DNA (mtDNA). The study leverages this unique inheritance pattern to investigate the genetic diversity, divergence, and population structure of M. balthica across its distribution range, from the North Sea to the Gironde Estuary in Southern France.

One of the most striking findings of this study is the discordant population structure inferred from the male- and female-type mtDNAs. The authors sequenced the cox1 gene from both F-type and M-type mtDNA in 302 male individuals across 14 sampling sites. They found that the genetic differentiation between northern and southern populations was nearly three times higher for the M-type mtDNA compared to the F-type mtDNA. This discrepancy was further highlighted by the geographic localization of the strongest genetic break, which differed significantly between the two markers. For the F-type mtDNA, the break was located at the Finistère Peninsula, while for the M-type mtDNA, it was found at the Cotentin Peninsula, approximately 250 km apart. The authors propose several explanations for these differences, including a higher mutation rate, relaxed negative selection, and variations in effective population sizes for the M-type mtDNA. These factors could contribute to the observed divergence in genetic structure between the two mitochondrial types. Additionally, the study suggests that mito-nuclear genetic incompatibilities, arising from the interaction between mitochondrial and nuclear genes involved in oxidative phosphorylation and ATP production, could play a role in maintaining these genetic barriers.

The study also provides valuable insights into the phylogeographic history of M. balthica. The divergence times estimated for the F-type and M-type mtDNA clades suggest that the split between the northern and southern populations occurred before the last glacial maximum (LGM). This finding supports a scenario of pre-LGM vicariance rather than post-glacial primary intergradation. The authors' use of net divergence to estimate the timing of cladogenesis events within the Macoma species complex adds a robust temporal dimension to their phylogeographic analysis.

Another intriguing aspect of the study is the evidence of asymmetric introgression and hybrid zone dynamics. The authors observed that the genetic clines for the F-type and M-type mtDNAs were not only discordant in their geographic locations but also in their widths. The cline for the M-type mtDNA was significantly narrower than that for the F-type mtDNA, suggesting different selective pressures or migration balances acting on the two mitochondrial types. This finding raises important questions about the role of sex-specific selection and gene flow in shaping the genetic structure of populations with DUI.

The study also highlights the importance of considering sex-specific genetic markers in population genetic studies. One of the most intriguing aspects is the implication that M-type mtDNA may be evolving under different constraints than its female counterpart. The authors found higher nucleotide diversity and net divergence in M-type sequences suggestive of a relaxed selective regime or an increased mutation rate, which aligns with previous studies on DUI species. Given that M-type mitochondria function predominantly in sperm cells, the potential for oxidative damage, reduced purifying selection, and a higher mutation rate could explain these patterns. More broadly, this finding reinforces the idea that mitochondrial genomes, though typically constrained by purifying selection, can evolve along sex-specific trajectories when their inheritance is decoupled from maternal transmission.

While the study provides compelling evidence for the role of DUI in shaping the genetic structure of M. balthica, it also raises several questions for future research. For instance, the mechanisms underlying the higher mutation rate and relaxed selection in the M-type mtDNA remain to be fully elucidated. Additionally, the potential role of mito-nuclear incompatibilities in maintaining genetic barriers warrants further investigation. The authors suggest that future studies should explore the fitness consequences of inter-lineage crosses and the potential for asymmetric hybrid fitness in the context of DUI.

In conclusion, Le Cam and colleagues have made a significant contribution to our understanding of the evolutionary dynamics of mitochondrial inheritance in bivalves. Their findings not only shed light on the complex interplay between genetic, demographic, and selective factors in shaping population structure but also underscore the importance of considering sex-specific genetic markers in evolutionary studies. This work opens up new avenues for research into the role of DUI in speciation, adaptation, and the maintenance of genetic diversity in marine organisms.

References

Sabrina Le Cam, Brémaud Julie, Vanessa Becquet, Valerie Huet, Pascale Garcia, Amélia Viricel, Sophie Breton, Eric Pante (2025) Discordant population structure inferred from male- and female-type mtDNAs from Macoma balthica, a bivalve species characterized by doubly uniparental inheritance of mitochondria. bioRxiv, ver.4 peer-reviewed and recommended by PCI Evol Biol https://doi.org/10.1101/2022.02.28.479517