Population genomics of the muskox' resilience in the near absence of genetic variation.
ancient DNA
genetic diversity
genetic load
inbreeding
muskox
population genomics
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
16 Nov 2023
16 Nov 2023
Historique:
revised:
07
10
2023
received:
23
06
2023
accepted:
01
11
2023
medline:
17
11
2023
pubmed:
17
11
2023
entrez:
16
11
2023
Statut:
aheadofprint
Résumé
Genomic studies of species threatened by extinction are providing crucial information about evolutionary mechanisms and genetic consequences of population declines and bottlenecks. However, to understand how species avoid the extinction vortex, insights can be drawn by studying species that thrive despite past declines. Here, we studied the population genomics of the muskox (Ovibos moschatus), an Ice Age relict that was at the brink of extinction for thousands of years at the end of the Pleistocene yet appears to be thriving today. We analysed 108 whole genomes, including present-day individuals representing the current native range of both muskox subspecies, the white-faced and the barren-ground muskox (O. moschatus wardi and O. moschatus moschatus) and a ~21,000-year-old ancient individual from Siberia. We found that the muskox' demographic history was profoundly shaped by past climate changes and post-glacial re-colonizations. In particular, the white-faced muskox has the lowest genome-wide heterozygosity recorded in an ungulate. Yet, there is no evidence of inbreeding depression in native muskox populations. We hypothesize that this can be explained by the effect of long-term gradual population declines that allowed for purging of strongly deleterious mutations. This study provides insights into how species with a history of population bottlenecks, small population sizes and low genetic diversity survive against all odds.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Carlsbergfondet
ID : CF20-0539
Organisme : Danmarks Frie Forskningsfond
ID : 8021-00344B
Informations de copyright
© 2023 John Wiley & Sons Ltd.
Références
Abascal, F., Corvelo, A., Cruz, F., Villanueva-Cañas, J. L., Vlasova, A., Marcet-Houben, M., Martínez-Cruz, B., Cheng, J. Y., Prieto, P., Quesada, V., Quilez, J., Li, G., García, F., Rubio-Camarillo, M., Frias, L., Ribeca, P., Capella-Gutiérrez, S., Rodríguez, J. M., Câmara, F., … Godoy, J. A. (2016). Extreme genomic erosion after recurrent demographic bottlenecks in the highly endangered Iberian lynx. Genome Biology, 17(1), 251.
Andrews, S. (2010). FastQC: a quality control tool for high throughput sequence data (Version 0.10.1) [Computer software]. https://www.bioinformatics.babraham.ac.uk/projects/fastqc/
Atwood, T. B., Valentine, S. A., Hammill, E., McCauley, D. J., Madin, E. M. P., Beard, K. H., & Pearse, W. D. (2020). Herbivores at the highest risk of extinction among mammals, birds, and reptiles. Science Advances, 6(32), eabb8458.
Bandelt, H. J., Forster, P., & Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16(1), 37-48.
Barr, W. (1991). The commercial trade in muskox hides in the Northwest Territories 1860-1916. Rangifer, 11(2), 81-82.
Bennike, O., & Andreasen, C. (2005). Radiocarbon dating of musk-ox (Ovibos moschatus) remains from northeast Greenland. The Polar Record, 41(219), 305-310.
Bertorelle, G., Raffini, F., Bosse, M., Bortoluzzi, C., Iannucci, A., Trucchi, E., Morales, H. E., & van Oosterhout, C. (2022). Genetic load: Genomic estimates and applications in non-model animals. Nature Reviews. Genetics, 23(8), 492-503.
Boitard, S., Rodríguez, W., Jay, F., Mona, S., & Austerlitz, F. (2016). Inferring population size history from large samples of genome-wide molecular data - an approximate Bayesian computation approach. PLoS Genetics, 12(3), e1005877.
Bouckaert, R., Vaughan, T. G., Barido-Sottani, J., Duchêne, S., Fourment, M., Gavryushkina, A., Heled, J., Jones, G., Kühnert, D., De Maio, N., Matschiner, M., Mendes, F. K., Müller, N. F., Ogilvie, H. A., du Plessis, L., Popinga, A., Rambaut, A., Rasmussen, D., Siveroni, I., … Drummond, A. J. (2019). BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology, 15(4), e1006650.
Brace, S., Palkopoulou, E., Dalén, L., Lister, A. M., Miller, R., Otte, M., Germonpré, M., Blockley, S. P. E., Stewart, J. R., & Barnes, I. (2012). Serial population extinctions in a small mammal indicate Late Pleistocene ecosystem instability. Proceedings of the National Academy of Sciences of the United States of America, 109(50), 20532-20536.
Buffalo, V. (2021). Quantifying the relationship between genetic diversity and population size suggests natural selection cannot explain Lewontin's Paradox. eLife, 10, e67509. https://doi.org/10.7554/eLife.67509
Busing, F. M. T. A., Meijer, E., & Leeden, R. V. D. (1999). Delete-m jackknife for unequal m. Statistics and Computing, 9(1), 3-8.
