Integrative phylogenetic, phylogeographic and morphological characterisation of the Unio crassus species complex reveals cryptic diversity with important conservation implications

• Published in: Molecular phylogenetics and evolution Vol. 195; p. 108046
• Main Authors: Lopes-Lima, M., Geist, J., Egg, S., Beran, L., Bikashvili, A., Van Bocxlaer, B., Bogan, A.E., Bolotov, I.N., Chelpanovskaya, O.A., Douda, K., Fernandes, V., Gomes-dos-Santos, A., Gonçalves, D.V., Gürlek, M.E., Johnson, N.A., Karaouzas, I., Kebapçı, Ü., Kondakov, A.V., Kuehn, R., Lajtner, J., Mumladze, L., Nagel, K.-O., Neubert, E., Österling, M., Pfeiffer, J., Prié, V., Riccardi, N., Sell, J., Schneider, LD, Shumka, S., Sîrbu, I., Skujienė, G., Smith, CH, Sousa, R., Stöckl, K., Taskinen, J., Teixeira, A., Todorov, M., Trichkova, T., Urbańska, M., Välilä, S., Varandas, S., Veríssimo, J., Vikhrev, I.V., Woschitz, G., Zając, K., Zając, T., Zanatta, D., Zieritz, A., Zogaris, S., Froufe, E.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.06.2024; Elsevier
• Subjects: Animal biology; Asia; Biodiversity; Biologi; Biology; Conservation; cryptic species; Europe; freshwater; Freshwater mussels; gene flow; genetic variation; hybrids; Invertebrate Zoology; Life Sciences; Miocene epoch; mitochondria; mitochondrial DNA; mitochondrial genome; morphometry; oxidoreductases; phylogeny; Phylogeography; Pleistocene epoch; Pliocene epoch; species; species diversity; Systematics, Phylogenetics and taxonomy; Unio; Unionida; Asia; Europe; Unionida; Freshwater mussels; Phylogeography; Conservation
• ISSN: 1055-7903; 1095-9513; 1095-9513
• DOI: 10.1016/j.ympev.2024.108046

[Display omitted] •Freshwater mussels of the Unio crassus complex were sampled comprehensively throughout Eurasia.•Sequences of COI, whole mitogenomes and nuclear Anchored Hybrid Enrichment were used to infer phylogenies.•The Unio crassus complex was divided into 12 geographically structured species.•Morphometry of the shell outline revealed morphospace overlaps among several species.•New systematics, taxonomy, and conservation remarks on these species are provided. The global decline of freshwater mussels and their crucial ecological services highlight the need to understand their phylogeny, phylogeography and patterns of genetic diversity to guide conservation efforts. Such knowledge is urgently needed for Unio crassus, a highly imperilled species originally widespread throughout Europe and southwest Asia. Recent studies have resurrected several species from synonymy based on mitochondrial data, revealing U. crassus to be a complex of cryptic species. To address long-standing taxonomic uncertainties hindering effective conservation, we integrate morphometric, phylogenetic, and phylogeographic analyses to examine species diversity within the U. crassus complex across its entire range. Phylogenetic analyses were performed using cytochrome c oxidase subunit I (815 specimens from 182 populations) and, for selected specimens, whole mitogenome sequences and Anchored Hybrid Enrichment (AHE) data on ∼ 600 nuclear loci. Mito-nuclear discordance was detected, consistent with mitochondrial DNA gene flow between some species during the Pliocene and Pleistocene. Fossil-calibrated phylogenies based on AHE data support a Mediterranean origin for the U. crassus complex in the Early Miocene. The results of our integrative approach support 12 species in the group: the previously recognised Unio bruguierianus, Unio carneus, Unio crassus, Unio damascensis, Unio ionicus, Unio sesirmensis, and Unio tumidiformis, and the reinstatement of five nominal taxa: Unio desectusstat. rev., Unio gontieriistat. rev., Unio mardinensisstat. rev., Unio nanusstat. rev., and Unio vicariusstat. rev. Morphometric analyses of shell contours reveal important morphospace overlaps among these species, highlighting cryptic, but geographically structured, diversity. The distribution, taxonomy, phylogeography, and conservation of each species are succinctly described.