Multiple types of genomic variation contribute to adaptive traits in the mustelid subfamily Guloninae.

adaptation gene family evolution genomics mustelids positive selection structural variation

Journal

Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478

Informations de publication

Date de publication:
05 2022
Historique:
revised: 06 03 2022
received: 18 11 2021
accepted: 14 03 2022
pubmed: 26 3 2022
medline: 18 5 2022
entrez: 25 3 2022
Statut: ppublish

Résumé

Species of the mustelid subfamily Guloninae inhabit diverse habitats on multiple continents, and occupy a variety of ecological niches. They differ in feeding ecologies, reproductive strategies and morphological adaptations. To identify candidate loci associated with adaptations to their respective environments, we generated a de novo assembly of the tayra (Eira barbara), the earliest diverging species in the subfamily, and compared this with the genomes available for the wolverine (Gulo gulo) and the sable (Martes zibellina). Our comparative genomic analyses included searching for signs of positive selection, examining changes in gene family sizes and searching for species-specific structural variants. Among candidate loci associated with phenotypic traits, we observed many related to diet, body condition and reproduction. For example, for the tayra, which has an atypical gulonine reproductive strategy of aseasonal breeding, we observed species-specific changes in many pregnancy-related genes. For the wolverine, a circumpolar hypercarnivore that must cope with seasonal food scarcity, we observed many changes in genes associated with diet and body condition. All types of genomic variation examined (single nucleotide polymorphisms, gene family expansions, structural variants) contributed substantially to the identification of candidate loci. This argues strongly for consideration of variation other than single nucleotide polymorphisms in comparative genomics studies aiming to identify loci of adaptive significance.

Identifiants

pubmed: 35334142
doi: 10.1111/mec.16443
doi:

Banques de données

Dryad
['10.5061/dryad.xgxd254hz']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2898-2919

