Genomic recovery lags behind demographic recovery in bottlenecked populations of the Channel Island fox, Urocyon littoralis.
Channel Islands
bottleneck
conservation
conservation genomics
demography
exome capture
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
08 2023
08 2023
Historique:
revised:
26
04
2023
received:
14
07
2022
accepted:
05
05
2023
medline:
25
7
2023
pubmed:
22
5
2023
entrez:
22
5
2023
Statut:
ppublish
Résumé
With continued global change, recovery of species listed under the Endangered Species Act is increasingly challenging. One rare success was the recovery and delisting of the Channel Island fox (Urocyon littoralis) after 90%-99% population declines in the 1990s. While their demographic recovery was marked, less is known about their genetic recovery. To address genetic changes, we conducted the first multi-individual and population-level direct genetic comparison of samples collected before and after the recent bottlenecks. Using whole-exome sequencing, we found that already genetically depauperate populations were further degraded by the 1990s declines and remain low, particularly on San Miguel and Santa Rosa Islands, which underwent the most severe bottlenecks. The two other islands that experienced recent bottlenecks (Santa Cruz, and Santa Catalina islands) showed mixed results based on multiple metrics of genetic diversity. Previous island fox genomics studies showed low genetic diversity before the declines and no change after the demographic recovery, thus this is the first study to show a decrease in genetic diversity over time in U. littoralis. Additionally, we found that divergence between populations consistently increased over time, complicating prospects for using inter-island translocation as a conservation tool. The Santa Catalina subspecies is now federally listed as threatened, yet other de-listed subspecies are still recovering genetic variation which may limit their ability to adapt to changing environmental conditions. This study further demonstrates that species conservation is more complex than population size and that some island fox populations are not yet 'out of the woods'.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4151-4164Informations de copyright
© 2023 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.
Références
Adams, N. E., Becker, M. A., & Edmands, S. (2021). Effect of geography and captivity on scat bacterial communities in the Imperiled Channel Island fox. Frontiers in Microbiology, 12, 748323. https://doi.org/10.3389/FMICB.2021.748323
Allendorf, F. W. (1986). Genetic drift and the loss of alleles versus heterozygosity. Zoo Biology, 5(2), 181-190. https://doi.org/10.1002/zoo.1430050212
Axelsson, E., Willerslev, E., Gilbert, M. T. P., & Nielsen, R. (2008). The effect of ancient DNA damage on inferences of demographic histories. Molecular Biology and Evolution, 25(10), 2181-2187. https://doi.org/10.1093/MOLBEV/MSN163
Barrett, R. D. H., & Schluter, D. (2008). Adaptation from standing genetic variation. Trends in Ecology and Evolution, 23(1), 38-44. https://doi.org/10.1016/j.tree.2007.09.008
Bi, K., Linderoth, T., Vanderpool, D., Good, J. M., Nielsen, R., & Moritz, C. (2013). Unlocking the vault: Next-generation museum population genomics. Molecular Ecology, 22(24), 6018-6032. https://doi.org/10.1111/mec.12516
Broeckx, B. J. G., Coopman, F., Verhoeven, G. E. C., Bavegems, V., De Keulenaer, S., De Meester, E., Van Niewerburgh, F., & Deforce, D. (2014). Development and performance of a targeted whole exome sequencing enrichment kit for the dog (Canis familiaris build 3.1). Scientific Reports, 4, 5597. https://doi.org/10.1038/srep05597
Carpenter, M. L., Buenrostro, J. D., Valdiosera, C., Schroeder, H., Allentoft, M. E., Sikora, M., Rasmussen, M., Gravel, S., Guillén, S., Nekhrizov, G., Leshtakov, K., Dimitrova, D., Theodossiev, N., Pettener, D., Luiselli, D., Sandoval, K., Moreno-Estrada, A., Li, Y., Wang, J., … Bustamante, C. D. (2013). Pulling out the 1%: Whole-genome capture for the targeted enrichment of ancient DNA sequencing libraries. American Journal of Human Genetics, 93(5), 852-864. https://doi.org/10.1016/j.ajhg.2013.10.002
