Multi-locus fossil-calibrated phylogeny, biogeography and a subgeneric revision of the Margaritiferidae (Mollusca: Bivalvia: Unionoida)

• The crown group of Margaritiferidae originated during the Cretaceous.
• All margaritiferids are in the genus Margaritifera but are separated into 3 subgenera.
• M. togakushiensis is a synonym of M. middendorffi, which ranges widely into East Asia.
• Substitution rates of mtDNA evolution of the Margaritiferidae are slow.

The taxonomy and biogeographic history of the bivalve family Margaritiferidae are controversial because previous molecular studies did not provide a well-resolved phylogenetic framework for these enigmatic freshwater mussels that have extensive but disjunct distribution in North America, Eurasia and North Africa. In this study, we present a new, fossil-calibrated phylogenetic hypothesis based on five molecular markers (∼4 kb of total length) for ten species. Our results indicate that all recent margaritiferids are in the single genus, Margaritifera Schumacher, 1816. Additionally, we identified three relatively well-supported phylogenetic clades that are valid subgenera, i.e., Margaritifera s. str. (Holarctic), Margaritanopsis (=Cumberlandia) (southeast North America-southeast Asia disjunct) and Pseudunio (Mediterranean). We suggest that the crown lineage of the Margaritiferidae most likely originated in the Cretaceous (mean age 93 Ma, 95% CI 66–126 Ma). The combined results of ancestral area reconstructions based on the three different approaches (S-DIVA, DEC and S-DEC) showed that ancient vicariance events could have played an important role in speciation within the family. The rates of mitochondrial evolution of margaritiferids are notably slow, which may be associated with their longevity, long generation time and low metabolic rates. Our findings highlight the complex biogeographic history of the Margaritiferidae as an intermixing of ancient vicariance and dispersal events, which were most likely associated with some inland barriers, continental movements and a sea level dynamic.

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