Commentaires et corrections

Type : ErratumIn

Informations de copyright

© 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

Références

Abduriyim, S., Nishita, Y., Abramov, A. V., Solovyev, V. A., Saveljev, A. P., Kosintsev, P. A., Kryukov, A. P., Raichev, E., Väinölä, R., Kaneko, Y., & Masuda, R. (2019). Variation in pancreatic amylase gene copy number among Eurasian badgers (Carnivora, Mustelidae, Meles) and its relationship to diet. Journal of Zoology, 308(1), 28-36.
Alatalo, R. V., & Mappes, J. (1996). Tracking the evolution of warning signals. Nature, 382(6593), 708-710.
Alonge, M., Soyk, S., Ramakrishnan, S., Wang, X., Goodwin, S., Sedlazeck, F. J., Lippman, Z. B., & Schatz, M. C. (2019). RaGOO: fast and accurate reference-guided scaffolding of draft genomes. Genome Biology, 20(1), 224. https://doi.org/10.1186/s13059-019-1829-6
Al-Qusairi, L., Prokic, I., Amoasii, L., Kretz, C., Messaddeq, N., Mandel, J.-L., & Laporte, J. (2013). Lack of myotubularin (MTM1) leads to muscle hypotrophy through unbalanced regulation of the autophagy and ubiquitin-proteasome pathways. FASEB Journal, 27(8), 3384-3394. https://doi.org/10.1096/fj.12-220947
Angelis, K., & Dos Reis, M. (2015). The impact of ancestral population size and incomplete lineage sorting on Bayesian estimation of species divergence times. Current Zoology, 61(5), 874-885.
Anisimova, M., & Gascuel, O. (2006). Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Systematic Biology, 55(4), 539-552.
Armstrong, E. E., Taylor, R. W., Prost, S., Blinston, P., van der Meer, E., Madzikanda, H., Mufute, O., Mandisodza-Chikerema, R., Stuelpnagel, J., Sillero-Zubiri, C., & Petrov, D. (2019). Cost-effective assembly of the African wild dog (Lycaon pictus) genome using linked reads. GigaScience, 8(2), https://doi.org/10.1093/gigascience/giy124
Avellino, R., Carrella, S., Pirozzi, M., Risolino, M., Salierno, F. G., Franco, P., Stoppelli, P., Verde, P., Banfi, S., & Conte, I. (2013). miR-204 targeting of Ankrd13A controls both mesenchymal neural crest and lens cell migration. PLoS One, 8(4), e61099. https://doi.org/10.1371/journal.pone.0061099
Barnett, R., Westbury, M. V., Sandoval-Velasco, M., Vieira, F. G., Jeon, S., Zazula, G., Martin, M. D., Ho, S. Y. W., Mather, N., Gopalakrishnan, S., Ramos-Madrigal, J., de Manuel, M., Zepeda-Mendoza, M. L., Antunes, A., Baez, A. C., De Cahsan, B., Larson, G., O’Brien, S. J., Eizirik, E., … Gilbert, M. T. P. (2020). Genomic adaptations and evolutionary history of the extinct scimitar-toothed cat, Homotherium latidens. Current Biology, 30(24), 5018-5025.e5. https://doi.org/10.1016/j.cub.2020.09.051
Beichman, A. C., Koepfli, K.-P., Li, G., Murphy, W., Dobrynin, P., Kilver, S., Tinker, M. T., Murray, M. J., Johnson, J., Lindblad-Toh, K., Karlsson, E. K., Lohmueller, K. E., & Wayne, R. K. (2019). Aquatic adaptation and depleted diversity: a deep dive into the genomes of the sea otter and giant otter. Molecular Biology and Evolution, 36(12), 2631-2655. https://doi.org/10.1093/molbev/msz101
Blottner, S., Schön, J., & Jewgenow, K. (2006). Seasonally activated spermatogenesis is correlated with increased testicular production of testosterone and epidermal growth factor in mink (Mustela vison). Theriogenology, 66(6-7), 1593-1598. https://doi.org/10.1016/j.theriogenology.2006.01.041
Blount, J. D., Speed, M. P., Ruxton, G. D., & Stephens, P. A. (2009). Warning displays may function as honest signals of toxicity. Proceedings Biological Sciences, 276(1658), 871-877.
Broad Institute (2019). Picard Toolkit. GitHub Repository. https://broadinstitute.github.io/picard/
Brown, J. A., Eberhardt, D. M., Schrick, F. N., Roberts, M. P., & Godkin, J. D. (2003). Expression of retinol-binding protein and cellular retinol-binding protein in the bovine ovary. Molecular Reproduction and Development, 64(3), 261-269. https://doi.org/10.1002/mrd.10225
Buckley, R. M., Davis, B. W., Brashear, W. A., Farias, F. H. G., Kuroki, K., Graves, T., Hillier, L. W., Kremitzki, M., Li, G., Middleton, R. P., Minx, P., Tomlinson, C., Lyons, L. A., Murphy, W. J., & Warren, W. C. (2020). A new domestic cat genome assembly based on long sequence reads empowers feline genomic medicine and identifies a novel gene for dwarfism. PLoS Genetics, 16(10), e1008926. https://doi.org/10.1371/journal.pgen.1008926
Cahill, J. A., Soares, A. E. R., Green, R. E., & Shapiro, B. (2016). Inferring species divergence times using pairwise sequential Markovian coalescent modelling and low-coverage genomic data. Philosophical Transactions of the Royal Society B: Biological Sciences, 371(1699), https://doi.org/10.1098/rstb.2015.0138
Carmo, S. D., Fournier, D., Mounier, C., & Rassart, E. (2009). Human apolipoprotein D overexpression in transgenic mice induces insulin resistance and alters lipid metabolism. American Journal of Physiology-Endocrinology and Metabolism, 296(4), E802-E811. https://doi.org/10.1152/ajpendo.90725.2008
Catanach, A., Crowhurst, R., Deng, C., David, C., Bernatchez, L., & Wellenreuther, M. (2019). The genomic pool of standing structural variation outnumbers single nucleotide polymorphism by threefold in the marine teleost Chrysophrys auratus. Molecular Ecology, 28(6), 1210-1223.
Cavagna, P., Menotti, A., & Stanyon, R. (2000). Genomic homology of the domestic ferret with cats and humans. Mammalian Genome: Official Journal of the International Mammalian Genome Society, 11(10), 866-870. https://doi.org/10.1007/s003350010172
Chang, J.-M., Di Tommaso, P., & Notredame, C. (2014). TCS: a new multiple sequence alignment reliability measure to estimate alignment accuracy and improve phylogenetic tree reconstruction. Molecular Biology and Evolution, 31(6), 1625-1637. https://doi.org/10.1093/molbev/msu117
Chen, X., Schulz-Trieglaff, O., Shaw, R., Barnes, B., Schlesinger, F., Källberg, M., Cox, A. J., Kruglyak, S., & Saunders, C. T. (2016). Manta: rapid detection of structural variants and indels for germline and cancer sequencing applications. Bioinformatics, 32(8), 1220-1222. https://doi.org/10.1093/bioinformatics/btv710
Chiang, C., Layer, R. M., Faust, G. G., Lindberg, M. R., Rose, D. B., Garrison, E. P., Marth, G. T., Quinlan, A. R., & Hall, I. M. (2015). SpeedSeq: ultra-fast personal genome analysis and interpretation. Nature Methods, 12(10), 966-968. https://doi.org/10.1038/nmeth.3505
Chiang, C., Scott, A. J., Davis, J. R., Tsang, E. K., Li, X., Kim, Y., Hadzic, T., Damani, F. N., Ganel, L., Montgomery, S. B., Battle, A., Conrad, D. F., & Hall, I. M. (2017). The impact of structural variation on human gene expression. Nature Genetics, 49(5), 692-699. https://doi.org/10.1038/ng.3834