Campos, P. F., Willerslev, E., Sher, A., Orlando, L., Axelsson, E., Tikhonov, A., Aaris-Sørensen, K., Greenwood, A. D., Kahlke, R.-D., Kosintsev, P., Krakhmalnaya, T., Kuznetsova, T., Lemey, P., MacPhee, R., Norris, C. A., Shepherd, K., Suchard, M. A., Zazula, G. D., Shapiro, B., & Gilbert, M. T. P. (2010). Ancient DNA analyses exclude humans as the driving force behind late Pleistocene musk ox (Ovibos moschatus) population dynamics. Proceedings of the National Academy of Sciences of the United States of America, 107(12), 5675-5680.
Canteri, E., Brown, S. C., Schmidt, N. M., Heller, R., Nogués-Bravo, D., & Fordham, D. A. (2022). Spatiotemporal influences of climate and humans on muskox range dynamics over multiple millennia. Global Change Biology, 28(22), 6602-6617.
Caughley, G. (1994). Directions in conservation biology. The Journal of Animal Ecology, 63(2), 215-244.
Chang, C. C., Chow, C. C., Tellier, L. C., Vattikuti, S., Purcell, S. M., & Lee, J. J. (2015). Second-generation PLINK: Rising to the challenge of larger and richer datasets. GigaScience, 4(1), 7. https://doi.org/10.1186/s13742-015-0047-8
Cho, Y. S., Hu, L., Hou, H., Lee, H., Xu, J., Kwon, S., Oh, S., Kim, H.-M., Jho, S., Kim, S., Shin, Y.-A., Kim, B. C., Kim, H., Kim, C.-U., Luo, S.-J., Johnson, W. E., Koepfli, K.-P., Schmidt-Küntzel, A., Turner, J. A., … Bhak, J. (2013). The tiger genome and comparative analysis with lion and snow leopard genomes. Nature Communications, 4, 2433.
Cingolani, P., Platts, A., Wang, L. L., Coon, M., Nguyen, T., Wang, L., Land, S. J., Lu, X., & Ruden, D. M. (2012). A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly, 6(2), 80-92.
Colella, J. P., Lan, T., Schuster, S. C., Talbot, S. L., Cook, J. A., & Lindqvist, C. (2018). Whole-genome analysis of Mustela erminea finds that pulsed hybridization impacts evolution at high latitudes. Communications Biology, 1, 51.
Cuyler, C., Rowell, J., Adamczewski, J., Anderson, M., Blake, J., Bretten, T., Brodeur, V., Campbell, M., Checkley, S. L., Cluff, H. D., Côté, S. D., Davison, T., Dumond, M., Ford, B., Gruzdev, A., Gunn, A., Jones, P., Kutz, S., Leclerc, L.-M., … Ytrehus, B. (2020). Muskox status, recent variation, and uncertain future. Ambio, 49(3), 805-819.
Dalén, L., Fuglei, E., Hersteinsson, P., Kapel, C. M. O., Roth, J. D., Samelius, G., Tannerfeldt, M., & Angerbjörn, A. (2005). Population history and genetic structure of a circumpolar species: The arctic fox. Biological Journal of the Linnean Society, 84(1), 79-89.
Darriba, D., Posada, D., Kozlov, A. M., Stamatakis, A., Morel, B., & Flouri, T. (2020). ModelTest-NG: A new and scalable tool for the selection of DNA and protein evolutionary models. Molecular Biology and Evolution, 37(1), 291-294.
Davydov, E. V., Goode, D. L., Sirota, M., Cooper, G. M., Sidow, A., & Batzoglou, S. (2010). Identifying a high fraction of the human genome to be under selective constraint using GERP. PLoS Computational Biology, 6(12), e1001025. https://doi.org/10.1371/journal.pcbi.1001025
Derrien, T., Estellé, J., Marco Sola, S., Knowles, D. G., Raineri, E., Guigó, R., & Ribeca, P. (2012). Fast computation and applications of genome mappability. PLoS One, 7(1), e30377.
Desforges, J.-P., Marques, G. M., Beumer, L. T., Chimienti, M., Hansen, L. H., Pedersen, S. H., Schmidt, N. M., & van Beest, F. M. (2021). Environment and physiology shape Arctic ungulate population dynamics. Global Change Biology, 27(9), 1755-1771.
Díez-del-Molino, D., Sánchez-Barreiro, F., Barnes, I., Gilbert, M. T. P., & Dalén, L. (2018). Quantifying temporal genomic erosion in endangered species. Trends in Ecology & Evolution, 33(3), 176-185.
Durand, E. Y., Patterson, N., Reich, D., & Slatkin, M. (2011). Testing for ancient admixture between closely related populations. Molecular Biology and Evolution, 28(8), 2239-2252.
Dussex, N., van der Valk, T., Morales, H. E., Wheat, C. W., Díez-del-Molino, D., von Seth, J., Foster, Y., Kutschera, V. E., Guschanski, K., Rhie, A., Phillippy, A. M., Korlach, J., Howe, K., Chow, W., Pelan, S., Mendes Damas, J. D., Lewin, H. A., Hastie, A. R., Formenti, G., … Dalén, L. (2021). Population genomics of the critically endangered kākāpō. Cell Genomics, 1(1), 100002.
Ewels, P., Magnusson, M., Lundin, S., & Käller, M. (2016). MultiQC: Summarize analysis results for multiple tools and samples in a single report. Bioinformatics, 32(19), 3047-3048.
