Individual genotypes from environmental DNA: Fingerprinting snow tracks of three large carnivore species.

eDNA-based population studies high-throughput STR genotyping by sequencing individual identification large carnivores non-invasive genetics snow track sampling

Journal

Molecular ecology resources
ISSN: 1755-0998
Titre abrégé: Mol Ecol Resour
Pays: England
ID NLM: 101465604

Informations de publication

Date de publication:
15 Dec 2023
Historique:
revised: 24 11 2023
received: 28 05 2023
accepted: 30 11 2023
medline: 15 12 2023
pubmed: 15 12 2023
entrez: 15 12 2023
Statut: aheadofprint

Résumé

Continued advancements in environmental DNA (eDNA) research have made it possible to access intraspecific variation from eDNA samples, opening new opportunities to expand non-invasive genetic studies of wildlife populations. However, the use of eDNA samples for individual genotyping, as typically performed in non-invasive genetics, still remains elusive. We present successful individual genotyping of eDNA obtained from snow tracks of three large carnivores: brown bear (Ursus arctos), European lynx (Lynx lynx) and wolf (Canis lupus). DNA was extracted using a protocol for isolating water eDNA and genotyped using amplicon sequencing of short tandem repeats (STR), and for brown bear a sex marker, on a high-throughput sequencing platform. Individual genotypes were obtained for all species, but genotyping performance differed among samples and species. The proportion of samples genotyped to individuals was higher for brown bear (5/7) and wolf (7/10) than for lynx (4/9), and locus genotyping success was greater for brown bear (0.88). The sex marker was typed in six out of seven brown bear samples. Results for three species show that reliable individual genotyping, including sex identification, is now possible from eDNA in snow tracks, underlining its vast potential to complement the non-invasive genetic methods used for wildlife. To fully leverage the application of snow track eDNA, improved understanding of the ideal species- and site-specific sampling conditions, as well as laboratory methods promoting genotyping success, is needed. This will also inform efforts to retrieve and type nuclear DNA from other eDNA samples, thereby advancing eDNA-based individual and population-level studies.

Identifiants

pubmed: 38099394
doi: 10.1111/1755-0998.13915
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e13915

Subventions

Organisme : European Commission
ID : LIFE16 NAT/SI/000634
Organisme : European Commission
ID : LIFE18 NAT/IT/000972
Organisme : Javna Agencija za Raziskovalno Dejavnost RS
ID : P1-0184
Organisme : Swiss Federal Office for the Environment (FOEN)

Informations de copyright

© 2023 The Authors. Molecular Ecology Resources published by John Wiley & Sons Ltd.