Coan, P. M., Vaughan, O. R., Sekita, Y., Finn, S. L., Burton, G. J., Constancia, M., & Fowden, A. L. (2010). Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice. The Journal of Physiology, 588(Pt 3), 527-538. https://doi.org/10.1113/jphysiol.2009.181214
Copeland, J. P., & Kucera, T. E. (1997). Wolverine (Gulo gulo). In: J. E. Harris, & C. V. Ogan, eds. Mesocarnivores of Northern California: Biology, management, and survey techniques, workshop manual. Humboldt State Univ. and the Wildlife Society, California North Coast Chapter, 127 p
D’Ambrosio, D. N., Clugston, R. D., & Blaner, W. S. (2011). Vitamin A metabolism: An update. Nutrients, 3(1), 63-103. https://doi.org/10.3390/nu3010063
Davison, A., Birks, J. D., Brookes, R. C., Messenger, J. E., & Griffiths, H. I. (2001). Mitochondrial phylogeography and population history of pine martens Martes martes compared with polecats Mustela putorius. Molecular Ecology, 10(10), 2479-2488. https://doi.org/10.1046/j.1365-294X.2001.01381.x
Defler, T. R. (1980). Notes on interactions between the Tayra (Eira barbara) and the white-fronted capuchin (Cebus albifrons). Journal of Mammalogy, 61(1), 156. https://doi.org/10.2307/1379979
DeSelm, C. J., Miller, B. C., Zou, W., Beatty, W. L., van Meel, E., Takahata, Y., Klumperman, J., Tooze, S. A., Teitelbaum, S. L., & Virgin, H. W. (2011). Autophagy proteins regulate the secretory component of osteoclastic bone resorption. Developmental Cell, 21(5), 966-974. https://doi.org/10.1016/j.devcel.2011.08.016
Dobrynin, P., Liu, S., Tamazian, G., Xiong, Z., Yurchenko, A. A., Krasheninnikova, K., Kliver, S., Schmidt-Küntzel, A., Koepfli, K.-P., Johnson, W., Kuderna, L. F. K., García-Pérez, R., Manuel, M. D., Godinez, R., Komissarov, A., Makunin, A., Brukhin, V., Qiu, W., Zhou, L., … O’Brien, S. J. (2015). Genomic legacy of the African cheetah, Acinonyx jubatus. Genome Biology, 16, 277. https://doi.org/10.1186/s13059-015-0837-4
Dudchenko, O., Batra, S. S., Omer, A. D., Nyquist, S. K., Hoeger, M., Durand, N. C., Shamim, M. S., Machol, I., Lander, E. S., Aiden, A. P., & Aiden, E. L. (2017). De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science, 356(6333), 92-95.
Dudchenko, O., Shamim, M. S., Batra, S. S., Durand, N. C., Musial, N. T., Mostofa, R., Pham, M., St Hilaire, B. G., Yao, W., Stamenova, E., Hoeger, M., Nyquist, S. K., Korchina, V., Pletch, K., Flanagan, J. P., Tomaszewicz, A., McAloose, D., Estrada, C. P., Novak, B. J., Aiden, E. L. (2018). The Juicebox Assembly Tools module facilitates de novo assembly of mammalian genomes with chromosome-length scaffolds for under $1000 (p. 254797). https://doi.org/10.1101/254797
Ekblom, R., Brechlin, B., Persson, J., Smeds, L., Johansson, M., Magnusson, J., Flagstad, Ø., & Ellegren, H. (2018). Genome sequencing and conservation genomics in the Scandinavian wolverine population. Conservation Biology: the Journal of the Society for Conservation Biology, 32(6), 1301-1312. https://doi.org/10.1111/cobi.13157
Ellerman, D. A., Pei, J., Gupta, S., Snell, W. J., Myles, D., & Primakoff, P. (2009). Izumo is part of a multiprotein family whose members form large complexes on mammalian sperm. Molecular Reproduction and Development, 76(12), 1188-1199. https://doi.org/10.1002/mrd.21092
Etherington, G. J., Heavens, D., Baker, D., Lister, A., McNelly, R., Garcia, G., Clavijo, B., Macaulay, I., Haerty, W., & Di Palma, F. (2020). Sequencing smart: De novo sequencing and assembly approaches for a non-model mammal. GigaScience, 9(5), https://doi.org/10.1093/gigascience/giaa045
Fahien, L. A., & Macdonald, M. J. (2011). The complex mechanism of glutamate dehydrogenase in insulin secretion. Diabetes, 60(10), 2450-2454. https://doi.org/10.2337/db10-1150
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. https://doi.org/10.1073/pnas.1921046117
Forde, N., Simintiras, C. A., Sturmey, R., Mamo, S., Kelly, A. K., Spencer, T. E., Bazer, F. W., & Lonergan, P. (2014). Amino acids in the uterine luminal fluid reflects the temporal changes in transporter expression in the endometrium and conceptus during early pregnancy in cattle. PLoS One, 9(6), e100010. https://doi.org/10.1371/journal.pone.0100010
Frith, M. C., & Kawaguchi, R. (2015). Split-alignment of genomes finds orthologies more accurately. Genome Biology, 16, 106. https://doi.org/10.1186/s13059-015-0670-9
Ge, S. X., Jung, D., & Yao, R. (2020). ShinyGO: a graphical gene-set enrichment tool for animals and plants. Bioinformatics, 36(8), 2628-2629. https://doi.org/10.1093/bioinformatics/btz931
Gosejacob, D., Jäger, P. S., Vom Dorp, K., Frejno, M., Carstensen, A. C., Köhnke, M., Degen, J., Dörmann, P., & Hoch, M. (2016). Ceramide synthase 5 is essential to maintain C16:0-ceramide pools and contributes to the development of diet-induced obesity. Journal of Biological Chemistry, 291(13), 6989-7003. https://doi.org/10.1074/jbc.M115.691212
Gurevich, A., Saveliev, V., Vyahhi, N., & Tesler, G. (2013). QUAST: quality assessment tool for genome assemblies. Bioinformatics, 29(8), 1072-1075. https://doi.org/10.1093/bioinformatics/btt086
Han, M. V., Thomas, G. W. C., Lugo-Martinez, J., & Hahn, M. W. (2013). Estimating gene gain and loss rates in the presence of error in genome assembly and annotation using CAFE 3. Molecular Biology and Evolution, 30(8), 1987-1997. https://doi.org/10.1093/molbev/mst100
Han, X., Jiang, T., Yu, L., Zeng, C., Fan, B., & Liu, B. (2012). Molecular characterization of the porcine MTPAP gene associated with meat quality traits: chromosome localization, expression distribution, and transcriptional regulation. Molecular and Cellular Biochemistry, 364(1-2), 173-180. https://doi.org/10.1007/s11010-011-1216-4
Harney, J. P., Ott, T. L., Geisert, R. D., & Bazer, F. W. (1993). Retinol-binding protein gene expression in cyclic and pregnant endometrium of pigs, sheep, and cattle. Biology of Reproduction, 49(5), 1066-1073.
Hecker, N., Sharma, V., & Hiller, M. (2019). Convergent gene losses illuminate metabolic and physiological changes in herbivores and carnivores. Proceedings of the National Academy of Sciences of the United States of America, 116(8), 3036-3041. https://doi.org/10.1073/pnas.1818504116
Heldstab, S. A., Müller, D. W. H., Graber, S. M., Bingaman Lackey, L., Rensch, E., Hatt, J.-M., Zerbe, P., & Clauss, M. (2018). Geographical origin, delayed implantation, and induced ovulation explain reproductive seasonality in the Carnivora. Journal of Biological Rhythms, 33(4), 402-419. https://doi.org/10.1177/0748730418773620
