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TitleMesozoic mitogenome rearrangements and freshwater mussel (Bivalvia: Unionoidea) macroevolution
AbstractUsing a new fossil-calibrated mitogenome-based approach, we identified macroevolutionary shifts in mitochondrial gene order among the freshwater mussels (Unionoidea). We show that the early Mesozoic divergence of the two Unionoidea clades, Margaritiferidae and Unionidae, was accompanied by a synchronous split in the gene arrangement in the female mitogenome (i.e., gene orders MF1 and UF1). Our results suggest that this macroevolutionary jump was completed within a relatively short time interval (95% HPD 201-226 Ma) that coincided with the Triassic-Jurassic mass extinction. Both gene orders have persisted within these clades for ~200 Ma. The monophyly of the so-called "problematic" Gonideinae taxa was supported by all the inferred phylogenies in this study using, for the first time, the M- and F-type mitogenomes either singly or combined. Within Gonideinae, two additional splits in the gene order (UF1 to UF2, UF2 to UF3) occurred in the Mesozoic and have persisted for ~150 and ~100 Ma, respectively. Finally, the mitogenomic results suggest ancient connections between freshwater basins of East Asia and Europe near the Cretaceous-Paleogene boundary, probably via a continuous paleo-river system or along the Tethys coastal line, which are well supported by at least three independent but almost synchronous divergence events.
SourceHeredity (Edinb., Print)
KeywordsMitogenome rearrangementspunctuated equilibriumTriassic-Jurassic mass extinctionmacroevolutionary jumpsfreshwater musselsGonideinae
JournalHeredity (Edinb., Print)
EditorLongman Group, Edinburgh, Regno Unito
Year2019
TypeArticolo in rivista
DOI10.1038/s41437-019-0242-y
AuthorsFroufe E.; Bolotov I.; Aldridge D.C.; Bogan A.E.; Breton S.; Gan H.M.; Kovitvadhi U.; Kovitvadhi S.; Riccardi N.; Secci-Petretto G.; Sousa R.; Teixeira A.; Varandas S.; Zanatta D.; Zieritz A.; Fonseca M.M.; Lopes-Lima M.
Text407733 2019 10.1038/s41437 019 0242 y Scopus 2 s2.0 85068035132 Mitogenome rearrangements punctuated equilibrium Triassic Jurassic mass extinction macroevolutionary jumps freshwater mussels Gonideinae Mesozoic mitogenome rearrangements and freshwater mussel Bivalvia Unionoidea macroevolution Froufe E.; Bolotov I.; Aldridge D.C.; Bogan A.E.; Breton S.; Gan H.M.; Kovitvadhi U.; Kovitvadhi S.; Riccardi N.; Secci Petretto G.; Sousa R.; Teixeira A.; Varandas S.; Zanatta D.; Zieritz A.; Fonseca M.M.; Lopes Lima M. CIIMAR/CIMAR Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos s/n, Matosinhos, 4450 208, CIIMAR/CIMAR Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos s/n, Matosinhos, 4450 208, Portugal, , , Portugal; CIIMAR/CIMAR Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos s/n, Matosinhos, 4450 208, CIIMAR/CIMAR Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos s/n, Matosinhos, 4450 208, Portugal, , , Portugal; IBIGER Institute of Biogeography and Genetic Resources, Federal Center for Integrated Arctic Research, Russian Academy of Sciences, Severnaya Dvina Emb. 23, Arkhangelsk, 163000, IBIGER Institute of Biogeography and Genetic Resources, Federal Center for Integrated Arctic Research, Russian Academy of Sciences, Severnaya Dvina Emb. 23, Arkhangelsk, 163000, Russian Federation, , , , Russian Federation; IBIGER Institute of Biogeography and Genetic Resources, Federal Center for Integrated Arctic Research, Russian Academy of Sciences, Severnaya Dvina Emb. 23, Arkhangelsk, 163000, IBIGER Institute of Biogeography and Genetic Resources, Federal Center for Integrated Arctic Research, Russian Academy of Sciences, Severnaya Dvina Emb. 23, Arkhangelsk, 163000, Russian Federation, , , , Russian Federation; IBIGER Institute of Biogeography and Genetic Resources, Federal Center for Integrated Arctic Research, Russian Academy of Sciences, Severnaya Dvina Emb. 23, Arkhangelsk, 163000, IBIGER Institute of Biogeography and Genetic Resources, Federal Center for Integrated Arctic Research, Russian Academy of Sciences, Severnaya Dvina Emb. 23, Arkhangelsk, 163000, Russian Federation, , , , Russian Federation; Northern Arctic Federal University, Severnaya Dvina Emb. 17, Arkhangelsk, 163000, Northern Arctic Federal University, Severnaya Dvina Emb. 17, Arkhangelsk, 163000, Russian Federation, , Russian Federation; Department of Zoology, University of Cambridge, The David Attenborough Building, Pembroke Street, Cambridge, CB2 3QZ, Department of Zoology, University of Cambridge, The David Attenborough Building, Pembroke Street, Cambridge, CB2 3QZ, UK, , United Kingdom; North Carolina State Museum of Natural Sciences, 11 West Jones St., Raleigh, NC, 27601, North Carolina State Museum of Natural Sciences, 11 West Jones St., Raleigh, NC, 27601, USA, , United States; Departement de Sciences Biologiques, Universite de Montreal, Montreal, QC, H2V 2S9, Departement de Sciences Biologiques, Universite de Montreal, Montreal, QC, H2V 2S9, Canada, , Canada; Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Geelong, VIC, 3220, Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Geelong, 3220, VIC, Australia, , Australia; Department of Zoology, Faculty of Science, Kasetsart University, Bangkok, 