Falk, J. M., Schmidt, N. M., Christensen, T. R., & Ström, L. (2015). Large herbivore grazing affects the vegetation structure and greenhouse gas balance in a high arctic mire. Environmental Research Letters, 10(4), 45001.
Fedorov, V. B., & Stenseth, N. C. (2002). Multiple glacial refugia in the North American Arctic: Inference from phylogeography of the collared lemming (Dicrostonyx groenlandicus). Proceedings of the Royal Society of London. Series B: Biological Sciences, 269(1505), 2071-2077.
Flynn, J. M., Hubley, R., Goubert, C., Rosen, J., Clark, A. G., Feschotte, C., & Smit, A. F. (2020). RepeatModeler2 for automated genomic discovery of transposable element families. Proceedings of the National Academy of Sciences of the United States of America, 117(17), 9451-9457.
Foote, A. D., Alexander, A., Ballance, L. T., Constantine, R., Galletti Vernazzani Muñoz, B., Guinet, C., Robertson, K. M., Sinding, M.-H. S., Sironi, M., Tixier, P., Totterdell, J., Towers, J. R., Wellard, R., Pitman, R. L., & Morin, P. A. (2023). “Type D” killer whale genomes reveal long-term small population size and low genetic diversity. The Journal of Heredity, 114(2), 94-109.
Frankham, R. (1996). Relationship of genetic variation to population size in wildlife. Conservation Biology, 10(6), 1500-1508.
Garcia-Erill, G., & Albrechtsen, A. (2020). Evaluation of model fit of inferred admixture proportions. Molecular Ecology Resources, 20(4), 936-949.
Gelman, A., & Rubin, D. B. (1992). Inference from iterative simulation using multiple sequences. Statistical Science, 7(4), 457-472.
Gooley, R., Hogg, C. J., Belov, K., & Grueber, C. E. (2017). No evidence of inbreeding depression in a Tasmanian devil insurance population despite significant variation in inbreeding. Scientific Reports, 7(1), 1830.
Green, R. E., Krause, J., Briggs, A. W., Maricic, T., Stenzel, U., Kircher, M., Patterson, N., Li, H., Zhai, W., Fritz, M. H.-Y., Hansen, N. F., Durand, E. Y., Malaspinas, A.-S., Jensen, J. D., Marques-Bonet, T., Alkan, C., Prüfer, K., Meyer, M., Burbano, H. A., … Pääbo, S. (2010). A draft sequence of the Neandertal genome. Science, 328(5979), 710-722.
Grossen, C., Guillaume, F., Keller, L. F., & Croll, D. (2020). Purging of highly deleterious mutations through severe bottlenecks in Alpine ibex. Nature Communications, 11, 1001. https://doi.org/10.1038/s41467-020-14803-1
Groves, P. (1997). Intraspecific variation in mitochondrial DNA of muskoxen, based on control-region sequences. Canadian Journal of Zoology, 75(4), 568-575.
Gunn, A., & Forchhammer, M. (2022). Ovibos moschatus.(errata version published in 2016.). The IUCN Red List of Threatened Species 2022.
Hanghøj, K., Moltke, I., Andersen, P. A., Manica, A., & Korneliussen, T. S. (2019). Fast and accurate relatedness estimation from high-throughput sequencing data in the presence of inbreeding. GigaScience, 8(5), giz034. https://doi.org/10.1093/gigascience/giz034
Hansen, C. C. R., Hvilsom, C., Schmidt, N. M., Aastrup, P., Van Coeverden de Groot, P. J., Siegismund, H. R., & Heller, R. (2018). The muskox lost a substantial part of its genetic diversity on its long road to Greenland. Current Biology, 28(24), 4022-4028.e5.
Harington, C. R. (1961). History, distribution and ecology of the muskoxen. https://escholarship.mcgill.ca/concern/theses/s7526c702
Hassanin, A., Ropiquet, A., Couloux, A., & Cruaud, C. (2009). Evolution of the mitochondrial genome in mammals living at high altitude: New insights from a study of the tribe Caprini (Bovidae, Antilopinae). Journal of Molecular Evolution, 68(4), 293-310.
Hasselgren, M., Dussex, N., von Seth, J., Angerbjörn, A., Olsen, R.-A., Dalén, L., & Norén, K. (2021). Genomic and fitness consequences of inbreeding in an endangered carnivore. Molecular Ecology, 30(12), 2790-2799.
Jónsson, H., Ginolhac, A., Schubert, M., Johnson, P. L. F., & Orlando, L. (2013). mapDamage2.0: Fast approximate Bayesian estimates of ancient DNA damage parameters. Bioinformatics, 29(13), 1682-1684.
Kafle, P., Peller, P., Massolo, A., Hoberg, E., Leclerc, L.-M., Tomaselli, M., & Kutz, S. (2020). Range expansion of muskox lungworms track rapid arctic warming: Implications for geographic colonization under climate forcing. Scientific Reports, 10(1), 17323. https://doi.org/10.1038/s41598-020-74358-5
Kahlke, R.-D. (2014). The origin of Eurasian mammoth faunas (Mammuthus-Coelodonta Faunal Complex). Quaternary Science Reviews, 96, 32-49.
Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30(4), 772-780.
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., & Drummond, A. (2012). Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28(12), 1647-1649.