Hill, M., Pařízek, A., Kancheva, R., & Jirásek, J. E. (2011). Reduced progesterone metabolites in human late pregnancy. Physiological Research, 60(2), 225-241. https://doi.org/10.33549/physiolres.932077
Hron, T., Elleder, D., & Gifford, R. J. (2019). Deltaretroviruses have circulated since at least the Paleogene and infected a broad range of mammalian species. Retrovirology, 16(1), 33. https://doi.org/10.1186/s12977-019-0495-9
Inman, R. M., Magoun, A. J., Persson, J., & Mattisson, J. (2012). The wolverine’s niche: Linking reproductive chronology, caching, competition, and climate. Journal of Mammalogy, 93(3), 634-644. https://doi.org/10.1644/11-MAMM-A-319.1
Inoue, K., Maeda, N., Mori, T., Sekimoto, R., Tsushima, Y., Matsuda, K., Yamaoka, M., Suganami, T., Nishizawa, H., Ogawa, Y., Funahashi, T., & Shimomura, I. (2014). Possible involvement of Opa-interacting protein 5 in adipose proliferation and obesity. PLoS One, 9(2), e87661. https://doi.org/10.1371/journal.pone.0087661
Jeffares, D. C., Jolly, C., Hoti, M., Speed, D., Shaw, L., Rallis, C., Balloux, F., Dessimoz, C., Bähler, J., & Sedlazeck, F. J. (2017). Transient structural variations have strong effects on quantitative traits and reproductive isolation in fission yeast. Nature Communications, 8, 14061. https://doi.org/10.1038/ncomms14061
Jewgenow, K., Goeritz, F., Neubauer, K., Fickel, J., & Naidenko, S. V. (2006). Characterization of reproductive activity in captive male Eurasian lynx (Lynx lynx). European Journal of Wildlife Research, 52(1), 34-38. https://doi.org/10.1007/s10344-005-0002-6
Johnson, R. J., & Andrews, P. (2010). Fructose, uricase, and the back-to-Africa hypothesis. Evolutionary Anthropology, 19(6), 250-257. https://doi.org/10.1002/evan.20266
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A., & Jermiin, L. S. (2017). ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14(6), 587-589. https://doi.org/10.1038/nmeth.4285
Kashtanov, S. N., Svischeva, G. R., Pishchulina, S. L., Lazebny, O. E., Meshchersky, I. G., Simakin, L. V., & Rozhnov, V. V. (2015). Geographical structure of the sable (Martes zibellina L.) gene pool on the basis of microsatellite loci analysis. Russian Journal of Genetics, 51(1), 69-79.
Kassal, B. Y., & Sidorov, G. N. (2013). Distribution of the sable (Martes zibellina) and the pine marten (Martes martes) in Omsk Oblast and biogeographic effects of their hybridization. Russian Journal of Biological Invasions, 4(2), 105-115. https://doi.org/10.1134/S2075111713020070
Kim, B.-M., Lee, Y. J., Kim, J.-H., Kim, J.-H., Kang, S., Jo, E., Lee, S. J., Lee, J. H., Chi, Y. M., & Park, H. (2020). The genome assembly and annotation of the southern elephant seal Mirounga leonina. Genes, 11(2), https://doi.org/10.3390/genes11020160
Koepfli, K.-P., Deere, K. A., Slater, G. J., Begg, C., Begg, K., Grassman, L., Lucherini, M., Veron, G., & Wayne, R. K. (2008). Multigene phylogeny of the Mustelidae: Resolving relationships, tempo and biogeographic history of a mammalian adaptive radiation. BMC Biology, 6, 10. https://doi.org/10.1186/1741-7007-6-10
Kosiol, C., Vinar, T., da Fonseca, R. R., Hubisz, M. J., Bustamante, C. D., Nielsen, R., & Siepel, A. (2008). Patterns of positive selection in six Mammalian genomes. PLoS Genetics, 4(8), e1000144. https://doi.org/10.1371/journal.pgen.1000144
Krebs, J., Lofroth, E., Copeland, J., Banci, V., Cooley, D., Golden, H., Magoun, A., Mulders, R., & Shults, B. (2004). Synthesis of survival rates and causes of mortality in North American wolverines. Journal of Wildlife Management, 68(3), 493-502.
Kriventseva, E. V., Kuznetsov, D., Tegenfeldt, F., Manni, M., Dias, R., Simão, F. A., & Zdobnov, E. M. (2019). OrthoDB v10: sampling the diversity of animal, plant, fungal, protist, bacterial and viral genomes for evolutionary and functional annotations of orthologs. Nucleic Acids Research, 47(D1), D807-D811. https://doi.org/10.1093/nar/gky1053
Kronenberg, Z. N., Osborne, E. J., Cone, K. R., Kennedy, B. J., Domyan, E. T., Shapiro, M. D., Elde, N. C., & Yandell, M. (2015). Wham: Identifying structural variants of biological consequence. PLoS Computational Biology, 11(12), e1004572. https://doi.org/10.1371/journal.pcbi.1004572
Langmead, B., & Salzberg, S. L. (2012). Fast gapped-read alignment with Bowtie2. Nature Methods, 9(4), 357-359. https://doi.org/10.1038/nmeth.1923
Larivière, S., & Ferguson, S. H. (2003). Evolution of induced ovulation in North American Carnivores. Journal of Mammalogy, 84(3), 937-947. https://doi.org/10.1644/BME-003
Law, C. J., Slater, G. J., & Mehta, R. S. (2018). Lineage diversity and size disparity in Musteloidea: Testing patterns of adaptive radiation using molecular and fossil-based methods. Systematic Biology, 67(1), 127-144. https://doi.org/10.1093/sysbio/syx047
Layer, R. M., Chiang, C., Quinlan, A. R., & Hall, I. M. (2014). LUMPY: A probabilistic framework for structural variant discovery. Genome Biology, 15(6), R84. https://doi.org/10.1186/gb-2014-15-6-r84
Lee, J.-E., Oh, H.-A., Song, H., Jun, J. H., Roh, C.-R., Xie, H., Dey, S. K., & Lim, H. J. (2011). Autophagy regulates embryonic survival during delayed implantation. Endocrinology, 152(5), 2067-2075. https://doi.org/10.1210/en.2010-1456
Lennox, A. R., & Goodship, A. E. (2008). Polar bears (Ursus maritimus), the most evolutionary advanced hibernators, avoid significant bone loss during hibernation. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 149(2), 203-208. https://doi.org/10.1016/j.cbpa.2007.11.012
Lewin, H. A., Graves, J. A. M., Ryder, O. A., Graphodatsky, A. S., & O’Brien, S. J. (2019). Precision nomenclature for the new genomics. GigaScience, 8(8), https://doi.org/10.1093/gigascience/giz086
Li, B., Wolsan, M., Wu, D., Zhang, W., Xu, Y., & Zeng, Z. (2014). Mitochondrial genomes reveal the pattern and timing of marten (Martes), wolverine (Gulo), and fisher (Pekania) diversification. Molecular Phylogenetics and Evolution, 80, 156-164. https://doi.org/10.1016/j.ympev.2014.08.002
Li, H., & Durbin, R. (2011). Inference of human population history from individual whole-genome sequences. Nature, 475(7357), 493-496.
Lim, H. J., & Song, H. (2014). Evolving tales of autophagy in early reproductive events. The International Journal of Developmental Biology, 58(2-4), 183-187. https://doi.org/10.1387/ijdb.130337hl
Liu, G., Zhao, C., Xu, D., Zhang, H., Monakhov, V., Shang, S., Gao, X., Sha, W., Ma, J., Zhang, W., Tang, X., Li, B., Hua, Y., Cao, X., Liu, Z., & Zhang, H. (2020). First draft genome of the sable, Martes zibellina. Genome Biology and Evolution, 12(3), 59-65. https://doi.org/10.1093/gbe/evaa029
