Integrative phylogenetic, phylogeographic and morphological characterisation of the Unio crassus species complex reveals cryptic diversity with important conservation implications
Manuel Lopes‐Lima, Juergen Geist, Sarah Egg, Luboš Beran, Ani Bikashvili, Bert Van Bocxlaer, Arthur E. Bogan, Ivan N. Bolotov, O.A. Chelpanovskaya, Karel Douda, Vasco Fernandes, André Gomes‐dos‐Santos, Duarte V. Gonçãlves, Mevlüt Gürlek, N.A. Johnson, Ioannis Karaouzas, Ümit Kebapçı, Alexander V. Kondakov, Ralph Kuehn, Jasna Lajtner, Levan Mumladze, K.-O. Nagel, Eike Neubert, Martin Österling, John M. Pfeiffer, Vincent Prié, Nicoletta Riccardi, Jerzy Sell, LD. Schneider, Spase Shumka, Ioan Sîrbu, Grita Skujienė, CH. Smith, Ronaldo Sousa, Katharina Stöckl, Jouni Taskinen, Amílcar Teixeira, Milcho Todorov, Teodora Trichkova, Maria Urbańska, S. Välilä, Simone Varandas, Jady L. Veríssimo, Ilya V. Vikhrev, G. Woschitz, Katarzyna Zając, Tomasz Zając, David T. Zanatta, Alexandra Zieritz, Stamatis Zogaris, Elsa Froufe
Abstract
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.