Khan, A., Patel, K., Shukla, H., Viswanathan, A., van der Valk, T., Borthakur, U., Nigam, P., Zachariah, A., Jhala, Y. V., Kardos, M., & Ramakrishnan, U. (2021). Genomic evidence for inbreeding depression and purging of deleterious genetic variation in Indian tigers. Proceedings of the National Academy of Sciences of the United States of America, 118(49), e2023018118. https://doi.org/10.1073/pnas.2023018118
Klütsch, C. F. C., Manseau, M., Anderson, M., Sinkins, P., & Wilson, P. J. (2017). Evolutionary reconstruction supports the presence of a Pleistocene Arctic refugium for a large mammal species. Journal of Biogeography, 44(12), 2729-2739.
Knuth, E. (1967). Archaeology of the musk-ox way. École pratique des hautes études, Sorbonne.
Kolokotronis, S.-O., Macphee, R. D. E., & Greenwood, A. D. (2007). Detection of mitochondrial insertions in the nucleus (NuMts) of Pleistocene and modern muskoxen. BMC Evolutionary Biology, 7, 67.
Korneliussen, T. S., Albrechtsen, A., & Nielsen, R. (2014). ANGSD: Analysis of next generation sequencing data. BMC Bioinformatics, 15, 356.
Kutschera, V. E., Kierczak, M., van der Valk, T., von Seth, J., Dussex, N., Lord, E., Dehasque, M., Stanton, D. W. G., Khoonsari, P. E., Nystedt, B., Dalén, L., & Díez-del-Molino, D. (2022). GenErode: A bioinformatics pipeline to investigate genome erosion in endangered and extinct species. bioRxiv. https://doi.org/10.1101/2022.03.04.482637
Kutz, S., Bollinger, T., Branigan, M., Checkley, S., Davison, T., Dumond, M., Elkin, B., Forde, T., Hutchins, W., Niptanatiak, A., & Orsel, K. (2015). Erysipelothrix rhusiopathiae associated with recent widespread muskox mortalities in the Canadian Arctic. The Canadian Veterinary Journal, 56(6), 560-563.
Kutz, S. J. (2004). “Emerging” parasitic infections in arctic ungulates. Integrative and Comparative Biology, 44(2), 109-118.
Kyriazis, C. C., Beichman, A. C., Brzeski, K. E., Hoy, S. R., Peterson, R. O., Vucetich, J. A., Vucetich, L. M., Lohmueller, K. E., & Wayne, R. K. (2022). Genomic underpinnings of population persistence in Isle Royale moose. bioRxiv. https://doi.org/10.1101/2022.04.15.488504
Kyriazis, C. C., Wayne, R. K., & Lohmueller, K. E. (2021). Strongly deleterious mutations are a primary determinant of extinction risk due to inbreeding depression. Evolution Letters, 5(1), 33-47.
Laikre, L., Ryman, N., & Lundh, N. G. (1997). Estimated inbreeding in a small, wild muskox Ovibos moschatus population and its possible effects on population reproduction. Biological Conservation, 79(2), 197-204.
Lande, R. (1993). Risks of population extinction from demographic and environmental stochasticity and random catastrophes. The American Naturalist, 142(6), 911-927.
Leigh, J. W., Bryant, D., & Nakagawa, S. (2015). POPART: Full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6, 1110-1116.
Lent, P. C. (1998). Alaska's indigenous muskoxen: A history. Rangelands, 18(3-4), 133-144.
Li, H. (2011). A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics, 27(21), 2987-2993.
Li, H. (2013). Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv [q-bio.GN]. arXiv. http://arxiv.org/abs/1303.3997
Li, H., & Durbin, R. (2011). Inference of human population history from individual whole-genome sequences. Nature, 475(7357), 493-496.
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., & 1000 Genome Project Data Processing Subgroup. (2009). The sequence alignment/map format and SAMtools. Bioinformatics, 25(16), 2078-2079.
Li, M., Li, X., Wu, Z., Zhang, G., Wang, N., Dou, M., Liu, S., Yang, C., Meng, G., Sun, H., Hvilsom, C., Xie, G., Li, Y., Li, Z.h., Wang, W., Jiang, Y., Heller, R., & Wang, Y. (2023). Convergent molecular evolution of thermogenesis and circadian rhythm in Arctic ruminants. Proceedings of the Royal Society B, 290(1999), 20230538.
Lord, E., Dussex, N., Kierczak, M., Díez-Del-Molino, D., Ryder, O. A., Stanton, D. W. G., Gilbert, M. T. P., Sánchez-Barreiro, F., Zhang, G., Sinding, M.-H. S., Lorenzen, E. D., Willerslev, E., Protopopov, A., Shidlovskiy, F., Fedorov, S., Bocherens, H., Nathan, S. K. S. S., Goossens, B., van der Plicht, J., … Dalén, L. (2020). Pre-extinction demographic stability and genomic signatures of adaptation in the woolly rhinoceros. Current Biology, 30(19), 3871-3879.e7.
Lorenzen, E. D., Nogues-Bravo, D., Orlando, L., Weinstock, J., Binladen, J., Marske, K. A., Ugan, A., Borregaard, M. K., Gilbert, M. T. P., Nielsen, R., Ho, S. Y. W., Goebel, T., Graf, K. E., Byers, D., Stenderup, J. T., Rasmussen, M., Campos, P. F., Leonard, J. A., Koepfli, K.-P., … Willerslev, E. (2011). Species-specific responses of Late Quaternary megafauna to climate and humans. Nature, 479, 359-364.
