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Boundaries and hybridization in a secondary contact zone between freshwater mussel species (Family:Unionidae)

Abstract

Correct species identification and delineation are crucial for effective conservation and management. However, species delineation can be problematic in the presence of morphological ambiguities due to phenotypic plasticity, convergence, and/or interspecific hybridization. Here, we investigated the degree of hybridization between two closely related freshwater mussel species [Bivalvia: Unionidae; Lampsilis siliquoidea (Barnes) and L. radiata (Gmelin)] that present intermediate forms in areas of sympatry. Unionids have a distinct form of mitochondrial DNA (mtDNA) inheritance, termed doubly uniparental inheritance (DUI) where female mtDNA (F-type) is transmitted to all progeny but male mtDNA (M-type) is mostly inherited by the males resulting in mostly homoplasmic females and heteroplasmic males. An individual was identified as hybrid when F-type and M-type mtDNA of the two different species were found in the same individual. Twelve out of 116 sequenced males were identified as hybrids indicating that these species hybridize where their geographic range overlaps in the lower Great Lakes and St. Lawrence basins. Microsatellite analyses further support the occurrence of hybridization but at a larger spatial scale than indicated by the mitochondrial analyses. We also found that strong within-species population genetic structure affects the detection of purebred individuals overestimating the number of hybrids. Given the large geographic scale and proportion of hybrids found in this study, natural hybridization and introgression need to be considered when implementing local biodiversity inventories, identifying waterbodies as source of organisms for relocation and restoration projects and when setting appropriate conservation policies.

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Fig. 1: Sampling sites for Lampsilis siliquoidea (orange), L. radiata (dark blue), and putative hybrid zone (shaded gray).
Fig. 2
Fig. 3: Maternally-inherited COI (F-type) Bayesian Inference (BI) and Maximum Likelihood (ML) combined tree.
Fig. 4: Paternally-inherited COI (M-type) Bayesian likelihood and Maximum Likelihood combined tree. Support values are posterior probability for BI and bootstrap for ML.
Fig. 5: Geographic distribution of maternally and paternally-inherited COI haplotypes for Lampsilis siliquoidea (orange) and L. radiata (dark blue) in the putative hybrid zone (as described in Fig. 1).
Fig. 6: Estimation of the number of clusters (K) using the program STRUCTURE for both species.

Data availability

Mitochondrial sequences were deposited in GenBank: accession numbers MN432615-MN432653 and MN432654-MN432663. Microsatellite data were deposited in Dryad data repository accessed at https://doi.org/10.5061/dryad.15dv41nwr.

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Acknowledgements

The authors would like to deeply thank all the colleagues listed in Table 1 who provided tissues. We are very thankful to Nicole Bobel, Susan Daniel, Andrew Hannes, Kimberly McKinnon, Rachel Morganti, Isabelle Picard, Brandon Sansom, Patricia Shulenburg, Vanessa Smilanksi and Brianne Tulumello, who helped in the field collecting tissue. This project was funded by the Student Grants-to-support Research Program, the Great Lakes Research Consortium (IP); Melbourne R. Carriker Student Research Awards in Malacology, The American Malacological Society (IP); and by the Great Lakes Fish and Wildlife Restoration Act “Conservation of Native Freshwater Mussel Refuges in Great Lakes Coastal Wetlands” (project # 30191-A-G152) (DZ and LB). This manuscript is contribution #150 of the Central Michigan University Institute for Great Lakes Research.

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Correspondence to Isabel Porto-Hannes.

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Porto-Hannes, I., Burlakova, L.E., Zanatta, D.T. et al. Boundaries and hybridization in a secondary contact zone between freshwater mussel species (Family:Unionidae). Heredity 126, 955–973 (2021). https://doi.org/10.1038/s41437-021-00424-x

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