Cavill, E. L., Gopalakrishnan, S., Puetz, L. C., Ribeiro, Â. M., Mak, S. S. T., da Fonseca, R. R., Pacheco, G., Dunlop, B., Accouche, W., Shah, N., Zora, A., Calabrese, L., Genner, M., Jones, G., Guo, C., Zhang, G., & Gilbert, M. T. P. (2022). Conservation genomics of the endangered Seychelles magpie-Robin (Copsychus sechellarum): A unique insight into the history of a precious endemic bird. IBIS, 164(2), 396-410. https://doi.org/10.1111/IBI.13023
Ceballos, F. C., Hazelhurst, S., & Ramsay, M. (2018). Assessing runs of homozygosity: A comparison of SNP array and whole genome sequence low coverage data. BMC Genomics, 19(1), 1-12. https://doi.org/10.1186/s12864-018-4489-0
Ceballos, F. C., Joshi, P. K., Clark, D. W., Ramsay, M., & Wilson, J. F. (2018). Runs of homozygosity: Windows into population history and trait architecture. Nature Reviews Genetics, 19(4), 220-234. https://doi.org/10.1038/nrg.2017.109
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
Cingolani, P., Patel, V. M., Coon, M., Nguyen, T., Land, S. J., Ruden, D. M., & Lu, X. (2012). Using Drosophila melanogaster as a model for genotoxic chemical mutational studies with a new program, SnpSift. Frontiers in Genetics, 3(MAR), 35. https://doi.org/10.3389/fgene.2012.00035
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. https://doi.org/10.4161/fly.19695
Coonan, T. J., Bakker, V., Hudgens, B., Boser, C. L., Garcelon, D. K., & Morrison, S. A. (2014). On the fast track to recovery: Island foxes on the northern Channel Islands. Monographs of the Western North American Naturalist, 7, 373-381.
Coonan, T. J., Schwemm, C. A., & Garcelon, D. K. (2010). Decline and recovery of the Island fox. Cambridge University Press.
Coonan, T. J., Schwemm, C. A., Roemer, G. W., Garcelon, D. K., & Munson, L. (2005). Decline of an Island fox subspecies to near extinction. The Southwestern Naturalist, 50(1), 32-41.
Danecek, P., Auton, A., Abecasis, G., Albers, C. A., Banks, E., DePristo, M. A., Handsaker, R. E., Lunter, G., Marth, G. T., Sherry, S. T., McVean, G., & Durbin, R. (2011). The variant call format and VCFtools. Bioinformatics, 27(15), 2156-2158. https://doi.org/10.1093/bioinformatics/btr330
Danecek, P., Bonfield, J. K., Liddle, J., Marshall, J., Ohan, V., Pollard, M. O., Whitwham, A., Keane, T., McCarthy, S. A., Davies, R. M., & Li, H. (2021). Twelve years of SAMtools and BCFtools. GigaScience, 10(2), giab008.
DeCandia, A. L., Brenner, L. J., King, J. L., & VonHoldt, B. M. (2020). Ear mite infection is associated with altered microbial communities in genetically depauperate Santa Catalina Island foxes (Urocyon littoralis catalinae). Molecular Ecology, 29(8), 1463-1475. https://doi.org/10.1111/mec.15325
Devlin, B., & Roeder, K. (1999). Genomic control for association studies. Biometrics, 55(4), 997-1004. https://doi.org/10.1111/j.0006-341X.1999.00997.x
Do, C., Waples, R. S., Peel, D., Macbeth, G. M., Tillett, B. J., & Ovenden, J. R. (2014). NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Molecular Ecology Resources, 14(1), 209-214. https://doi.org/10.1111/1755-0998.12157
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., Lewin, H. A., Hastie, A. R., Formenti, G., … Dalén, L. (2021). Population genomics of the critically endangered kākāpō. Cell Genomics, 1, 100002. https://doi.org/10.1016/j.xgen.2021.100002
Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), 1792-1797. https://doi.org/10.1093/nar/gkh340
Frankham, R. (2016). Genetic rescue benefits persist to at least the F3 generation, based on a meta-analysis. Biological Conservation, 195, 33-36. https://doi.org/10.1016/j.biocon.2015.12.038
Frankham, R., Ballou, J. D., & Briscoe, D. A. (2010). Genetic management of captive populations for reintroduction. In Introduction to conservation genetics (pp. 431-452). Cambridge University Press.