Références

Adams, C. I. M., Knapp, M., Gemmell, N. J., Jeunen, G.-J., Bunce, M., Lamare, M. D., & Taylor, H. R. (2019). Beyond biodiversity: Can environmental DNA (eDNA) cut it as a population genetics tool? Genes, 10(3), 192. https://doi.org/10.3390/genes10030192
Andres, K. J., Sethi, S. A., Lodge, D. M., & Andrés, J. (2021). Nuclear eDNA estimates population allele frequencies and abundance in experimental mesocosms and field samples. Molecular Ecology, 30(3), 685-697. https://doi.org/10.1111/mec.15765
Andrews, K. R., De Barba, M., Russello, M. A., & Waits, L. P. (2018). Advances in using non-invasive, archival, and environmental samples for population genomic studies. In P. A. Hohenlohe & O. P. Rajora (Eds.), Population genomics: Wildlife (pp. 63-99). Springer International Publishing. https://doi.org/10.1007/13836_2018_45
Barber-Meyer, S. M., Dysthe, J. C., & Pilgrim, K. L. (2020). Testing environmental DNA from wolf snow tracks for species, sex, and individual identification. Canadian Wildlife Biology and Management, 9(1), 12-20.
Barber-Meyer, S. M., Zeller, V., & Pilgrim, K. L. (2022). Testing environmental DNA from wolf snow tracks for species, sex, and individual identification - An addendum. Canadian Wildlife Biology and Management, 11(1), 12-14.
Barnes, M. A., & Turner, C. R. (2016). The ecology of environmental DNA and implications for conservation genetics. Conservation Genetics, 17(1), 1-17. https://doi.org/10.1007/s10592-015-0775-4
Beng, K. C., & Corlett, R. T. (2020). Applications of environmental DNA (eDNA) in ecology and conservation: Opportunities, challenges and prospects. Biodiversity and Conservation, 29(7), 2089-2121. https://doi.org/10.1007/s10531-020-01980-0
Boyer, F., Mercier, C., Bonin, A., Le Bras, Y., Taberlet, P., & Coissac, E. (2016). Obitools: A unix-inspired software package for DNA metabarcoding. Molecular Ecology Resources, 16(1), 176-182.
Broquet, T., & Petit, E. (2004). Quantifying genotyping errors in noninvasive population genetics. Molecular Ecology, 13(11), 3601-3608.
Carøe, C., & Bohmann, K. (2020). Tagsteady: A metabarcoding library preparation protocol to avoid false assignment of sequences to samples. Molecular Ecology Resources, 20(6), 1620-1631. https://doi.org/10.1111/1755-0998.13227
Coissac, E. (2012). OligoTag: A program for designing sets of tags for next-generation sequencing of multiplexed samples. In F. Pompanon & A. Bonin (Eds.), Data production and analysis in population genomics (pp. 13-31). Humana Press.
Cristescu, M. E., & Hebert, P. D. N. (2018). Uses and misuses of environmental DNA in biodiversity science and conservation. Annual Review of Ecology, Evolution, and Systematics, 49(1), 209-230. https://doi.org/10.1146/annurev-ecolsys-110617-062306
Dalén, L., Götherström, A., Meijer, T., & Shapiro, B. (2007). Recovery of DNA from footprints in the snow. The Canadian Field-Naturalist, 121(3), 321-324. https://doi.org/10.22621/cfn.v121i3.482
De Barba, M., Miquel, C., Boyer, F., Mercier, C., Rioux, D., Coissac, E., & Taberlet, P. (2014). DNA metabarcoding multiplexing and validation of data accuracy for diet assessment: Application to omnivorous diet. Molecular Ecology Resources, 14(2), 306-323. https://doi.org/10.1111/1755-0998.12188
De Barba, M., Miquel, C., Lobréaux, S., Quenette, P. Y., Swenson, J. E., & Taberlet, P. (2017). High-throughput microsatellite genotyping in ecology: Improved accuracy, efficiency, standardization and success with low-quantity and degraded DNA. Molecular Ecology Resources, 17(3), 492-507. https://doi.org/10.1111/1755-0998.12594
De Barba, M., & Waits, L. P. (2010). Multiplex pre-amplification for noninvasive genetic sampling: Is the extra effort worth it? Molecular Ecology Resources, 10, 659-665. https://doi.org/10.1111/j.1755-0998.2009.02818.x
Deiner, K., Bik, H. M., Mächler, E., Seymour, M., Lacoursière-Roussel, A., Altermatt, F., Creer, S., Bista, I., Lodge, D. M., de Vere, N., Pfrender, M. E., & Bernatchez, L. (2017). Environmental DNA metabarcoding: Transforming how we survey animal and plant communities. Molecular Ecology, 26(21), 5872-5895. https://doi.org/10.1111/mec.14350
Deiner, K., Yamanaka, H., & Bernatchez, L. (2021). The future of biodiversity monitoring and conservation utilizing environmental DNA. Environmental DNA, 3(1), 3-7.
Dufresnes, C., Remollino, N., Stoffel, C., Manz, R., Weber, J.-M., & Fumagalli, L. (2019). Two decades of non-invasive genetic monitoring of the grey wolves recolonizing the Alps support very limited dog introgression. Scientific Reports, 9(1), 148. https://doi.org/10.1038/s41598-018-37331-x