MacPhee, R. D. E., Tikhonov, A. N., Mol, D., & Greenwood, A. D. (2005). Late Quaternary loss of genetic diversity in muskox (Ovibos). BMC Evolutionary Biology, 5, 49.
Maher, W. J. (1968). Muskox bone of possible Wisconsin age from Banks Island, Northwest Territories. Arctic, 21(4), 260-266.
Maier, R., Flegontov, P., Flegontova, O., Changmai, P., & Reich, D. (2022). On the limits of fitting complex models of population history to genetic data. bioRxiv. https://doi.org/10.1101/2022.05.08.491072
Marshall, C., & Parson, W. (2021). Interpreting NUMTs in forensic genetics: Seeing the forest for the trees. Forensic Science International. Genetics, 53, 102497.
Martin, S. H., & Van Belleghem, S. M. (2017). Exploring evolutionary relationships across the genome using topology weighting. Genetics, 206(1), 429-438.
Mathur, S., & Andrew DeWoody, J. (2021). Genetic load has potential in large populations but is realized in small inbred populations. Evolutionary Applications, 14(6), 1540-1557.
Meisner, J., & Albrechtsen, A. (2018). Inferring population structure and admixture proportions in low-depth NGS data. Genetics, 210(2), 719-731.
Meisner, J., & Albrechtsen, A. (2019). Testing for Hardy-Weinberg equilibrium in structured populations using genotype or low-depth next generation sequencing data. Molecular Ecology Resources, 19(5), 1144-1152.
Meyer, M., & Kircher, M. (2010). Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harbor Protocols, 2010(6), db. prot5448.
Minh, B. Q., Schmidt, H. A., Chernomor, O., Schrempf, D., Woodhams, M. D., von Haeseler, A., & Lanfear, R. (2020). IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution, 37(5), 1530-1534.
Mölder, F., Jablonski, K. P., Letcher, B., Hall, M. B., Tomkins-Tinch, C. H., Sochat, V., Forster, J., Lee, S., Twardziok, S. O., Kanitz, A., Wilm, A., Holtgrewe, M., Rahmann, S., Nahnsen, S., & Köster, J. (2021). Sustainable data analysis with Snakemake. F1000Research, 10, 33.
Mølgaard, H. S. (2002). Overgrown hooves from muskoxen (Ovibos moschatus) of Kangaarsuk (Kap Atholl) Northwest Greenland. Greenland Institute of Natural Resources.
Mooney, J. A., Marsden, C. D., Yohannes, A., Wayne, R. K., & Lohmueller, K. E. (2023). Long-term small population size, deleterious variation, and altitude adaptation in the Ethiopian wolf, a severely endangered canid. Molecular Biology and Evolution, 40(1), msac277.
Morin, P. A., Archer, F. I., Avila, C. D., Balacco, J. R., Bukhman, Y. V., Chow, W., Fedrigo, O., Formenti, G., Fronczek, J. A., Fungtammasan, A., Gulland, F. M. D., Haase, B., Peter Heide-Jorgensen, M., Houck, M. L., Howe, K., Misuraca, A. C., Mountcastle, J., Musser, W., Paez, S., … Jarvis, E. D. (2021). Reference genome and demographic history of the most endangered marine mammal, the vaquita. Molecular Ecology Resources, 21(4), 1008-1020.
Mosbacher, J. B., Kristensen, D. K., Michelsen, A., Stelvig, M., & Schmidt, N. M. (2016). Quantifying muskox plant biomass removal and spatial relocation of nitrogen in a high Arctic tundra ecosystem. Arctic, Antarctic, and Alpine Research, 48(2), 229-240.
Mosbacher, J. B., Michelsen, A., Stelvig, M., Hjermstad-Sollerud, H., & Schmidt, N. M. (2019). Muskoxen modify plant abundance, phenology, and nitrogen dynamics in a high arctic fen. Ecosystems, 22(5), 1095-1107.
Nielsen, R., Korneliussen, T., Albrechtsen, A., Li, Y., & Wang, J. (2012). SNP calling, genotype calling, and sample allele frequency estimation from New-Generation Sequencing data. PLoS One, 7(7), e37558.
Nursyifa, C., Brüniche-Olsen, A., Garcia-Erill, G., Heller, R., & Albrechtsen, A. (2022). Joint identification of sex and sex-linked scaffolds in non-model organisms using low depth sequencing data. Molecular Ecology Resources, 22(2), 458-467.
Olesen, C. R. (1993). Rapid population increase in an introduced muskox population, West Greenland. Rangelands, 13(1), 27-32.
Orlando, L., Ginolhac, A., Zhang, G., Froese, D., Albrechtsen, A., Stiller, M., Schubert, M., Cappellini, E., Petersen, B., Moltke, I., Johnson, P. L. F., Fumagalli, M., Vilstrup, J. T., Raghavan, M., Korneliussen, T., Malaspinas, A.-S., Vogt, J., Szklarczyk, D., Kelstrup, C. D., … Willerslev, E. (2013). Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature, 499(7456), 74-78.