Lopes, F. L., Desmarais, J., Gevry, N. Y., Ledoux, S., & Murphy, B. D. (2003). Expression of vascular endothelial growth factor isoforms and receptors Flt-1 and KDR during the peri-implantation period in the mink, Mustela vison. Biology of Reproduction, 68(5), 1926-1933.
Löytynoja, A. (2014). Phylogeny-aware alignment with PRANK. Methods in Molecular Biology, 1079, 155-170.
Lynch, M., & Conery, J. S. (2000). The evolutionary fate and consequences of duplicate genes [Review of The evolutionary fate and consequences of duplicate genes]. Science, 290(5494), 1151-1155.
Maglott, D., Ostell, J., Pruitt, K. D., & Tatusova, T. (2011). Entrez Gene: Gene-centered information at NCBI. Nucleic Acids Research, 39(Database issue), D52-D57. https://doi.org/10.1093/nar/gkq1237
Martinez, B., & Ortiz, R. M. (2017). Thyroid hormone regulation and insulin resistance: Insights from animals naturally adapted to fasting. Physiology, 32(2), 141-151. https://doi.org/10.1152/physiol.00018.2016
McGee-Lawrence, M., Buckendahl, P., Carpenter, C., Henriksen, K., Vaughan, M., & Donahue, S. (2015). Suppressed bone remodeling in black bears conserves energy and bone mass during hibernation. The Journal of Experimental Biology, 218(Pt 13), 2067-2074. https://doi.org/10.1242/jeb.120725
McLaren, W., Gil, L., Hunt, S. E., Riat, H. S., Ritchie, G. R. S., Thormann, A., Flicek, P., & Cunningham, F. (2016). The Ensembl variant effect predictor. Genome Biology, 17(1), 122. https://doi.org/10.1186/s13059-016-0974-4
McNutt, J. W., Groom, R., & Woodroffe, R. (2019). Ambient temperature provides an adaptive explanation for seasonal reproduction in a tropical mammal. Journal of Zoology, 309(3), 153-160. https://doi.org/10.1111/jzo.12712
Mead, R. A. (1981). Delayed implantation in mustelids, with special emphasis on the spotted skunk. Journal of Reproduction and Fertility 29, 11-24.
Mead, R. A. (1989). The physiology and evolution of delayed implantation in carnivores. In J. L. Gittleman (Ed.), Carnivore behavior, ecology, and evolution (pp. 437-464). Springer US.
Mendes, F. K., & Hahn, M. W. (2016). Gene tree discordance causes apparent substitution rate variation. Systematic Biology, 65(4), 711-721. https://doi.org/10.1093/sysbio/syw018
Mérot, C., Oomen, R. A., Tigano, A., & Wellenreuther, M. (2020). A roadmap for understanding the evolutionary significance of structural genomic variation. Trends in Ecology & Evolution, 35(7), 561-572. https://doi.org/10.1016/j.tree.2020.03.002
Minh, B. Q., Hahn, M. W., & Lanfear, R. (2020). New methods to calculate concordance factors for phylogenomic datasets. Molecular Biology and Evolution, 37(9), 2727-2733. https://doi.org/10.1093/molbev/msaa106
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. https://doi.org/10.1093/molbev/msaa015
Miranda, I., Giska, I., Farelo, L., Pimenta, J., Zimova, M., Bryk, J., Dalén, L., Mills, L. S., Zub, K., & Melo-Ferreira, J. (2021). Museomics dissects the genetic basis for adaptive seasonal colouration in the least weasel. Molecular Biology and Evolution, 38(10), 4388-4402. https://doi.org/10.1093/molbev/msab177
Mizuarai, S., Miki, S., Araki, H., Takahashi, K., & Kotani, H. (2005). Identification of dicarboxylate carrier Slc25a10 as malate transporter in de novo fatty acid synthesis. Journal of Biological Chemistry, 280(37), 32434-32441. https://doi.org/10.1074/jbc.M503152200
Monakhov, V. G. (2011). Martes zibellina (Carnivora: Mustelidae). Mammalian Species, 43(876), 75-86. https://doi.org/10.1644/876.1
Montaseri, A., Giampietri, C., Rossi, M., Riccioli, A., Del Fattore, A., & Filippini, A. (2020). The role of autophagy in osteoclast differentiation and bone resorption function. Biomolecules, 10(10), https://doi.org/10.3390/biom10101398
Morales-Simfors, N., Bundschuh, J., Herath, I., Inguaggiato, C., Caselli, A. T., Tapia, J., Choquehuayta, F. E. A., Armienta, M. A., Ormachea, M., Joseph, E., & López, D. L. (2020). Arsenic in Latin America: A critical overview on the geochemistry of arsenic originating from geothermal features and volcanic emissions for solving its environmental consequences. Science of the Total Environment, 716, 135564. https://doi.org/10.1016/j.scitotenv.2019.135564
Mustonen, A.-M., Käkelä, R., Käkelä, A., Pyykönen, T., Aho, J., & Nieminen, P. (2007). Lipid metabolism in the adipose tissues of a carnivore, the raccoon dog, during prolonged fasting. Experimental Biology and Medicine, 232(1), 58-69.
Mustonen, A.-M., Puukka, M., Saarela, S., Paakkonen, T., Aho, J., & Nieminen, P. (2006). Adaptations to fasting in a terrestrial mustelid, the sable (Martes zibellina). Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 144(4), 444-450. https://doi.org/10.1016/j.cbpa.2006.03.008
Nelson, D. W. M., Crossland, M. R., & Shine, R. (2011). Foraging responses of predators to novel toxic prey: effects of predator learning and relative prey abundance. Oikos, 120(1), 152-158. https://doi.org/10.1111/j.1600-0706.2010.18736.x
Nielsen, R., Bustamante, C., Clark, A. G., Glanowski, S., Sackton, T. B., Hubisz, M. J., Fledel-Alon, A., Tanenbaum, D. M., Civello, D., White, T. J., J. Sninsky, J., Adams, M. D., & Cargill, M. (2005). A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biology, 3(6), e170. https://doi.org/10.1371/journal.pbio.0030170
Nieminen, P., Käkelä, R., Pyykönen, T., & Mustonen, A.-M. (2006). Selective fatty acid mobilization in the American mink (Mustela vison) during food deprivation. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology, 145(1), 81-93. https://doi.org/10.1016/j.cbpb.2006.06.007
Nieminen, P., & Mustonen, A.-M. (2007). Uniform fatty acid mobilization from anatomically distinct fat depots in the sable (Martes zibellina). Lipids, 42(7), 659-669. https://doi.org/10.1007/s11745-007-3061-5
O’Brien, S. J., Graphodatsky, A. S., & Perelman, P. L. (2020). Atlas of mammalian chromosomes. John Wiley & Sons.
Okamoto, T., Imaizumi, K., & Kaneko, M. (2020). The role of tissue-specific ubiquitin ligases, RNF183, RNF186, RNF182 and RNF152, in disease and biological function. International Journal of Molecular Sciences, 21(11), https://doi.org/10.3390/ijms21113921
Olson, M. V. (1999). When less is more: gene loss as an engine of evolutionary change. American Journal of Human Genetics, 64(1), 18-23. https://doi.org/10.1086/302219
Pacifici, M., Santini, L., Di Marco, M., Baisero, D., Francucci, L., Grottolo Marasini, G., Visconti, P., & Rondinini, C. (2013). Generation length for mammals. Nature Conservation, 5, 89-94. https://doi.org/10.3897/natureconservation.5.5734
Papin, C., Rouget, C., Lorca, T., Castro, A., & Mandart, E. (2004). XCdh1 is involved in progesterone-induced oocyte maturation. Developmental Biology, 272(1), 66-75. https://doi.org/10.1016/j.ydbio.2004.04.018