Dugal, L., Thomas, L., Jensen, M. R., Sigsgaard, E. E., Simpson, T., Jarman, S., Thomsen, P. F., & Meekan, M. (2022). Individual haplotyping of whale sharks from seawater environmental DNA. Molecular Ecology Resources, 22(1), 56-65. https://doi.org/10.1111/1755-0998.13451
Farrell, J. A., Whitmore, L., Mashkour, N., Rollinson Ramia, D. R., Thomas, R. S., Eastman, C. B., Burkhalter, B., Yetsko, K., Mott, C., Wood, L., Zirkelbach, B., Meers, L., Kleinsasser, P., Stock, S., Libert, E., Herren, R., Eastman, S., Crowder, W., Bovery, C., … Duffy, D. J. (2022). Detection and population genomics of sea turtle species via noninvasive environmental DNA analysis of nesting beach sand tracks and oceanic water. Molecular Ecology Resources, 22(7), 2471-2493. https://doi.org/10.1111/1755-0998.13617
Fordyce, S. L., Ávila-Arcos, M. C., Rockenbauer, E., Børsting, C., Frank-Hansen, R., Petersen, F. T., Willerslev, E., Hansen, A. J., Morling, N., & Gilbert, M. T. P. (2011). High-throughput sequencing of core STR loci for forensic genetic investigations using the Roche Genome Sequencer FLX platform. BioTechniques, 51(2), 127-133.
Fordyce, S. L., Mogensen, H. S., Børsting, C., Lagacé, R. E., Chang, C.-W., Rajagopalan, N., & Morling, N. (2015). Second-generation sequencing of forensic STRs using the Ion Torrent™ HID STR 10-plex and the Ion PGM™. Forensic Science International: Genetics, 14, 132-140. https://doi.org/10.1016/j.fsigen.2014.09.020
Franklin, T. W., McKelvey, K. S., Golding, J. D., Mason, D. H., Dysthe, J. C., Pilgrim, K. L., Squires, J. R., Aubry, K. B., Long, R. A., Greaves, S. E., Raley, C. M., Jackson, S., MacKay, P., Lisbon, J., Sauder, J. D., Pruss, M. T., Heffington, D., & Schwartz, M. K. (2019). Using environmental DNA methods to improve winter surveys for rare carnivores: DNA from snow and improved noninvasive techniques. Biological Conservation, 229, 50-58. https://doi.org/10.1016/j.biocon.2018.11.006
Hellström, M., Wijkmark, N., Edbom-Blomstrand, C., Hellström, P., & Näslund, J. (2019). Footsteps in the snow-Pilot study for future monitoring of individual lynx (Lynx lynx) from eDNA in snow tracks. AquaBiota Report, 10, 1-16.
Howell, L., LaRue, M., & Flanagan, S. P. (2021). Environmental DNA as a tool for monitoring Antarctic vertebrates. New Zealand Journal of Zoology, 48(3-4), 245-262. https://doi.org/10.1080/03014223.2021.1900299
Jensen, M. R., Sigsgaard, E. E., Liu, S., Manica, A., Bach, S. S., Hansen, M. M., Møller, P. R., & Thomsen, P. F. (2021). Genome-scale target capture of mitochondrial and nuclear environmental DNA from water samples. Molecular Ecology Resources, 21(3), 690-702. https://doi.org/10.1111/1755-0998.13293
Kelly, M. J., Betsch, J., Wultsch, C., Mesa, B., & Mills, L. S. (2012). Noninvasive sampling for carnivores. In L. Boitani & R. A. Powell (Eds.), Carnivore ecology and conservation: A handbook of techniques (pp. 47-69). Oxford University Press.
Kinoshita, G., Yonezawa, S., Murakami, S., & Isagi, Y. (2019). Environmental DNA collected from snow tracks is useful for identification of mammalian species. Zoological Science, 36(3), 198-207. https://doi.org/10.2108/zs180172
Liberg, O., Aronson, Å., Sand, H., Wabakken, P., Maartmann, E., Svensson, L., & Åkesson, M. (2011). Monitoring of wolves in Scandinavia. Hystrix, 23(1), 29-34. https://doi.org/10.4404/hystrix-23.1-4670
Miquel, C., Bellemain, E., Poillot, C., Bessiere, J., Durand, A., & Taberlet, P. (2006). Quality indexes to assess the reliability of genotypes in studies using noninvasive sampling and multiple tube approach. Molecular Ecology Notes, 6(4), 985-988.
Mumma, M. A., Zieminski, C., Fuller, T. K., Mahoney, S. P., & Waits, L. P. (2015). Evaluating noninvasive genetic sampling techniques to estimate large carnivore abundance. Molecular Ecology Resources, 15(5), 1133-1144. https://doi.org/10.1111/1755-0998.12390
Ogden, R., Dawnay, N., & McEwing, R. (2009). Wildlife DNA forensics-Bridging the gap between conservation genetics and law. Endangered Species Research, 9, 179-195.
Paetkau, D. (2003). An empirical exploration of data quality in DNA-based population inventories. Molecular Ecology, 12, 1375-1387.
Pagès, M., Maudet, C., Bellemain, E., Taberlet, P., Hughes, S., & Hänni, C. (2009). A system for sex determination from degraded DNA: A useful tool for palaeogenetics and conservation genetics of ursids. Conservation Genetics, 10(4), 897-907.