Palkopoulou, E., Mallick, S., Skoglund, P., Enk, J., Rohland, N., Li, H., Omrak, A., Vartanyan, S., Poinar, H., Götherström, A., Reich, D., & Dalén, L. (2015). Complete genomes reveal signatures of demographic and genetic declines in the woolly mammoth. Current Biology, 25(10), 1395-1400.
Paradis, E., & Schliep, K. (2019). ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics, 35(3), 526-528.
Patterson, N., Moorjani, P., Luo, Y., Mallick, S., Rohland, N., Zhan, Y., Genschoreck, T., Webster, T., & Reich, D. (2012). Ancient admixture in human history. Genetics, 192(3), 1065-1093.
Pečnerová, P., Díez-Del-Molino, D., Dussex, N., Feuerborn, T., von Seth, J., van der Plicht, J., Nikolskiy, P., Tikhonov, A., Vartanyan, S., & Dalén, L. (2017). Genome-based sexing provides clues about behavior and social structure in the woolly mammoth. Current Biology, 27(22), 3505-3510.e3.
Pečnerová, P., Díez-Del-Molino, D., Vartanyan, S., & Dalén, L. (2016). Changes in variation at the MHC class II DQA locus during the final demise of the woolly mammoth. Scientific Reports, 6, 25274.
Pečnerová, P., Garcia-Erill, G., Liu, X., Nursyifa, C., Waples, R. K., Santander, C. G., Quinn, L., Frandsen, P., Meisner, J., Staeger, F. F., Rasmussen, M. S., Brüniche-Olsen, A., Hviid Friis Jørgensen, C., da Fonseca, R. R., Siegismund, H. R., Albrechtsen, A., Heller, R., Moltke, I., & Hanghøj, K. (2021). High genetic diversity and low differentiation reflect the ecological versatility of the African leopard. Current Biology, 31(9), 1862-1871.e5.
Pečnerová, P., Palkopoulou, E., Wheat, C. W., Skoglund, P., Vartanyan, S., Tikhonov, A., Nikolskiy, P., van der Plicht, J., Díez-Del-Molino, D., & Dalén, L. (2017). Mitogenome evolution in the last surviving woolly mammoth population reveals neutral and functional consequences of small population size. Evolution Letters, 1(6), 292-303.
Pedersen, C. B., & Aastrup, P. (2000). Muskoxen in Angujaartorfiup Nunaat, West Greenland: Monitoring, population growth, and sustainable harvest. Arctic, 53(6), 18-26.
Petkova, D., Novembre, J., & Stephens, M. (2016). Visualizing spatial population structure with estimated effective migration surfaces. Nature Genetics, 48(1), 94-100.
Pickrell, J. K., & Pritchard, J. K. (2012). Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genetics, 8(11), e1002967.
Pimm, S. L., & Raven, P. (2000). Biodiversity. Extinction by numbers [Review of Biodiversity. Extinction by numbers]. Nature, 403(6772), 843-845.
Plummer, M., Best, N., Cowles, K., & Vines, K. (2006). CODA: Convergence diagnosis and output analysis for MCMC. R News, 6(1), 7-11.
Powers, R. P., & Jetz, W. (2019). Global habitat loss and extinction risk of terrestrial vertebrates under future land-use-change scenarios. Nature Climate Change, 9(4), 323-329.
Prewer, E., Kutz, S., Leclerc, L. M., & Kyle, C. J. (2020). Already at the bottom? Demographic declines are unlikely further to undermine genetic diversity of a large Arctic ungulate: Muskox, Ovibos moschatus (Artiodactyla: Bovidae). Biological Journal of the Linnean Society, 129(2), 459-469.
Primmer, C. R. (2009). From conservation genetics to conservation genomics. Annals of the New York Academy of Sciences, 1162, 357-368.
Purcell, S., & Chang, C. (2015). PLINK 1.9. www.cog-genomics.org/plink/1.9/
Purvis, A., Gittleman, J. L., Cowlishaw, G., & Mace, G. M. (2000). Predicting extinction risk in declining species. Proceedings. Biological Sciences/The Royal Society, 267(1456), 1947-1952.
R Core Team. (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/
Rambaut, A. (2014). FigTree: Tree figure drawing tool (Version 1.4.4) [Computer software]. https://github.com/rambaut/figtree
Rambaut, A., Drummond, A. J., Xie, D., Baele, G., & Suchard, M. A. (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67(5), 901-904.
Ramsey, C. B. (2009). Bayesian analysis of radiocarbon dates. Radiocarbon, 51(1), 337-360.
Reich, D., Thangaraj, K., Patterson, N., Price, A. L., & Singh, L. (2009). Reconstructing Indian population history. Nature, 461(7263), 489-494.
Reimer, P. J., Austin, W. E. N., Bard, E., Bayliss, A., Blackwell, P. G., Ramsey, C. B., Butzin, M., Cheng, H., Lawrence Edwards, R., Friedrich, M., Grootes, P. M., Guilderson, T. P., Hajdas, I., Heaton, T. J., Hogg, A. G., Hughen, K. A., Kromer, B., Manning, S. W., Muscheler, R., … Talamo, S. (2020). The IntCal20 northern hemisphere radiocarbon age calibration curve (0-55 cal kBP). Radiocarbon, 62(4), 725-757.
Renaud, G., Hanghøj, K., Korneliussen, T. S., Willerslev, E., & Orlando, L. (2019). Joint estimates of heterozygosity and runs of homozygosity for modern and ancient samples. Genetics, 212(3), 587-614.