10900, Department of Zoology, Faculty of Science, Kasetsart University, Bangkok, 10900, Thailand, , Thailand; Department of Agriculture, Faculty of Science and Technology, Bansomdejchaopraya Rajabhat University, Bangkok, 10600, Department of Agriculture, Faculty of Science and Technology, Bansomdejchaopraya Rajabhat University, Bangkok, 10600, Thailand, , Thailand; CNR Institute for Ecosystems Studies, Verbania Pallanza VB , CNR Institute for Ecosystems Studies, Verbania Pallanza VB , Italy, , Italy; CBMA Centre of Molecular and Environmental Biology, Department of Biology, University of Minho, Campus Gualtar, Braga, 4710 057, CBMA Centre of Molecular and Environmental Biology, Department of Biology, University of Minho, Campus Gualtar, Braga, 4710 057, Portugal, , Portugal; CIMO/ESA/IPB Mountain Research Centre, School of Agriculture, Polytechnic Institute of Bragança, Campus de Santa Apolonia, Apartado 1172, Bragança, 5301 854, CIMO/ESA/IPB Mountain Research Centre, School of Agriculture, Polytechnic Institute of Bragança, Campus de Santa Apolonia, Apartado 1172, Bragança, 5301 854, Portugal, , Portugal; CITAB/UTAD Centre for Research and Technology of Agro Environment and Biological Sciences, University of Tras os Montes and Alto Douro, Forestry Department, Vila Real, 5000 801, CITAB/UTAD Centre for Research and Technology of Agro Environment and Biological Sciences, University of Tras os Montes and Alto Douro, Forestry Department, Vila Real, 5000 801, Portugal, , , Portugal; CITAB/UTAD Centre for Research and Technology of Agro Environment and Biological Sciences, University of Tras os Montes and Alto Douro, Forestry Department, Vila Real, 5000 801, CITAB/UTAD Centre for Research and Technology of Agro Environment and Biological Sciences, University of Tras os Montes and Alto Douro, Forestry Department, Vila Real, 5000 801, Portugal, , , Portugal; Biology Department, Institute for Great Lakes Research, Central Michigan University, Biosciences Bldg. 2408, Mount Pleasant, MI, 48859, Biology Department, Institute for Great Lakes Research, Central Michigan University, Biosciences Bldg. 2408, Mount Pleasant, MI, 48859, USA, , United States; School of Environmental and Geographical Sciences, University of Nottingham Malaysia Campus, Jalan Broga, Semenyih, 43500, School of Environmental and Geographical Sciences, University of Nottingham Malaysia Campus, Jalan Broga, Semenyih, 43500, Malaysia, , Malaysia; CIBIO/InBIO Research Center in Biodiversity and Genetic Resources, University of Porto, Campus Agrario de Vairão, Rua Padre Armando Quintas 7, Vairão, Porto, 4485 661, CIBIO/InBIO Research Center in Biodiversity and Genetic Resources, University of Porto, Campus Agrario de Vairão, Rua Padre Armando Quintas 7, Vairão, Porto, 4485 661, Portugal, , , Portugal; CIBIO/InBIO Research Center in Biodiversity and Genetic Resources, University of Porto, Campus Agrario de Vairão, Rua Padre Armando Quintas 7, Vairão, Porto, 4485 661, CIBIO/InBIO Research Center in Biodiversity and Genetic Resources, University of Porto, Campus Agrario de Vairão, Rua Padre Armando Quintas 7, Vairão, Porto, 4485 661, Portugal, , , Portugal; SSC/IUCN Mollusc Specialist Group, Species Survival Commission, International Union for Conservation of Nature, c/o The David Attenborough Building, Pembroke Street, Cambridge, CB2 3QZ, SSC/IUCN Mollusc Specialist Group, Species Survival Commission, International Union for Conservation of Nature, c/o The David Attenborough Building, Pembroke Street, Cambridge, CB2 3QZ, UK, , United Kingdom Using a new fossil calibrated mitogenome based approach, we identified macroevolutionary shifts in mitochondrial gene order among the freshwater mussels Unionoidea . We show that the early Mesozoic divergence of the two Unionoidea clades, Margaritiferidae and Unionidae, was accompanied by a synchronous split in the gene arrangement in the female mitogenome i.e., gene orders MF1 and UF1 . Our results suggest that this macroevolutionary jump was completed within a relatively short time interval 95% HPD 201 226 Ma that coincided with the Triassic Jurassic mass extinction. Both gene orders have persisted within these clades for 200 Ma. The monophyly of the so called problematic Gonideinae taxa was supported by all the inferred phylogenies in this study using, for the first time, the M and F type mitogenomes either singly or combined. Within Gonideinae, two additional splits in the gene order UF1 to UF2, UF2 to UF3 occurred in the Mesozoic and have persisted for 150 and 100 Ma, respectively. Finally, the mitogenomic results suggest ancient connections between freshwater basins of East Asia and Europe near the Cretaceous Paleogene boundary, probably via a continuous paleo river system or along the Tethys coastal line, which are well supported by at least three independent but almost synchronous divergence events. Postprint http //www.scopus.com/record/display.url eid=2 s2.0 85068035132 origin=inward Mesozoic mitogenome rearrangements and freshwater mussel Bivalvia Unionoidea macroevolution. Froufeetal_Heredity_2019.pdf Articolo in rivista Longman Group 0018 067X Heredity Edinb., Print Heredity Edinb., Print Heredity Edinb., Print Heredity Edinb., Print nicolettarita.riccardi RICCARDI NICOLETTA RITA