Frankham, R., Ballou, J. D., & Briscoe, D. A. (2002). Introduction to conservation genetics (third). Cambridge University Press http://books.google.co.jp/books?id=F-XB8hqZ4s8C
Freedman, A. H., Gronau, I., Schweizer, R. M., Vecchyo, D. O.-D., Han, E., Silva, P. M., Galaverni, M., Fan, Z., Marx, P., Lorente-Galdos, B., Beale, H., Ramirez, O., Hormozdiari, F., Alkan, C., Vilà, C., Squire, K., Geffen, E., Kusak, J., Boyko, A. R., … Novembre, J. (2014). Genome sequencing highlights the dynamic early history of dogs. PLoS Genetics, 10(1), e1004016. https://doi.org/10.1371/JOURNAL.PGEN.1004016
Funk, W. C., Lovich, R. E., Hohenlohe, P. A., Hofman, C. A., Morrison, S. A., Sillett, T. S., Ghalambor, C. K., Maldonado, J. E., Rick, T. C., Day, M. D., Polato, N. R., Fitzpatrick, S. W., Coonan, T. J., Crooks, K. R., Dillon, A., Garcelon, D. K., King, J. L., Boser, C. L., Gould, N., & Andelt, W. F. (2016). Adaptive divergence despite strong genetic drift: Genomic analysis of the evolutionary mechanisms causing genetic differentiation in the Island fox (Urocyon littoralis). Molecular Ecology, 25(10), 2176-2194. https://doi.org/10.1111/mec.13605
Garrison, E., & Marth, G. (2012). Haplotype-based variant detection from short-read sequencing. ArXiv, 1-9. arXiv:1207.3907 [q-bio.GN].
Gelfman, S., Burstein, D., Penn, O., Savchenko, A., Amit, M., Schwartz, S., Pupko, T., & Ast, G. (2012). Changes in exon − intron structure during vertebrate evolution affect the splicing pattern of exons. Genome Research, 22, 35-50. https://doi.org/10.1101/gr.119834.110
Ginolhac, A., Rasmussen, M., Gilbert, M. T. P., Willerslev, E., & Orlando, L. (2011). mapDamage: Testing for damage patterns in ancient DNA sequences. Bioinformatics, 27(15), 2153-2155. https://doi.org/10.1093/bioinformatics/btr347
Hand, B. K., Muhlfeld, C. C., Wade, A. A., Kovach, R. P., Whited, D. C., Narum, S. R., Matala, A. P., Ackerman, M. W., Garner, B. A., Kimball, J. S., Stanford, J. A., & Luikart, G. (2016). Climate variables explain neutral and adaptive variation within salmonid metapopulations: The importance of replication in landscape genetics. Molecular Ecology, 25(3), 689-705. https://doi.org/10.1111/mec.13517
Hofman, C. A., Rick, T. C., Hawkins, M. T. R., Funk, W. C., Morrison, A., Newsome, S. D., Sillett, T. S., & Fleischer, R. C. (2015). Mitochondrial genomes suggest rapid evolution of dwarf California Channel Islands foxes (Urocyon littoralis). PLoS One, 10, e0118240. https://doi.org/10.1371/journal.pone.0118240
Holgate, P. (1966). A mathematical study of the founder principle of evolutionary genetics. Journal of Applied Probability, 3(1), 115-128.
Island Fox Conservation Working Group. (2018). Summary report. Santa Barbara, California.