Parsons, K. M., Everett, M., Dahlheim, M., & Park, L. (2018). Water, water everywhere: Environmental DNA can unlock population structure in elusive marine species. Royal Society Open Science, 5(8), 180537. https://doi.org/10.1098/rsos.180537
Rodgers, T. W., & Janečka, J. E. (2013). Applications and techniques for non-invasive faecal genetics research in felid conservation. European Journal of Wildlife Research, 59(1), 1-16. https://doi.org/10.1007/s10344-012-0675-6
Schnell, I. B., Bohmann, K., & Gilbert, M. T. P. (2015). Tag jumps illuminated - Reducing sequence-to-sample misidentifications in metabarcoding studies. Molecular Ecology Resources, 15(6), 1289-1303. https://doi.org/10.1111/1755-0998.12402
Schwartz, M. K., Luikart, G., & Waples, R. S. (2007). Genetic monitoring as a promising tool for conservation and management. Trends in Ecology & Evolution, 22(1), 25-33.
Sergiel, A., Naves, J., Kujawski, P., Maślak, R., Serwa, E., Ramos, D., Fernández-Gil, A., Revilla, E., Zwijacz-Kozica, T., Zięba, F., Painer, J., & Selva, N. (2017). Histological, chemical and behavioural evidence of pedal communication in brown bears. Scientific Reports, 7(1), 1052. https://doi.org/10.1038/s41598-017-01136-1
Sigsgaard, E. E., Jensen, M. R., Winkelmann, I. E., Møller, P. R., Hansen, M. M., & Thomsen, P. F. (2020). Population-level inferences from environmental DNA-Current status and future perspectives. Evolutionary Applications, 13(2), 245-262. https://doi.org/10.1111/eva.12882
Sigsgaard, E. E., Nielsen, I. B., Bach, S. S., Lorenzen, E. D., Robinson, D. P., Knudsen, S. W., Pedersen, M. W., Jaidah, M. A., Orlando, L., Willerslev, E., Møller, P. R., & Thomsen, P. F. (2016). Population characteristics of a large whale shark aggregation inferred from seawater environmental DNA. Nature Ecology & Evolution, 1, 0004. https://doi.org/10.1038/s41559-016-0004
Sindičić, M., Polanc, P., Gomerčić, T., Jelenčič, M., Huber, Đ., Trontelj, P., & Skrbinšek, T. (2013). Genetic data confirm critical status of the reintroduced Dinaric population of Eurasian lynx. Conservation Genetics, 14(5), 1009-1018. https://doi.org/10.1007/s10592-013-0491-x
Skrbinšek, T., Luštrik, R., Majić-Skrbinšek, A., Potočnik, H., Kljun, F., Jelenčič, M., Kos, I., & Trontelj, P. (2019). From science to practice: Genetic estimate of brown bear population size in Slovenia and how it influenced bear management. European Journal of Wildlife Research, 65(2), 29. https://doi.org/10.1007/s10344-019-1265-7
Székely, D., Corfixen, N. L., Mørch, L. L., Knudsen, S. W., McCarthy, M. L., Teilmann, J., Heide-Jørgensen, M. P., & Olsen, M. T. (2021). Environmental DNA captures the genetic diversity of bowhead whales (Balaena mysticetus) in West Greenland. Environmental DNA, 3(1), 248-260. https://doi.org/10.1002/edn3.176
Taberlet, P., Bonin, A., Zinger, L., & Coissac, E. (2018). Environmental DNA: For biodiversity research and monitoring. Oxford University Press.
Taberlet, P., Coissac, E., Hajibabaei, M., & Rieseberg, L. H. (2012). Environmental DNA. Molecular Ecology, 21(8), 1789-1793. https://doi.org/10.1111/j.1365-294X.2012.05542.x
Taberlet, P., Griffin, S., Goossens, B., Questiau, S., Manceau, V., Escaravage, N., Waits, L., & Bouvet, J. (1996). Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Research, 24(16), 3189-3194.
Von Duyke, A. L., Crawford, J. A., Quakenbush, L., Adams, J. R., & Waits, L. P. (2023). Determination of polar bear (Ursus maritimus) individual genotype and sex based on DNA extracted from paw-prints in snow. Frontiers in Conservation Science, 4, 1166279. https://doi.org/10.3389/fcosc.2023.1166279
Waits, L. P., & Paetkau, D. (2005). Noninvasive genetic sampling tools for wildlife biologists: A review of applications and recommendations for accurate data collection. Journal of Wildlife Management, 69(4), 1419-1433. https://doi.org/10.2193/0022-541X(2005)69[1419:NGSTFW]2.0.CO;2
Wilcox, T. M., & Jensen, M. R. (2022). Drawing a line in the sand: Environmental DNA population genomics. Molecular Ecology Resources, 22, 2455-2457. https://doi.org/10.1111/1755-0998.13686
Zinger, L., Bonin, A., Alsos, I. G., Bálint, M., Bik, H., Boyer, F., Chariton, A. A., Creer, S., Coissac, E., Deagle, B. E., Barba, M. D., Dickie, I. A., Dumbrell, A. J., Ficetola, G. F., Fierer, N., Fumagalli, L., Gilbert, M. T. P., Jarman, S., Jumpponen, A., … Taberlet, P. (2019). DNA metabarcoding-Need for robust experimental designs to draw sound ecological conclusions. Molecular Ecology, 28(8), 1857-1862. https://doi.org/10.1111/mec.15060