Pasitschniak-Arts, M., & Larivière, S. (1995). Gulo gulo. Mammalian Species, 499, 1-10.
Peng, C., Niu, L., Deng, J., Yu, J., Zhang, X., Zhou, C., Xing, J., & Li, J. (2018). Can-SINE dynamics in the giant panda and three other Caniformia genomes. Mobile DNA, 9, 32. https://doi.org/10.1186/s13100-018-0137-0
Peng, X., Alföldi, J., Gori, K., Eisfeld, A. J., Tyler, S. R., Tisoncik-Go, J., Brawand, D., Law, G. L., Skunca, N., Hatta, M., Gasper, D. J., Kelly, S. M., Chang, J., Thomas, M. J., Johnson, J., Berlin, A. M., Lara, M., Russell, P., Swofford, R., … Katze, M. G. (2014). The draft genome sequence of the ferret (Mustela putorius furo) facilitates study of human respiratory disease. Nature Biotechnology, 32(12), 1250-1255. https://doi.org/10.1038/nbt.3079
Plummer, M., Best, N., Cowles, K., & Vines, K. (2006). CODA: convergence diagnosis and output analysis for MCMC. R News, 6(1), 7-11.
Poglayen-Neuwall, I., Durrant, B. S., Swansen, M. L., Williams, R. C., & Barnes, R. A. (1989). Estrous cycle of the tayra, Eira barbara. Zoo Biology, 8(2), 171-177. https://doi.org/10.1002/zoo.1430080208
Poon, C. E., Lecce, L., Day, M. L., & Murphy, C. R. (2014). Mucin 15 is lost but mucin 13 remains in uterine luminal epithelial cells and the blastocyst at the time of implantation in the rat. Reproduction, Fertility, and Development, 26(3), 421-431. https://doi.org/10.1071/RD12313
Poplin, R., Ruano-Rubio, V., DePristo, M. A., Fennell, T. J., Carneiro, M. O., Van der Auwera, G. A., Kling, D. E., Gauthier, L. D., Levy-Moonshine, A., Roazen, D., Shakir, K., Thibault, J., Chandran, S., Whelan, C., Lek, M., Gabriel, S., Daly, M. J., Neale, B., MacArthur, D. G., & Banks, E. (2018). Scaling accurate genetic variant discovery to tens of thousands of samples. bioRxiv, 201178. https://doi.org/10.1101/201178
Porubsky, D., Sanders, A. D., Höps, W., Hsieh, P., Sulovari, A., Li, R., Mercuri, L., Sorensen, M., Murali, S. C., Gordon, D., Cantsilieris, S., Pollen, A. A., Ventura, M., Antonacci, F., Marschall, T., Korbel, J. O., & Eichler, E. E. (2020). Recurrent inversion toggling and great ape genome evolution. Nature Genetics, 52(8), 849-858. https://doi.org/10.1038/s41588-020-0646-x
Proulx, G., & Aubry, K. B. (2017). The Martes complex: A monophyletic clade that shares many life-history traits and conservation challenges. In: G. Proulx (Ed.). The Martes Complex in the 21st Century: ecology and conservation (pp. 3-24). Mammal Research Institute, Polish Academy of Sciences.
Ranwez, V., Harispe, S., Delsuc, F., & Douzery, E. J. P. (2011). MACSE: Multiple alignment of coding SEquences accounting for frameshifts and stop codons. PLoS One, 6(9), e22594. https://doi.org/10.1371/journal.pone.0022594
Reis, A., Chang, H.-Y., Levasseur, M., & Jones, K. T. (2006). APCcdh1 activity in mouse oocytes prevents entry into the first meiotic division. Nature Cell Biology, 8(5), 539-540. https://doi.org/10.1038/ncb1406
Ren, X., Aleshin, M., Jo, W. J., Dills, R., Kalman, D. A., Vulpe, C. D., Smith, M. T., & Zhang, L. (2011). Involvement of N-6 adenine-specific DNA methyltransferase 1 (N6AMT1) in arsenic biomethylation and its role in arsenic-induced toxicity. Environmental Health Perspectives, 119(6), 771-777.
Reynolds, A., Qiao, H., Yang, Y., Chen, J. K., Jackson, N., Biswas, K., Holloway, J. K., Baudat, F., de Massy, B., Wang, J., Höög, C., Cohen, P. E., & Hunter, N. (2013). RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis. Nature Genetics, 45(3), 269-278. https://doi.org/10.1038/ng.2541
Rinker, D. C., Specian, N. K., Zhao, S., & Gibbons, J. G. (2019). Polar bear evolution is marked by rapid changes in gene copy number in response to dietary shift. Proceedings of the National Academy of Sciences of the United States of America, 116(27), 13446-13451. https://doi.org/10.1073/pnas.1901093116
Sato, J. J., Wolsan, M., Prevosti, F. J., D’Elía, G., Begg, C., Begg, K., Hosoda, T., Campbell, K. L., & Suzuki, H. (2012). Evolutionary and biogeographic history of weasel-like carnivorans (Musteloidea). Molecular Phylogenetics and Evolution, 63(3), 745-757. https://doi.org/10.1016/j.ympev.2012.02.025
Sayyari, E., & Mirarab, S. (2016). Fast coalescent-based computation of local branch support from quartet frequencies. Molecular Biology and Evolution, 33(7), 1654-1668. https://doi.org/10.1093/molbev/msw079
Schweitzer, L. D., Comb, W. C., Bar-Peled, L., & Sabatini, D. M. (2015). Disruption of the rag-ragulator complex by c17orf59 inhibits mTORC1. Cell Reports, 12(9), 1445-1455. https://doi.org/10.1016/j.celrep.2015.07.052
Serão, N. V. L., Veroneze, R., Ribeiro, A. M. F., Verardo, L. L., Braccini Neto, J., Gasparino, E., Campos, C. F., Lopes, P. S., & Guimarães, S. E. F. (2011). Candidate gene expression and intramuscular fat content in pigs. Journal of Animal Breeding and Genetics, 128(1), 28-34. https://doi.org/10.1111/j.1439-0388.2010.00887.x
Shi, G., Xing, L., Liu, Z., Qu, Z., Wu, X., Dong, Z., Wang, X., Gao, X., Huang, M., Yan, J., Yang, L., Liu, Y., Ptácek, L. J., & Xu, Y. (2013). Dual roles of FBXL3 in the mammalian circadian feedback loops are important for period determination and robustness of the clock. Proceedings of the National Academy of Sciences of the United States of America, 110(12), 4750-4755. https://doi.org/10.1073/pnas.1302560110
Shumate, A., & Salzberg, S. L. (2020). Liftoff: an accurate gene annotation mapping tool. https://doi.org/10.1101/2020.06.24.169680
Siepka, S. M., Yoo, S.-H., Park, J., Song, W., Kumar, V., Hu, Y., Lee, C., & Takahashi, J. S. (2007). Circadian mutant Overtime reveals F-box protein FBXL3 regulation of cryptochrome and period gene expression. Cell, 129(5), 1011-1023. https://doi.org/10.1016/j.cell.2007.04.030
Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V., & Zdobnov, E. M. (2015). BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics, 31(19), 3210-3212. https://doi.org/10.1093/bioinformatics/btv351
Singh, B. N., Gong, W., Das, S., Theisen, J. W. M., Sierra-Pagan, J. E., Yannopoulos, D., Skie, E., Shah, P., Garry, M. G., & Garry, D. J. (2019). Etv2 transcriptionally regulates Yes1 and promotes cell proliferation during embryogenesis. Scientific Reports, 9(1), 9736. https://doi.org/10.1038/s41598-019-45841-5
Smit, A. F. A. (2004). Repeat-masker open-3.0. http://www.repeatmasker.org and https://ci.nii.ac.jp/naid/10029514778/
Soley, F. G., & Alvarado-Díaz, I. (2011). Prospective thinking in a mustelid? Eira barbara (Carnivora) cache unripe fruits to consume them once ripened. Die Naturwissenschaften, 98(8), 693-698. https://doi.org/10.1007/s00114-011-0821-0
