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Population genomics of Monadenia (Gastropoda: Stylommatophora: Xanthonychidae) land snails reveals structuring but gene-flow across distinct species and morphotypes

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Abstract

Establishing conservation priorities requires an understanding of the diversity within and among taxa. Land snails in the subgenus Monadenia consist of six species, three of which are recognized in Oregon, M. fidelis, M. chaceana and a recently discovered M. infumata found north of its presumed range limits in Northern California. Further, M. fidelis is composed of at least six named subspecies, one of which is a candidate for federal listing, and extensive sampling and expert assessments of shell morphology have uncovered even more distinct forms. Still, it is unknown if these morphological variants are truly distinctive units of diversity or rather reflect environmentally driven plasticity. Here we investigate whether there are multiple, structured units of diversity in Washington, Oregon, and California Monadenia. We used COI, a mitochondrial barcode gene, a ddRAD-based genome-wide SNP dataset, along with expert-assessment of morphology, to better delimit diversity of Monadenia in Oregon and in parts of Washington and California to inform conservation strategies for this group. Morphological analyses confirm the existence of distinctive morphotypes, but genomic data show widespread admixture, even at the species level. Still, we do find limited geographic structuring between samples collected in the northern versus southern portions of the study area and possibly weak structuring between populations in the Coast Ranges compared to the Cascade Mountains. Genetic differentiation was similar among the morphotypes in the north–south grouping, but pairwise estimates of differentiation were much greater among some morphotypes and species. Our finding of admixture and gene flow across Monadenia, even at the species level, complicates assessment of individuated units of diversity critical for establishing conservation prioritization. Further work is still necessary, such as including more Monadenia taxa, in order to evaluate species limits and investigate mechanisms underlying the morphological diversity in this group.

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Data availability

COI data is deposited on NCBI GenBank (MZ558785-MZ559288). The ddRAD data can be found on NCBI SRA (PRJNA719865, accession numbers SAMN18674863-SAMN18674973). Accession numbers can be found in Supplementary File 1. Monadenia vouchers were deposited at the Oregon State Arthropod Collection (Accession # OSAC_AC_2021_06_30_001-01; 655 specimens: OSAC_0001258622 — OSAC_0001259277).

Code availability

Code is available through various R package documentation and is available upon request.

Change history

  • 30 November 2021

    On page 8, left column: the word “MMultilocus” replaced with “Multilocus”

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Acknowledgements

We thank Ryan Terrill and Bryan McLean for figure and ddRAD advice; and John Slapcinsky and the Florida Museum for the M. f. infumata tissue sample. Chris Marshall from the Oregon State Arthropod Collection (OSAC) has kindly offered to house the full collection. Field sampling was conducted by a host of people including Bonnie Allison, Molly Brewer, Emily Burke, Dave Clayton, Matt D’Agrosa, Nancy Duncan, Candace Fallon, Dave Gonnella, Carol Hughes, Sarah Malaby, Steve Sheehy, Bryce Smith, Jesse Soy, Nick Stenkamp, Brenda Tippin, Michelle Trombino, and Joe Whiteman. Special thanks to Kevin and Kelly Velarde for allowing access to their property to collect specimens from the M. chaceana type locality.

Funding

This study was funded by BLM L16AC00095, USFS AG-046W-P-17-0084, and USFS 12046W18P0054.

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Authors and Affiliations

  1. Florida Museum of Natural History, University of Florida, 1659 Museum Road, Gainesville, FL, 32611, USA

    Jessica A. Oswald, Cathleen Mestre & Robert P. Guralnick

  2. Biology Department, University of Nevada, Reno, Reno, NV, 89503, USA

    Jessica A. Oswald, Trevor M. Faske & Julie M. Allen

  3. San Francisco, USA

    Barry Roth

  4. USDA Forest Service, Pacific Northwest Region, Portland, OR, 97204, USA

    Darci Rivers-Pankratz

  5. USDI Bureau of Land Management, Oregon/Washington State Office, Portland, OR, 97204, USA

    Kelli Van Norman

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  1. Jessica A. Oswald
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Contributions

BR, DRP, KVN, RPG conceived and designed the study. JAO and CM performed laboratory work. JAO, TMF, JMA performed and/or guided the genomic data analyses. BR identified all Monadenia samples. DRP, KVN led field work initiatives. All authors contributed towards data interpretation and writing of the manuscript. All authors gave final approval for publication and agree to be held accountable for the work performed herein.

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Correspondence to Jessica A. Oswald.

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Washington Department of Fish and Wildlife, Washington State Scientific Collection Permit numbers: VAN NORMAN 16–352 and VAN NORMAN 18–127. Permits are not required in Oregon. California collections were made on private land with permission of landowner, Kevin and Kelly Velarde, Yreka, CA.

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Oswald, J.A., Roth, B., Faske, T.M. et al. Population genomics of Monadenia (Gastropoda: Stylommatophora: Xanthonychidae) land snails reveals structuring but gene-flow across distinct species and morphotypes. Conserv Genet 23, 299–311 (2022). https://doi.org/10.1007/s10592-021-01410-w

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