Jackson, H. A., Percival-Alwyn, L., Ryan, C., Albeshr, M. F., Venturi, L., Morales, H. E., Mathers, T. C., Cocker, J., Speak, S. A., Accinelli, G. G., Barker, T., Heavens, D., Willman, F., Dawson, D., Ward, L., Tatayah, V., Zuël, N., Young, R., Concannon, L., … van Oosterhout, C. (2022). Genomic erosion in a demographically recovered bird species during conservation rescue. Conservation Biology, 36(4), 1-13. https://doi.org/10.1111/cobi.13918
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. https://doi.org/10.1093/bioinformatics/btt193
Kassambara, A. (2023). Rstatix: Pipe-friendly framework for basic statistical tests. R package version 0.7.2. https://rpkgs.datanovia.com/rstatix/
Kent, W. J., Sugnet, C. W., Furey, T. S., & Roskin, K. M. (2002). The human genome browser at UCSC. Genome Research, 12(6), 996-1006. https://doi.org/10.1101/gr.229102
King, J. L., Duncan, C. L., & Garcelon, D. K. (2014). Status of the Santa Catalina Island fox thirteen years after its decline. Monographs of the Western North American Naturalist, 7(1), 382-396. https://doi.org/10.3398/042.007.0129
Korunes, K. L., & Samuk, K. (2021). Pixy: Unbiased estimation of nucleotide diversity and divergence in the presence of missing data. Molecular Ecology Resources, 21, 1359-1368. https://doi.org/10.1111/1755-0998.13326
Laughrin, L. (1980). Populations and status of the Island fox. In D. M. Power (Ed.), The California Islands: Proceedings of a multidisciplinary symposium, Santa Barbara Museum of Natural History, Santa Barbara, California (pp. 745-750). Santa Barbara Museum of Natural History.
Lee, T.-H., Guo, H., Wang, X., Kim, C., & Paterson, A. H. (2014). SNPhylo: A pipeline to construct a phylogenetic tree from huge SNP data. BMC Genomics, 15(1), 162. https://doi.org/10.1186/1471-2164-15-162
Li, H., & Durbin, R. (2009). Fast and accurate short read alignment with burrows-Wheeler transform. Bioinformatics, 25, 1754-1760.
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., & Durbin, R. (2009). The sequence alignment/map format and SAMtools. Bioinformatics, 25(16), 2078-2079. https://doi.org/10.1093/bioinformatics/btp352
Li, Y. Y., Tsang, E. P. K., Cui, M. Y., & Chen, X. Y. (2012). Too early to call it success: An evaluation of the natural regeneration of the endangered Metasequoia glyptostroboides. Biological Conservation, 150(1), 1-4. https://doi.org/10.1016/j.biocon.2012.02.020
Lindblad-Toh, K., Wade, C. M., Mikkelsen, T. S., Karlsson, E. K., Jaffe, D. B., Kamal, M., Clamp, M., Chang, J. L., Kulbokas, E. J., Zody, M. C., Mauceli, E., Xie, X., Breen, M., Wayne, R. K., Ostrander, E. a., Ponting, C. P., Galibert, F., Smith, D. R., DeJong, P. J., … Lander, E. S. (2005). Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature, 438(7069), 803-819. https://doi.org/10.1038/nature04338
Lischer, H. E. L., & Excoffier, L. (2012). PGDSpider: An automated data conversion tool for connecting population genetics and genomics programs. Bioinformatics, 28(2), 298-299. https://doi.org/10.1093/bioinformatics/btr642
Luikart, G., Allendorf, F. W., Cornuet, J. M., & Sherwin, W. B. (1998). Distortion of allele frequency distributions provides a test for recent population bottlenecks. Journal of Heredity, 89(3), 238-247. https://doi.org/10.1093/jhered/89.3.238
Matala, A. P., Ackerman, M. W., Campbell, M. R., & Narum, S. R. (2014). Relative contributions of neutral and non-neutral genetic differentiation to inform conservation of steelhead trout across highly variable landscapes. Evolutionary Applications, 7(6), 682-701. https://doi.org/10.1111/eva.12174
Mullen, L. M., & Hoekstra, H. E. (2008). Natural selection along an environmental gradient: A classic cline in mouse pigmentation. Evolution, 62(7), 1555-1570. https://doi.org/10.1111/J.1558-5646.2008.00425.X
Naqvi, S., Godfrey, A. K., Hughes, J. F., Goodheart, M. L., Mitchell, R. N., & Page, D. C. (2019). Conservation, acquisition, and functional impact of sex-biased gene expression in mammals. Science, 365(6450), eaaw7317. https://doi.org/10.1126/science.aaw7317
Nei, M., Maruyama, T., & Chakraborty, R. (1975). The bottleneck effect and genetic variability in populations. Evolution, 29(March), 1-10.
