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

Author:

Johnson Nathan A1ORCID,Henderson Andrew R2,Jones Jess W3ORCID,Beaver Caitlin E1ORCID,Ahlstedt Steven A4,Dinkins Gerald R4,Eckert Nathan L5,Endries Mark J2,Garner Jeffrey T6,Harris John L7,Hartfield Paul D8,Hubbs Don W9,Lane Timothy W10ORCID,McGregor Monte A11,Moles Kendall R12,Morrison Cheryl L13ORCID,Wagner Matthew D8,Williams James D14,Smith Chase H15ORCID

Affiliation:

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

Abstract

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.

Funder

U.S. Fish and Wildlife Service

U.S. Geological Survey

University of Texas at Austin Stengl-Wyer Endowment

Publisher

Oxford University Press (OUP)

Subject

Genetics (clinical),Genetics,Molecular Biology,Biotechnology

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