Robinson, J. A., Brown, C., Kim, B. Y., Lohmueller, K. E., & Wayne, R. K. (2018). Purging of strongly deleterious mutations explains long-term persistence and absence of inbreeding depression in island foxes. Current Biology, 28(21), 3487-3494.e4.
Robinson, J. A., Ortega-Del Vecchyo, D., Fan, Z., Kim, B. Y., vonHoldt, B. M., Marsden, C. D., Lohmueller, K. E., & Wayne, R. K. (2016). Genomic flatlining in the endangered island fox. Current Biology, 26(9), 1183-1189.
Robinson, J. A., Räikkönen, J., Vucetich, L. M., Vucetich, J. A., Peterson, R. O., Lohmueller, K. E., & Wayne, R. K. (2019). Genomic signatures of extensive inbreeding in Isle Royale wolves, a population on the threshold of extinction. Science Advances, 5(5), eaau0757.
Rstudio Team. (2019). RStudio: Integrated development environment for R.
Saitou, N., & Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4), 406-425.
Schliep, K., Potts, A. J., Morrison, D. A., & Grimm, G. W. (2017). Intertwining phylogenetic trees and networks. Methods in Ecology and Evolution, 8(10), 1212-1220.
Schliep, K. P. (2011). phangorn: Phylogenetic analysis in R. Bioinformatics, 27(4), 592-593.
Schmidt, N. M., Pedersen, S. H., Mosbacher, J. B., & Hansen, L. H. (2015). Long-term patterns of muskox (Ovibos moschatus) demographics in high arctic Greenland. Polar Biology, 38(10), 1667-1675.
Schmidt, N. M., Reneerkens, J., Christensen, J. H., Olesen, M., & Roslin, T. (2019). An ecosystem-wide reproductive failure with more snow in the Arctic. PLoS Biology, 17(10), e3000392.
Schubert, M., Jónsson, H., Chang, D., Der Sarkissian, C., Ermini, L., Ginolhac, A., Albrechtsen, A., Dupanloup, I., Foucal, A., Petersen, B., Fumagalli, M., Raghavan, M., Seguin-Orlando, A., Korneliussen, T. S., Velazquez, A. M. V., Stenderup, J., Hoover, C. A., Rubin, C.-J., Alfarhan, A. H., … Orlando, L. (2014). Prehistoric genomes reveal the genetic foundation and cost of horse domestication. Proceedings of the National Academy of Sciences of the United States of America, 111(52), E5661-E5669.
Schubert, M., Lindgreen, S., & Orlando, L. (2016). AdapterRemoval v2: Rapid adapter trimming, identification, and read merging. BMC Research Notes, 9, 88.
Shaffer, M. L. (1981). Minimum population sizes for species conservation. Bioscience, 31(2), 131-134.
Sinding, M.-H. S., Gopalakrishan, S., Vieira, F. G., Samaniego Castruita, J. A., Raundrup, K., Heide Jørgensen, M. P., Meldgaard, M., Petersen, B., Sicheritz-Ponten, T., Mikkelsen, J. B., Marquard-Petersen, U., Dietz, R., Sonne, C., Dalén, L., Bachmann, L., Wiig, Ø., Hansen, A. J., & Gilbert, M. T. P. (2018). Population genomics of grey wolves and wolf-like canids in North America. PLoS Genetics, 14(11), e1007745.
Skoglund, P., Northoff, B. H., Shunkov, M. V., Derevianko, A. P., Pääbo, S., Krause, J., & Jakobsson, M. (2014). Separating endogenous ancient DNA from modern day contamination in a Siberian Neandertal. Proceedings of the National Academy of Sciences of the United States of America, 111(6), 2229-2234.
Skotte, L., Korneliussen, T. S., & Albrechtsen, A. (2013). Estimating individual admixture proportions from next generation sequencing data. Genetics, 195(3), 693-702.
Smit, A., & Hubley, R. (2017). RMBlast. Institute for Systems Biology. [cited 2017 Dec 15]. http://www.Repeatmasker.org/RMBlast.html
Smit, A. F. A., Hubley, R., & Green, P. (2019). 2013-2015. RepeatMasker Open-4.0.
Soule, M. E. (1976). Allozyme variation, its determinants in space and time. In Molecular Evolution (pp. 60-77). Sinauer Associates.
Stecher, G., Tamura, K., & Kumar, S. (2020). Molecular evolutionary genetics analysis (MEGA) for macOS. Molecular Biology and Evolution, 37(4), 1237-1239.
Steiner, C. C., Putnam, A. S., Hoeck, P. E. A., & Ryder, O. A. (2013). Conservation genomics of threatened animal species. Annual Review of Animal Biosciences, 1, 261-281.
Stoffel, M. A., Johnston, S. E., Pilkington, J. G., & Pemberton, J. M. (2021). Genetic architecture and lifetime dynamics of inbreeding depression in a wild mammal. Nature Communciations, 12, 2972.
Stokes, C. R. (2017). Deglaciation of the Laurentide Ice Sheet from the last glacial maximum. Cuadernos de Investigación Geográfica, 43(2), 377-428.
Taylor, R. S., Manseau, M., Klütsch, C. F. C., Polfus, J. L., Steedman, A., Hervieux, D., Kelly, A., Larter, N. C., Gamberg, M., Schwantje, H., & Wilson, P. J. (2021). Population dynamics of caribou shaped by glacial cycles before the last glacial maximum. Molecular Ecology, 30(23), 6121-6143.
Tener, J. S. (1965). Muskoxen in Canada: A biological and taxonomic review. Department of Northern Affairs and National Resources, Canadian Wildlife Service.
Thomas, J. E., Carvalho, G. R., Haile, J., Rawlence, N. J., Martin, M. D., Ho, S. Y., Sigfússon, A. Þ., Jósefsson, V. A., Frederiksen, M., Linnebjerg, J. F., Samaniego Castruita, J. A., Niemann, J., Sinding, M.-H. S., Sandoval-Velasco, M., Soares, A. E., Lacy, R., Barilaro, C., Best, J., Brandis, D., … Knapp, M. (2019). Demographic reconstruction from ancient DNA supports rapid extinction of the great auk. eLife, 8, eLife.47509.
Thulin, C.-G., Englund, L., Ericsson, G., & Spong, G. (2011). The impact of founder events and introductions on genetic variation in the muskox Ovibos moschatus in Sweden. Acta Theriologica, 56(4), 305-314.
To, T.-H., Jung, M., Lycett, S., & Gascuel, O. (2016). Fast dating using least-squares criteria and algorithms. Systematic Biology, 65(1), 82-97.
Tomaselli, M., Dalton, C., Duignan, P. J., Kutz, S., van der Meer, F., Kafle, P., Surujballi, O., Turcotte, C., & Checkley, S. (2016). Contagious Ecthyma, Rangiferine Brucellosis, and lungworm infection in a Muskox (Ovibos moschatus) from the Canadian Arctic, 2014. Journal of Wildlife Diseases, 52(3), 719-724.
Van Coeverden de Groot, P. J. V. C. (2001). Conservation genetic implications of microsatellite variation in the muskox Ovibos moschatus: The effect of refugial isolation and the Arctic Ocean on genetic structure. PhD thesis, Queen's University.
Van Der Valk, T., De Manuel, M., Marques-Bonet, T., & Guschanski, K. (2021). Estimates of genetic load suggest frequent purging of deleterious alleles in small populations. bioRxiv. https://doi.org/10.1101/696831
van der Valk, T., Díez-Del-Molino, D., Marques-Bonet, T., Guschanski, K., & Dalén, L. (2019). Historical genomes reveal the genomic consequences of recent population decline in eastern gorillas. Current Biology, 29(1), 165-170.e6.
Van Rossum, G., & Drake, F. L. (2009). Python 3 reference manual: (python documentation manual part 2). CreateSpace Independent Publishing Platform.
Vibe, C. (1958). The musk ox in East Greenland. Mammalia, 22(1-4), 168-174.
Waltari, E., & Cook, J. A. (2005). Hares on ice: Phylogeography and historical demographics of Lepus arcticus, L. othus, and L. timidus (Mammalia: Lagomorpha). Molecular Ecology, 14(10), 3005-3016.
Waples, R. K., Albrechtsen, A., & Moltke, I. (2019). Allele frequency-free inference of close familial relationships from genotypes or low-depth sequencing data. Molecular Ecology, 28(1), 35-48.
Westbury, M. V., Hartmann, S., Barlow, A., Wiesel, I., Leo, V., Welch, R., Parker, D. M., Sicks, F., Ludwig, A., Dalén, L., & Hofreiter, M. (2018). Extended and continuous decline in effective population size results in low genomic diversity in the world's rarest hyena species, the brown hyena. Molecular Biology and Evolution, 35(5), 1225-1237.
Westbury, M. V., Petersen, B., Garde, E., Heide-Jørgensen, M. P., & Lorenzen, E. D. (2019). Narwhal genome reveals long-term low genetic diversity despite current large abundance size. iScience, 15, 592-599.
Wickham, H. (2021). ggplot2: elegant graphics for data analysis. 2016. 978-973 https://ggplot2.tidyverse.org
Xue, Y., Prado-Martinez, J., Sudmant, P. H., Narasimhan, V., Ayub, Q., Szpak, M., Frandsen, P., Chen, Y., Yngvadottir, B., Cooper, D. N., de Manuel, M., Hernandez-Rodriguez, J., Lobon, I., Siegismund, H. R., Pagani, L., Quail, M. A., Hvilsom, C., Mudakikwa, A., Eichler, E. E., … Scally, A. (2015). Mountain gorilla genomes reveal the impact of long-term population decline and inbreeding. Science, 348(6231), 242-245.
Yang, D. Y., Eng, B., Waye, J. S., Dudar, J. C., & Saunders, S. R. (1998). Technical Note: Improved DNA extraction from ancient bones using silica-based spin columns. American Journal of Physical Anthropology, 543, 539-543.
Zhou, X., Sun, F., Xu, S., Fan, G., Zhu, K., Liu, X., Chen, Y., Shi, C., Yang, Y., Huang, Z., Chen, J., Hou, H., Guo, X., Chen, W., Chen, Y., Wang, X., Lv, T., Yang, D., Zhou, J., … Yang, G. (2013). Baiji genomes reveal low genetic variability and new insights into secondary aquatic adaptations. Nature Communications, 4, 2708.