Nyakatura, K., & Bininda-Emonds, O. R. (2012). Updating the evolutionary history of carnivora (Mammalia): A new species-level supertree complete with divergence time estimates. BMC Biology, 10(1), 12. https://doi.org/10.1186/1741-7007-10-12
Ogle, D. H., Doll, J. C., Wheeler, A. P., & Dinno, A. (2023). FSA: Simple fisheries stock assessment methods. R package version 0.9.4. https://CRAN.R-project.org/package=FSA
Oliva, A., Tobler, R., Cooper, A., Llamas, B., & Souilmi, Y. (2021). Systematic benchmark of ancient DNA read mapping. Briefings in Bioinformatics, 22(5), bbab076. https://doi.org/10.1093/bib/bbab076
Perkins, S. J., Smith, K. F., Williams, S. C., Haris, P. I., Chapman, D., & Sim, R. B. (1994). The secondary structure of the von Willebrand factor type a domain in factor B of human complement by Fourier transform infrared spectroscopy: Its occurrence in collagen types VI, VII, XII and XIV, the integrins and other proteins by averaged structure predictions. Journal of Molecular Biology, 238(1), 104-119. https://doi.org/10.1006/jmbi.1994.1271
R Core Team. (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/
Ralls, K., Sunnucks, P., Lacy, R. C., & Frankham, R. (2020). Genetic rescue: A critique of the evidence supports maximizing genetic diversity rather than minimizing the introduction of putatively harmful genetic variation. Biological Conservation, 251(April), 108784. https://doi.org/10.1016/j.biocon.2020.108784
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. https://doi.org/10.1016/J.CUB.2018.08.066
Robinson, J. A., Vecchyo, D. O., Fan, Z., Marsden, C. D., Lohmueller, K. E., & Wayne, R. K. (2016). Genomic flatlining in the endangered Island fox. Current Biology, 26(9), 1183-1189.
Roemer, G. W., Coonan, T. J., Garcelon, D. K., Bascompte, J., Laughrin, L., & Al, E. T. (2001). Feral pigs facilitate hyperpredation by golden eagles and indirectly cause the decline of the Island fox. Animal Conservation, 4, 307-318.
Rowe, K. C., Singhal, S., Macmanes, M. D., Ayroles, J. F., Morelli, T. L., Rubidge, E. M., Bi, K., & Moritz, C. C. (2011). Museum genomics: Low-cost and high-accuracy genetic data from historical specimens. Molecular Ecology Resources, 11(6), 1082-1092. https://doi.org/10.1111/j.1755-0998.2011.03052.x
RStudio Team. (2022). RStudio: Integrated development environment for R. RStudio, PBC. http://www.rstudio.com/
Sanchez, J. N., & Hudgens, B. R. (2015). Interactions between density, home range behaviors, and contact rates in the Channel Island fox (Urocyon littoralis). Ecology and Evolution, 5(12), 2466-2477. https://doi.org/10.1002/ece3.1533
Schliep, K. (2011). Phangorn: Phylogenetic analysis in R. Bioinformatics, 27(4), 592-593. https://doi.org/10.1093/bioinformatics/btq706
Schubert, M., Ginolhac, A., Lindgreen, S., Thompson, J. F., Al-Rasheid, K. A. S., Willerslev, E., Krogh, A., & Orlando, L. (2012). Improving ancient DNA read mapping against modern reference genomes. BMC Genomics, 13, 178. https://doi.org/10.1186/1471-2164-13-178
Schubert, M., Lindgreen, S., & Orlando, L. (2016). AdapterRemoval v2: Rapid adapter trimming, identification, and read merging. BMC Research Notes, 9(1), 88. https://doi.org/10.1186/s13104-016-1900-2
Suckling, K., Mehrhoff, L. A., Beam, R., & Hartl, B. (2016). A wild success, a systematic review of bird recovery under the endangered species act. Center for Biological Diversity.