Sonna, L. A., Fujita, J., Gaffin, S. L., & Lilly, C. M. (2002). Invited review: Effects of heat and cold stress on mammalian gene expression. Journal of Applied Physiology, 92(4), 1725-1742. https://doi.org/10.1152/japplphysiol.01143.2001
Subramanian, A. R., Kaufmann, M., & Morgenstern, B. (2008). DIALIGN-TX: greedy and progressive approaches for segment-based multiple sequence alignment. Algorithms for Molecular Biology, 3, 6. https://doi.org/10.1186/1748-7188-3-6
Svishcheva, G. R., & Kashtanov, S. N. (2011). Reproductive strategy of the sable (Martes zibellina Linnaeus, 1758): An analysis of litter size inheritance in farm-raised populations. Russian Journal of Genetics: Applied Research, 1(3), 221-225. https://doi.org/10.1134/S2079059711030129
Tavori, H., Rashid, S., & Fazio, S. (2015). On the function and homeostasis of PCSK9: Reciprocal interaction with LDLR and additional lipid effects. Atherosclerosis, 238(2), 264-270. https://doi.org/10.1016/j.atherosclerosis.2014.12.017
The UniProt Consortium (2017). UniProt: the universal protein knowledgebase. Nucleic Acids Research, 45(D1), D158-D169.
Thomas, J. H. (2007). Rapid birth-death evolution specific to xenobiotic cytochrome P450 genes in vertebrates. PLoS Genetics, 3(5), e67. https://doi.org/10.1371/journal.pgen.0030067
Tigano, A., Colella, J. P., & MacManes, M. D. (2020). Comparative and population genomics approaches reveal the basis of adaptation to deserts in a small rodent. Molecular Ecology, 29(7), 1300-1314. https://doi.org/10.1111/mec.15401
Totikov, A., Tomarovsky, A., Prokopov, D., Yakupova, A., Bulyonkova, T., Derezanin, L., Rasskazov, D., Wolfsberger, W. W., Koepfli, K.-P., Oleksyk, T. K., & Kliver, S. (2021). Chromosome-level genome assemblies expand capabilities of genomics for conservation biology. Genes, 12(9), 1336. https://doi.org/10.3390/genes12091336
Viscarra, J. A., Rodriguez, R., Vazquez-Medina, J. P., Lee, A., Tift, M. S., Tavoni, S. K., Crocker, D. E., & Ortiz, R. M. (2013). Insulin and GLP-1 infusions demonstrate the onset of adipose-specific insulin resistance in a large fasting mammal: Potential glucogenic role for GLP-1. Physiological Reports, 1(2), e00023. https://doi.org/10.1002/phy2.23
Wang, J., Lu, Z.-X., Tokheim, C. J., Miller, S. E., & Xing, Y. (2015). Species-specific exon loss in human transcriptomes. Molecular Biology and Evolution, 32(2), 481-494. https://doi.org/10.1093/molbev/msu317
Webb, J. K., Brown, G. P., Child, T., Greenlees, M. J., Phillips, B. L., & Shine, R. (2008). A native dasyurid predator (common planigale, Planigale maculata) rapidly learns to avoid a toxic invader. Austral Ecology, 33(7), 821-829.
Weischenfeldt, J., Symmons, O., Spitz, F., & Korbel, J. O. (2013). Phenotypic impact of genomic structural variation: Insights from and for human disease. Nature Reviews. Genetics, 14(2), 125-138. https://doi.org/10.1038/nrg3373
Weisenfeld, N. I., Kumar, V., Shah, P., Church, D. M., & Jaffe, D. B. (2017). Direct determination of diploid genome sequences. Genome Research, 27(5), 757-767. https://doi.org/10.1101/gr.214874.116
Weissensteiner, M. H., Bunikis, I., Catalán, A., Francoijs, K.-J., Knief, U., Heim, W., Peona, V., Pophaly, S. D., Sedlazeck, F. J., Suh, A., Warmuth, V. M., & Wolf, J. B. W. (2020). Discovery and population genomics of structural variation in a songbird genus. Nature Communications, 11(1), 3403. https://doi.org/10.1038/s41467-020-17195-4
Wellenreuther, M., & Bernatchez, L. (2018). Eco-evolutionary genomics of chromosomal inversions. Trends in Ecology & Evolution, 33(6), 427-440. https://doi.org/10.1016/j.tree.2018.04.002
Wilcox, A., Katsanakis, K. D., Bheda, F., & Pillay, T. S. (2004). Asb6, an adipocyte-specific ankyrin and SOCS box protein, interacts with APS to enable recruitment of elongins B and C to the insulin receptor signaling complex. Journal of Biological Chemistry, 279(37), 38881-38888. https://doi.org/10.1074/jbc.M406101200
Wilson, D. E., Mittermeier, R. A. (2009). Family Mustelidae. In: Handbook of the mammals of the world (vol. 1, pp. 627-637). Lynx Editions.
Wu, X., Quondamatteo, F., Lefever, T., Czuchra, A., Meyer, H., Chrostek, A., Paus, R., Langbein, L., & Brakebusch, C. (2006). Cdc42 controls progenitor cell differentiation and beta-catenin turnover in skin. Genes & Development, 20(5), 571-585.
Wu, Z., Latendorf, T., Meyer-Hoffert, U., & Schröder, J.-M. (2011). Identification of trichohyalin-like 1, an s100 fused-type protein selectively expressed in hair follicles. Journal of Investigative Dermatology, 131(8), 1761-1763. https://doi.org/10.1038/jid.2011.71
Xing, Y., & Lee, C. (2006). Alternative splicing and RNA selection pressure-evolutionary consequences for eukaryotic genomes. Nature Reviews. Genetics, 7(7), 499-509. https://doi.org/10.1038/nrg1896
Yang, Z. (2007). PAML 4: Phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24(8), 1586-1591. https://doi.org/10.1093/molbev/msm088
Yu, Y.-H., Chang, Y.-C., Su, T.-H., Nong, J.-Y., Li, C.-C., & Chuang, L.-M. (2013). Prostaglandin reductase-3 negatively modulates adipogenesis through regulation of PPARγ activity. Journal of Lipid Research, 54(9), 2391-2399. https://doi.org/10.1194/jlr.M037556
Zhang, C., Rabiee, M., Sayyari, E., & Mirarab, S. (2018). ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics, 19(Suppl 6), 153. https://doi.org/10.1186/s12859-018-2129-y
Zhang, H., Ge, Y., He, P., Chen, X., Carina, A., Qiu, Y., Aga, D. S., & Ren, X. (2015). Interactive effects of N6AMT1 and As3MT in arsenic biomethylation. Toxicological Sciences: An Official Journal of the Society of Toxicology, 146(2), 354-362. https://doi.org/10.1093/toxsci/kfv101
Zhang, J. (2003). Evolution by gene duplication: an update. Trends in Ecology & Evolution, 18(6), 292-298. https://doi.org/10.1016/S0169-5347(03)00033-8
Zhang, J., Nielsen, R., & Yang, Z. (2005). Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Molecular Biology and Evolution, 22(12), 2472-2479. https://doi.org/10.1093/molbev/msi237
Zhang, Z., Li, J., Zhao, X.-Q., Wang, J., Wong, G.-K.-S., & Yu, J. (2006). KaKs_Calculator: Calculating Ka and Ks through model selection and model averaging. Genomics, Proteomics & Bioinformatics, 4(4), 259-263. https://doi.org/10.1016/S1672-0229(07)60007-2
Zhou, Y.-B., Newman, C., Xu, W.-T., Buesching, C. D., Zalewski, A., Kaneko, Y., Macdonald, D. W., & Xie, Z.-Q. (2011). Biogeographical variation in the diet of Holarctic martens (genus Martes, Mammalia: Carnivora: Mustelidae): adaptive foraging in generalists. Journal of Biogeography, 38(1), 137-147. https://doi.org/10.1111/j.1365-2699.2010.02396.x