Auteurs

Marta De Barba (M)

Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.
DivjaLabs Ltd., Ljubljana, Slovenia.

Molly Baur (M)

Laboratory for Conservation Biology, Department of Ecology and Evolution, Biophore, University of Lausanne, Lausanne, Switzerland.

Frédéric Boyer (F)

Université Grenoble Alpes, Université Savoie Mont Blanc, CNRS, LECA, Laboratoire d'Ecologie Alpine, Grenoble, France.

Luca Fumagalli (L)

Laboratory for Conservation Biology, Department of Ecology and Evolution, Biophore, University of Lausanne, Lausanne, Switzerland.
University Center of Legal Medicine Lausanne and Geneva, Lausanne University Hospital (CHUV) and University of Lausanne, Lausanne, Switzerland.

Marjeta Konec (M)

Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.
DivjaLabs Ltd., Ljubljana, Slovenia.

Christian Miquel (C)

Université Grenoble Alpes, Université Savoie Mont Blanc, CNRS, LECA, Laboratoire d'Ecologie Alpine, Grenoble, France.

Elena Pazhenkova (E)

Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.

Nadège Remollino (N)

Laboratory for Conservation Biology, Department of Ecology and Evolution, Biophore, University of Lausanne, Lausanne, Switzerland.

Tomaž Skrbinšek (T)

Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.
DivjaLabs Ltd., Ljubljana, Slovenia.

Céline Stoffel (C)

Laboratory for Conservation Biology, Department of Ecology and Evolution, Biophore, University of Lausanne, Lausanne, Switzerland.

Pierre Taberlet (P)

Université Grenoble Alpes, Université Savoie Mont Blanc, CNRS, LECA, Laboratoire d'Ecologie Alpine, Grenoble, France.
UiT - The Arctic University of Norway, Tromsø Museum, Tromsø, Norway.

Classifications MeSH