Taron, U. H., Lell, M., Barlow, A., & Paijmans, J. L. A. (2018). Testing of alignment parameters for ancient samples: Evaluating and optimizing mapping parameters for ancient samples using the TAPAS tool. Genes, 9(3), 157. https://doi.org/10.3390/genes9030157
Taylor, H. R., Colbourne, R. M., Robertson, H. A., Nelson, N. J., Allendorf, F. W., & Ramstad, K. M. (2017). Cryptic inbreeding depression in a growing population of a long-lived species. Molecular Ecology, 26(3), 799-813. https://doi.org/10.1111/MEC.13977
Timm, S. F., Munson, L., Summers, B. A., Terio, K. A., Dubovi, E. J., Rupprecht, C. E., Kapil, S., & Garcelon, D. K. (2009). A suspected canine distemper epidemic as the cause of a catastrophic decline in Santa Catalina Island foxes (Urocyon littoralis catalinae). Journal of Wildlife Diseases, 45(2), 333-343. https://doi.org/10.7589/0090-3558-45.2.333
Topalidou, I., Cattin-Ortolá, J., Pappas, A. L., Cooper, K., Merrihew, G. E., MacCoss, M. J., & Ailion, M. (2016). The EARP complex and its interactor EIPR-1 are required for cargo sorting to dense-core vesicles. PLoS Genetics, 12(5), 1-29. https://doi.org/10.1371/journal.pgen.1006074
U. S. Fish and Wildlife Service. (2017). ESA basics 40 years of conserving endangered species.
U.S. Department of the Interior. (2016). Interior announces fastest successful recovery of an endangered species act-listed mammal; three Island fox subspecies now fully delisted. https://www.doi.gov/pressreleases/interior-announces-fastest-successful-recovery-endangered-species-act-listed-mammal
Von Seth, J., Dussex, N., Díez-del-Molino, D., Van der Valk, T., Kutschera, V. E., Kierczak, M., Steiner, C. C., Liu, S., Gilbert, M. T. P., Sinding, M. S., Prost, F., Guschanski, K., Nathan, S. K. S. S., Brace, S., Chan, Y. L., Wheat, C. W., Skoglund, P., Ryder, O. A., Goossens, B., … Dalén, S. (2021). Genomic insights into the conservation status of the world's last remaining Sumatrans rhinoceros populations. Nature Communications, 12, 2393. https://doi.org/10.1038/s41467-021-22386-8
Weir, B. S., & Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution, 38(6), 1358. https://doi.org/10.2307/2408641
Wong, S. S. F., Kuei, J. J., Prasad, N., Agonafer, E., Mendoza, G. A., Pemberton, T. J., & Patel, P. I. (2007). A simple method for DNA isolation from clotted blood extricated rapidly from serum separator tubes. Clinical Chemistry, 53(3), 520-522. https://doi.org/10.1373/clinchem.2005.062604
Woodworth, L. M., Montgomery, M. E., Briscoe, D. A., & Frankham, R. (2002). Rapid genetic deterioration in captive populations: Causes and conservation implications. Conservation Genetics, 3, 277-288.
Yu, G., Smith, D. K., Zhu, H., Guan, Y., & Lam, T. T. Y. (2017). Ggtree: An r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods in Ecology and Evolution, 8(1), 28-36. https://doi.org/10.1111/2041-210X.12628
Zhan, X., Dixon, A., Batbayar, N., Bragin, E., Ayas, Z., Deutschova, L., Chavko, J., Domashevsky, S., Dorosencu, A., Bagyura, J., Gombobaatar, S., Grlica, I. D., Levin, A., Milobog, Y., Ming, M., Prommer, M., Purev-Ochir, G., Ragyov, D., Tsurkanu, V., … Bruford, M. W. (2015). Exonic versus intronic SNPs: Contrasting roles in revealing the population genetic differentiation of a widespread bird species. Heredity, 114(1), 1-9. https://doi.org/10.1038/hdy.2014.59
Zhao, C., Zhang, H., Liu, G., Yang, X., & Zhang, J. (2016). The complete mitochondrial genome of the Tibetan fox (Vulpes ferrilata) and implications for the phylogeny of Canidae. Comptes Rendus Biologies, 339(2), 68-77. https://doi.org/10.1016/j.crvi.2015.11.005
Zhao, J. H. (2007). Gap: Genetic analysis package. Journal of Statistical Software, 23(8), 1-18. https://doi.org/10.18637/jss.v023.i08