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Genetic and morphological comparisons of lesser celandine (Ficaria verna) invasions suggest regionally widespread sexual reproduction

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Abstract

Both asexual and sexual reproduction can provide important keys to the success of invasive species. A species with potential for both is lesser celandine (Ficaria verna), a European native with multiple subspecies that have been introduced in North America as ornamentals and escaped cultivation. Asexual reproduction via bulbils is prolific in many introduced populations of lesser celandine, with sexual reproduction reportedly rare. Although genetic and morphological diversity of European celandine has been studied, few have examined invasive North American populations. We aimed to document introduced genotypic and phenotypic diversity at a regional scale. We first compared sequence-related amplified polymorphism (SRAP) genotypes of 64 individuals collected from Columbus, Cincinnati, and Cleveland, OH. In a second experiment, we phenotyped 129 individuals from the same regions and from Louisville, KY, measuring traits in an outdoor common garden experiment. The SRAP markers were highly polymorphic and revealed surprising genetic differentiation. Genetic and trait variation were both structured across regions, but we also saw high variation within regions. Cleveland populations differed the most genetically and morphologically. Nearly every individual made asexual bulbils, and many individuals that flowered produced expanded achenes. Trait data suggested subspecies verna or ficariiformis occur in these regions. Genetic admixture within regions and within individuals, along with achene expansion, suggests sexual reproduction may be widespread. Sexual and asexual propagules may spread by different vectors, and our resistance analyses indicated water dispersal and habitat availability contribute to genetic structure. These findings suggest that celandine has substantial potential for further spread and evolutionary change.

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Acknowledgements

We are grateful for the help of Jennifer Hillmer and Pat Lorch of Cleveland Metroparks and Paul Pira of the Geauga Park District for assistance with sites. We thank Dr. Michael Broe, Leah Weston, Dr. Scott Martin, and Dr. Bill Peterman for assistance with analyses and Dr. Alison Bennett, Associate Editor Dr. Kristin Saltonstall, Alexis Wafer, Dr. Andi Wolfe, and two anonymous reviewers for feedback on analyses and writing. We thank the Cornell University Biotechnology Resource Center for fragment analysis services. For lab assistance, we thank Eleanor Chase. For facilities support, we thank Ohio State’s Biological Sciences and Biotechnology Support Greenhouses, Center for Applied Plant Sciences, Gary Posey, David Snodgrass, and Emily Yoders-Horn. This work was supported by the Ohio State Alumni Grant for Graduate Research and Scholarship and Presidential Fellowship to KZM and start-up funds to SMH.

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This work was supported by the Ohio State Alumni Grant for Graduate Research and Scholarship and Presidential Fellowship to KZM and start-up funds to SMH.

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SMH, CTCD, and AT together designed the project. CTCD, ESJR, and AT oversaw surveys and data collection, supervised by SMH. CTCD and KZM developed genetics protocols, KZM and AT executed genetic analyses, and AT performed morphological sampling. KZM and AT analysed and interpreted data, supervised by SMH and ESJR. KZM wrote the manuscript with contributions from AT, SMH, and ESJR. All authors reviewed and approved the final manuscript.

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Correspondence to Kali Z. Mattingly.

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10530_2022_2921_MOESM6_ESM.jpg

Fig. S1. Rasters used to create distance matrices in ResistanceGA (Peterman 2018), analysed as potential predictors of Columbus-area (n=51) genetic variation: a) slope, b) development, c) income, d) canopy, e) sand. Raster values were standardized to the same range. Raster spatial projections were NAD27 / UTM zone 17N, meters, with 30x30m cells (JPG 642 KB)

10530_2022_2921_MOESM7_ESM.jpg

Fig. S2. Density plot of the number of genetic markers that differed among all pairs of individuals, examined to detect clones having unique genotypes (multilocus lineages, Arnaud-Haond et al. 2007). Lack of a distinct peak near zero suggested no clones were present in our genetic dataset (JPG 705 KB)

10530_2022_2921_MOESM8_ESM.png

Fig. S3. Plots of top two principal coordinates from principal coordinates analyses (PCoA), which qualitatively assess how PCo clusters correspond to regions and STRUCTURE clusters. Axis labels list variation explained (%) by a PCo. Point labels are region abbreviations: Central Columbus (CCOL), East Columbus (ECOL), Cincinnati (CIN), Cleveland (CLE). Colors denote STRUCTURE clusters, with color gradations corresponding to individual assignment probabilities. a) All data (n=64) with K=2; b) Columbus samples (n=51) with K=2; c) all data (n=64) with K=3 (PNG 898 KB)

10530_2022_2921_MOESM9_ESM.jpg

Fig. S4. Single surface optimizations (ResistanceGA::SS_optim, Peterman 2018) describing the shape of the relationship of resistance to raster values (Fig. S1) for a) slope, b) development, c) income, d) canopy, and e) sand. Raster values were standardized to the same range prior to optimization. Response curves were estimated for continuous predictors, and the histograms visualize the distributions of original raster values relative to distributions of the estimated resistance values. For the categorical predictor (b), resistance was optimized for each category. Resistance is interpreted such that relatively higher values indicate barriers to gene flow, while lower values indicate conductors of gene flow (JPG 587 KB)

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Mattingly, K.Z., Day, C.T.C., Rauschert, E.S.J. et al. Genetic and morphological comparisons of lesser celandine (Ficaria verna) invasions suggest regionally widespread sexual reproduction. Biol Invasions 25, 379–397 (2023). https://doi.org/10.1007/s10530-022-02921-4

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