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Glacial vicariance and secondary contact shape demographic histories in a freshwater mussel species complex

Article in Journal of Heredity | November 2023 | DOI: 10.1093/jhered/esad075

Nathan A. Johnson1*, Andrew R. Henderson2, Jess W. Jones3, Caitlin E. Beaver1, Steven A. Ahlstedt4, Gerald R. Dinkins4, Nathan L. Eckert5, Mark J. Endries2, Jeffrey T. Garner6, John L. Harris 7, Paul D. Hartfield8, Don W. Hubbs9, Timothy W. Lane10, Monte A. McGregor11, Kendall R. Moles12, Cheryl L. Morrison13, Matthew D. Wagner8, James D. Williams14, Chase H. Smith15


Abstract

Characterizing the mechanisms influencing the distribution of genetic variation in aquatic species can be difficult due to the dynamic nature of hydrological landscapes. In North America‘s Central Highlands, a complex history of glacial dynamics, long-term isolation, and secondary contact have shaped genetic variation in aquatic species. Although the effects of glacial history have been demonstrated in many taxa, responses are often lineage- or species-specific and driven by organismal ecology. In this study, we reconstruct the evolutionary history of a freshwater mussel species complex using a suite of mitochondrial and nuclear loci to resolve taxonomic and demographic uncertainties. Our findings do not support Pleurobema rubrum as a valid species, which is proposed for listing as threatened under the U.S. Endangered Species Act. We synonymize P. rubrum under Pleurobema sintoxia—a common and widespread species found throughout the Mississippi River Basin. Further investigation of patterns of genetic variation in P. sintoxia identified a complex demographic history, including ancestral vicariance and secondary contact, within the Eastern Highlands. We hypothesize these patterns were shaped by ancestral vicariance driven by the formation of Lake Green and subsequent secondary contact after the last glacial maximum. Our inference aligns with demographic histories observed in other aquatic taxa in the region and mirrors patterns of genetic variation of a freshwater fish species (Erimystax dissimilis) confirmed to serve as a parasitic larval host for P. sintoxia. Our findings directly link species ecology to observed patterns of genetic variation and may have significant implications for future conservation and recovery actions of freshwater mussels.

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1 U.S. Geological Survey, Wetland and Aquatic Research Center, Gainesville, FL, United States
2 U.S. Fish and Wildlife Service, Ecological Services, Asheville, NC, United States
3 U.S. Fish and Wildlife Service, Virginia Tech University, Blacksburg, VA, United States
4 McClung Museum of Natural History and Culture, University of Tennessee, Knoxville, TN, United States
5 U.S. Fish and Wildlife Service, Neosho National Fish Hatchery, Neosho, MO, United States
6 Alabama Division of Wildlife and Freshwater Fisheries, Florence, AL, United States
7 Arkansas State University Museum of Zoology, Jonesboro, AR, United States
8 U.S. Fish and Wildlife Service, Ecological Services, Jackson, MS, United States
9 DJH Environmental Services, Camden, TN, United States
10 Virginia Department of Wildlife Resources, Marion, VA, United States
11 Kentucky Department of Fish and Wildlife Resources, Frankfort, KY, United States
12 Arkansas Game and Fish Commission, Benton, AR, United States
13 U.S. Geological Survey, Eastern Ecological Science Center, Kearneysville, WV, United States
14 Florida Museum, University of Florida, Gainesville, FL, United States
15 Department of Integrative Biology, University of Texas at Austin, Austin, TX, United States

*Corresponding author: U.S. Geological Survey, Wetland and Aquatic Research Center, 7920 NW 71st Street, Gainesville, FL 32653, United States.