Auteurs

Lorena Derežanin (L)

Leibniz Institute for Zoo and Wildlife Research (IZW), Berlin, Germany.

Asta Blažytė (A)

Department of Biomedical Engineering, College of Information and Biotechnology, Ulsan National Institute of Science and Technology (UNIST), Ulsan, Korea.

Pavel Dobrynin (P)

Computer Technologies Laboratory, ITMO University, Saint Petersburg, Russia.

David A Duchêne (DA)

Center for Evolutionary Hologenomics, The GLOBE Institute, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.

José Horacio Grau (JH)

Amedes Genetics, amedes Medizinische Dienstleistungen GmbH, Berlin, Germany.

Sungwon Jeon (S)

Department of Biomedical Engineering, College of Information and Biotechnology, Ulsan National Institute of Science and Technology (UNIST), Ulsan, Korea.

Sergei Kliver (S)

Institute of Molecular and Cellular Biology, SB RAS, Novosibirsk, Russia.

Klaus-Peter Koepfli (KP)

Computer Technologies Laboratory, ITMO University, Saint Petersburg, Russia.
Smithsonian-Mason School of Conservation, Front Royal, Virginia, USA.
Center for Species Survival, Smithsonian Conservation Biology Institute, National Zoological Park, Front Royal, Virginia, USA.

Dorina Meneghini (D)

Leibniz Institute for Zoo and Wildlife Research (IZW), Berlin, Germany.

Michaela Preick (M)

Institute for Biochemistry and Biology, Faculty of Mathematics and Natural Sciences, University of Potsdam, Potsdam OT Golm, Germany.

Andrey Tomarovsky (A)

Computer Technologies Laboratory, ITMO University, Saint Petersburg, Russia.
Institute of Molecular and Cellular Biology, SB RAS, Novosibirsk, Russia.
Novosibirsk State University, Novosibirsk, Russia.

Azamat Totikov (A)

Computer Technologies Laboratory, ITMO University, Saint Petersburg, Russia.
Institute of Molecular and Cellular Biology, SB RAS, Novosibirsk, Russia.
Novosibirsk State University, Novosibirsk, Russia.

Jörns Fickel (J)

Leibniz Institute for Zoo and Wildlife Research (IZW), Berlin, Germany.
Institute for Biochemistry and Biology, Faculty of Mathematics and Natural Sciences, University of Potsdam, Potsdam OT Golm, Germany.

Daniel W Förster (DW)

Leibniz Institute for Zoo and Wildlife Research (IZW), Berlin, Germany.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH