Estimation of the congruence between morphogenetic and molecular-genetic modules of gray voles Microtus S.L. variability along a climatic gradient

Cover Page

Cite item

Full Text

Abstract

Background. The exponential growth of research concerning a role of morphological modularity and integration in evolution has taking place from the beginning of the century. It was especially noted that inter-level integration should manifest itself, first of all, in the congruent variability of the modules of different structural levels. We analyzed congruence between the interspecific variability of the first lower molar (m1) masticatory surface and the mtDNA Cytb gene in ten species of the gray voles Microtus s.l. from the point of view of the modular organization.

Materials and methods. In total, 5306 pairs of chewing surface contours of vole molar m1 were investigated. Thirty one different morphotypes and 187 their different combinations are identified: 30 – symmetric and 157 – asymmetric. 576 sequences of the Cytb mtDNA gene from the GenBank database are used. Climatic data are taken from the website Climate:Date.org. Data are processed using a DJ-method. The morphogenetic matrix of Euclidean distances between species is obtained from the frequencies of m1 morphotypes co-occurrence from the right and left sides of the lower jaw, and the molecular-genetic one from the frequencies of synonymous codon substitutions. The algorithm is realized in the Jacobi 4 package.

Results. A high correlation (r = 0.847) between the first principal component of the molecular-genetic distance matrix and second principal component of the morphogenetic one is found. From the standpoint of the modular organization of the phenotype, the principal components of these matrices are treated as variability modules. The molecular-genetic module is caused by change of frequencies of the codons ACC and GCA along geo-climatic gradient, and morphogenetic one – various aspects of the m1 asymmetry.

Conclusions. The proposed approach allowed to identify two congruently varying modules from different trait systems of the studied species along the geo-climatic gradient.

About the authors

Vera Yu. Kovaleva

Federal Institute of Systematics and Ecology of Animals of the Siberian Branch of the Russian Academy of Sciences

Author for correspondence.
Email: vkova@ngs.ru
ORCID iD: 0000-0003-1685-4820

DSc, Sen Sci Res, Laboratory of Animal Ecology

Russian Federation, 11, Frunze street, Novosibirsk, 630091

Alexandr A. Pozdnyakov

Federal Institute of Systematics and Ecology of Animals of the Siberian Branch of the Russian Academy of Sciences

Email: al_ap@mail.ru

PhD, Sen Sci Res, Laboratory of Animal Ecology

Russian Federation, 11, Frunze street, Novosibirsk, 630091

Yuri N. Litvinov

Federal Institute of Systematics and Ecology of Animals of the Siberian Branch of the Russian Academy of Sciences

Email: Lyun13@yandex.ru

DSc, Deputy Director, Laboratory of Animal Ecology

Russian Federation, 11, Frunze street, Novosibirsk, 630091

Vadim M. Efimov

Federal Institute of Systematics and Ecology of Animals of the Siberian Branch of the Russian Academy of Sciences; Novosibirsk State University; Tomsk State University

Email: vmefimov@ngs.ru

DSc, Prof. of Cytology and Genetics Department; Prof. of Vertebrate Zoology and Ecology Department

Russian Federation, 11, Frunze street, Novosibirsk, 630091; 1, Pirogova street, Novosibirsk, 630090; 34a, Lenina prospect, Tomsk, 634050

References

  1. Ратнер В.А. Внешние и внутренние факторы и ограничения молекулярной эволюции // Современные проблемы теории эволюции / Под ред. Л.П. Татаринова. – М.: Наука; 1993. – С. 60–80. [Ratner VA. Vneshnie i vnutrennie faktory i ogranicheniya molekulyarnoi evolyutsii. In: Sovremennye problemy teorii evolyutsii. Ed by L.P. Tatarinov. Moscow: Nauka; 1993. P. 60-80. (In Russ.)]
  2. Wagner GP, Altenberg L. Complex adaptations and the evolution of evolvability. Evolution. 1996;50(3):967-76. https://doi.org/10.2307/2410639.
  3. Pigliucci M. Phenotypic integration: studying the ecology and evolution of complex phenotypes. Ecol Lett. 2003;6(3):265-272. https://doi.org/10.1046/j.1461-0248.2003.00428.x.3.
  4. Инге-Вечтомов С.Г. Поиски периодической системы... в эволюции // Наука из первых рук. – 2004. – № 2. – С. 20–25. [Inge-Vechtomov SG. Poiski periodicheskoi sistemy… w ehwolucii. Nauka iz pervykh ruk. 2004;(2):20-25. (In Russ.)]
  5. Winther RG. Evolutionary developmental biology meets levels of selection: modular integration or competition, or both? In: Modularity: understanding the development and evolution of natural complex systems. Ed. by W. Callebaut, D. Rasskin-Gutman, H.A. Simon. The Vienna Ser. in Theoretical biology. Cambridge: MIT Press; 2005. P. 61-90.
  6. Klingenberg CP. Morphological integration and developmental modularity. Annu Rev Ecol Evol Syst. 2008;39:115-132. https://doi.org/10.1146/annurev.ecolsys.37.091305.110054.
  7. Суслов В.В., Колчанов Н.А. Дарвиновская эволюция и регуляторные генетические системы // Информационный вестник ВОГиС. – 2009. – Т. 13. – № 2. – С. 410–439. [Suslov VV. Kolchanov NA. Darwinian evolution and regulatory gene structure. Informatsionnyi vestnik VOGiS. 2009;13(2):410-439. (In Russ.)]
  8. Esteve-Altava B. In search of morphological modules: a systematic review. Biol Rev Camb Philos Soc. 2017;92(3):1332-1347. https://doi.org/10.1111/brv.12284.
  9. Klingenberg CP. Integration, modules, and development: molecules to morphology to evolution. In: Phenotypic integration: studying the ecology and evolution of complex phenotypes. Ed by M. Pigliucci, K. Preston. New York: Oxford University Press; 2004. P. 213-230.
  10. Klingenberg CP. Studying morphological integration and modularity at multiple levels: Concepts and analysis. Philos Trans R Soc Lond B Biol Sci. 2014;369(1649):20130249. https://doi.org/10.1098/rstb.2013.0249.
  11. Goswami A, Polly PD. Methods for studying morphological integration, modularity and covariance evolution. In: Quantitative methods in paleobiology. Ed by J. Alroy, G.H. Ithaca. NY: Paleontological Society Papers Series; 2010;16:213-243. https://doi.org/10.1017/S1089332600001881.
  12. Goswami A, Smaers JB, Soligo C, Polly PD. The macroevolutionary consequences of phenotypic integration: from development to deep time. Philos Trans R Soc Lond B Biol Sci. 2014;369(1649):20130254. https://doi.org/10.1098/rstb.2013.0254.
  13. Cheverud JM. Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution. 1982;36(3):499-516. https://doi.org/10.1111/j.1558-5646.1982.tb05070.x.
  14. Magwene PM. S27-1 Integration and modularity in biological system: a review. Acta Zoologica Sinica. 2006;52(Suppl.):490-493.
  15. Winther RG. Varieties of modules: kinds, levels, origins, and behaviors. J Exper Zool. 2001;291(2):116-129. https://doi.org/10.1002/jez.1064.
  16. Esteve-Altava B, Marugan-Lobon J, Botella H, et al. Grist for Riedl’s mill: a network model perspective on the integration and modularity of the human skull. J Exp Zool B Mol Dev Evol. 2013;320(8):489-500. https://doi.org/10.1002/jez.b.22524.
  17. Terentjev PV. Biometrische Untersuchungen über die morphologischen Merkmale von Rana ridibunda pall: (Amphibia, Salientia). Biometrika. 1931;23(1-2):23. https://doi.org/10.2307/2333629.
  18. Haber A. A comparative analysis of integration indices. Evol Biol. 2011;38(4):476-488. https://doi.org/10.1007/s11692-011-9137-4.
  19. Olson EC, Miller RL. Morphological integration. Chicago: University of Chicago Press; 1958. 376 p.
  20. Шмальгаузен И.И. Организм как целое. – М.; Л.: Изд-во АН СССР, 1942. – 211 с. [Shmalgauzen II. Organizm kak tseloe. Moscow; Leningrad: AN SSSR; 1942. 211 p. (In Russ.)]
  21. Schluter D. Adaptive radiation along genetic lines of least resistance. Evolution. 1996;50:1766-1774. https://doi.org/10.1111/j.1558-5646.1996.tb03563.x.
  22. Martinez-Abadias N, Esparza M, Sjovold T, et al. Pervasive genetic integration directs the evolution of human skull shape. Evolution. 2012;66:1010-1023. https://doi.org/10.1111/j.1558-5646.2011.01496.x.
  23. Ковалева В.Ю., Абрамов С.А., Дупал Т.А., и др. Анализ соответствия и комбинирование молекулярно-генетических и морфологических данных в зоологической систематике // Известия РАН. Серия биол. – 2012. – № 4. – C. 404–414. [Kovaleva VYu, Abramov SA, Dupal TA, et al. Congruence analysis and combining of molecular genetics and morphological data in zoological systematics. Biology Bulletin. 2012;39(4):335-345. (In Russ.)]. https://doi.org/10.1134/S1062359012030053.
  24. Ковалева В.Ю., Литвинов Ю.Н., Ефимов В.М. Землеройки (Soricidae, Eulipotyphla) Сибири и Дальнего Востока: комбинирование и поиск конгруэнтности молекулярно-генетических и морфологических данных // Зоологический журнал. – 2013. – Т. 92. – № 11. – С. 1383–1398. [Kovaleva VYu, Litvinov YuN, Efimov VM. Shrews (Soricidae, Eulipotyphla) from the Far East and Siberia: combination and search for congruence of molecular-genetic and morphological data. Russian journal of zoology. 2013;92(11):1383-1398. (In Russ.)]. https://doi.org/10.7868/S0044513413110081.
  25. Raff RA, Sly BJ. Modularity and dissociation in the evolution of gene expression territories in development. Evol Dev. 2000;2(2):102-111. https://doi.org/10.1046/j.1525-142x.2000.00035.x.
  26. Schlosser G. Modularity and the units of evolution. Theory Biosci. 2002;121(1):1-80. https://doi.org/10.1078/1431-7613-00049.
  27. Wagner GP, Pavlicev M, Cheverud J. The road to modularity. Nat Rev Genet. 2007;8:921-931. https://doi.org/10.1038/nrg2267.
  28. Kuratani S. Modularity, comparative embryology and Evo-Devo: developmental dissection of evolving body plans. Dev Biol. 2009;332(1):61-69. https://doi.org/10.1016/j.ydbio.2009.05.564.
  29. Murren CJ. The integrated phenotype. Integr Comp Biol. 2012;52(1):64-76. https://doi.org/10.1093/icb/ics043.
  30. Rasskin-Gutman D, Esteve-Altava B. Connecting the dots: anatomical network analysis in morphological EvoDevo. Biol Theory. 2014;9:178-193. https://doi.org/10.1007/s13752-014-0175-x.
  31. Klingenberg CP. Evolution and development of shape: integrating quantitative approaches. Nat Rev Genet. 2010;11(9):623-635. https://doi.org/10.1038/nrg2829.
  32. Willmore KE, Klingenberg CP, Hallgrímsson B. The relationship between fluctuating asymmetry and environmental variance in rhesus macaque skulls. Evolution. 2005;59(4);898-909. https://doi.org/10.1111/j.0014-3820.2005.tb01763.x.
  33. Klingenberg CP, Zaklan SD. Morphological integration between developmental compartments in the Drosophila wing. Evolution. 2000;54(4);1273-1285. https://doi.org/10.1111/j.0014-3820.2000.tb00560.x.
  34. Debat V, Alibert P, David P, et al. Independence between developmental stability and canalization in the skull of the house mouse. Proc Biol Sci. 2000;267(1442):423-30. https://doi.org/10.1098/rspb.2000.1017.
  35. Klingenberg CP, Badyaev AV, Sowry SM, Beckwith NJ. Inferring developmental modularity from morphological integration: analysis of individual variation and asymmetry in bumblebee wings. Am Nat. 2001;157(1):11-23. https://doi.org/10.1086/317002.
  36. Ivanović A, Kalezić ML. Testing the hypothesis of morphological integration on a skull of a vertebrate with a biphasic life cycle: a case study of the alpine newt. J Exp Zool B Mol Dev Evol. 2010;314(7):527-538. https://doi.org/10.1002/jez.b.21358.
  37. Jojić V, Blagojević J, Vujošević M. B chromosomes and cranial variability in yellow-necked field mice (Apodemus flavicollis). J Mammalogy. 2011;92(2);396-406. https://doi.org/10.1644/10-mamm-a-158.1.
  38. Monteiro LR, Bonato V, dos Reis SF. Evolutionary integration and morphological diversification in complex morphological structures: mandible shape divergence in spiny rats (Rodentia, Echimyidae). Evol Dev. 2005;7(5):429-439. https://doi.org/10.1111/j.1525-142x.2005.05047.x
  39. Bastir M, Rosas A, Stringer C, et al. Effects of brain and facial size on basicranial form in human and primate evolution. J Hum Evol. 2010;58(5):424-431. https://doi.org/10.1016/j.jhevol.2010.03.001.
  40. Hautier L, Lebrun R, Cox PG. Patterns of covariation in the masticatory apparatus of hystricognathous rodents: implications for evolution and diversification. J Morphol. 2012;273(12):1319-1337. https://doi.org/10.1002/jmor.20061.
  41. Klingenberg CP, Marugán-Lobón J. Evolutionary covariation in geometric morphometric data: analyzing integration, modularity, and allometry in a phylogenetic context. Syst Biol. 2013;62(4):591-610. https://doi.org/10.1093/sysbio/syt025.
  42. Chamero B, Buscalioni ÁD, Marugán-Lobón J. Pectoral girdle and forelimb variation in extant Crocodylia: the coracoid-humerus pair as an evolutionary module. Biol J Linn Soc. 2013;108(3):600-618. https://doi.org/10.1111/j.1095-8312.2012.02037.x.
  43. Santana SE, Lofgren SE. Does nasal echolocation influence the modularity of the mammal skull? J Evol Biol. 2013;26(11):2520-2526. https://doi.org/10.1111/jeb.12235.
  44. Поздняков А.А. Структура морфологической изменчивости (на примере морфотипов жевательной поверхности первого нижнего коренного зуба серых полевок) // Журнал общей биологии. – 2011. – Т. 72. – № 2. – С. 127–139. [Pozdnyakov AA. The structure of morphological variability (with the masticatory surface morphotypes of the lower first molar in the voles as an example). Biology Bulletin Reviews. 2011;1(5):471-481. (In Russ.)]. https://doi.org/10.1134/S2079086411050070.
  45. Васильев А.Г. Фенетический анализ биоразнообразия на популяционном уровне: Автореф. дис. … д-ра биол. наук. – Екатеринбург, 1996. – 47 с. [Vasil`ev AG. Phenetic analysis of biodiversity at the population level. [dissertation] Yekaterinburg; 1996. 47 p. (In Russ.)]. Доступно по: https://search.rsl.ru/ru/record/01000128144. Ссылка активна на 14.01.2019.
  46. Ковалева В.Ю., Поздняков А.А., Ефимов В.М. Изучение структуры изменчивости морфотипов коренных зубов полевки-экономки (Microtus oeconomus) через билатеральную асимметрию их проявления // Зоологический журнал. – 2002. – Т. 81. – № 1. – С. 111–117. [Kovaleva VYu, Pozdnyakov AA, Efimov VM. Investigation of variability structure of root vole (Microtus oeconomus Pallas) molar morphotypes using bilateral asymmetry. Russian journal of zoology. 2002;81(1):111-117. (In Russ.)]
  47. Kovaleva VYu, Efimov VM, Litvinov YuN. Directional asymmetry of morphological traits during postnatal ontogeny in root vole Microtus oeconomus Pall. (Rodentia, Cricetidae). J SibFU. Biol. 2013;6(2):115-129. https://doi.org/10.17516/1997-1389-0111.
  48. Поздняков А.А. Морфологическое разнообразие: характеристика, структура, анализ // Сообщества и популяции животных: экологический и морфологический анализ / Под ред. В.Н. Большакова. Серия: Труды Института систематики и экологии животных СО РАН. – М.: Товарищество научных изданий КМК; 2010. – С. 133–157. [Pozdnyakov AA. Morfologicheskoe raznoobrazie: kharakteristika, struktura, analiz. In: Ser: Trudy Instituta sistematiki i ekologii zhivotnykh SO RAN. Soobshchestva i populyatsii zhivotnykh: ekologicheskii i morfologicheskii analiz. Ed by V.N. Bolshakov. Moscow: Tovarishchestvo nauchnykh izdanii KMK; 2010. P. 133-157. (In Russ.)]
  49. Nucleotide-NCBI. National Center for Biotechnology Information, U.S. National Library of Medicine [cited 2018 August 16]. Available from: http://www.ncbi.nlm.nih.gov/nucleotide/.
  50. Climate:Data.org. Климатические данные городов по всему миру. [Climate:Data.org. Klimaticheskie dannye gorodov po vsemu miru. (In Russ.)]. Доступно по: http://ru.climate-data.org/. Ссылка активна на 16.02.2019.
  51. Ефимов В.М., Мельчакова М.А., Ковалева В.Ю. Геометрические свойства эволюционных дистанций [электронный ресурс] // Вавиловский журнал генетики и селекции. – 2013. – Т. 17. – № 4/1. – С. 714–723. [Efimov VM, Melchakova MA, Kovaleva VYu. Geometric properties of evolutionary distances (Elektronnyi resurs). Vavilov Journal of Genetics and Breeding. 2013;17(4/1):714-723. (In Russ.)]. Доступно по: https://docplayer.ru/42679204-Geometricheskie-svoystva-evolyucionnyh-distanciy.html. Ссылка активна на 11.01.2019.
  52. Ангерманн Р. Гомологическая изменчивость коренных зубов у полевок (Microtinae) // Проблемы эволюции. Т. 3 / Под ред. Н.Н. Воронцова. – Новосибирск: Наука. Сиб. отд-ние, 1973. – С. 104–118. [Angermann R. The homologous variability of molars in voles (Microtinae). In: Problems of evolution. Ed by N.N. Vorontsov. V. 3. Novosibirsk: Nauka, Sib. otd-nie; 1973. P. 104-118. (In Russ.)]
  53. Абрамсон Н.И., Лисовский А.А. Подсемейство Arvicolinae // Млекопитающие России: систематико-географический справочник / Под ред. И.Я. Павлинова, А.А. Лисовского. –М.: Товарищество научных изданий КМК, 2012. – С. 220–276. [Abramson NI, Lisovskii AA. Subfamily Arvicolinae. In: The mammals of Russia. A taxonomic and geographic reference. Ed by I.Ya. Pavlinov, A.A. Lissovsky. Moscow: Tovarishchestvo nauchnykh izdanii KMK; 2012. P. 220-276. (In Russ.)]
  54. Wold S, Sjöström M, Eriksson L. PLS-regression: a basic tool of chemometrics. Chemom Intell Lab Syst. 2001;58(2):109-130. https://doi.org/10.1016/S0169-7439(01)00155-1.
  55. Gower JC. Generalized procrustes analysis. Psychometrika. 1975;40(1):33-51. https://doi.org/10.1007/bf02291478.
  56. Полунин Д.А., Штайгер И.А., Ефимов В.М. Разработка программного комплекса JACOBI 4 для многомерного анализа микрочиповых данных // Вестник НГУ. Серия: Информационные технологии. – 2014. – Т. 12. – № 2. – С. 90–98. [Polunin DA, Shtayger IA, Efimov VM. JACOBI 4 software for multivariate analysis of microarray data. Vestnik NSU. Ser.: Information Technology. 2014;12(2):90-98. (In Russ.)]
  57. Cavalli-Sforza LL, Edwards AW. Phylogenetic analysis. Models and estimation procedures. Am J Hum Genet. 1967;19:233-257. https://doi.org/10.1111/j.1558-5646.1967.tb03411.x.
  58. Sharp PM, Li WH. An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol. 1986;24(1-2):28-38. https://doi.org/10.1007/bf02099948.
  59. Goldman N, Yang Z. A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol. 1994;11(5):725-736. https://doi.org/10.1093/oxfordjournals.molbev.a040153.
  60. Schneider A, Cannarozzi GM, Gonnet GH. Empirical codon substitution matrix. BMC bioinformatics. 2005;6:134. https://doi.org/10.1186/1471-2105-6-134.
  61. Torgerson WS. Multidimensional scaling: I. Theory and method. Psychometrika. 1952;17(4):401-419. https://doi.org/10.1007/bf02288916.
  62. Gower JC. Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika. 1966;53:325-338. https://doi.org/10.1093/biomet/53.3-4.325.
  63. Legendre P, Legendre L. Numerical Ecology: second English edition. In: Developments in Environmental Modelling. Amsterdam: Elsevier; 1998. 853 p.
  64. Adams DC. Quantifying and comparing phylogenetic evolutionary rates for shape and other high-dimensional phenotypic data. Syst Biol. 2014;63(2):166-177. https://doi.org/10.1093/sysbio/syt105.
  65. Ефимов В.М., Ковалева В.Ю., Литвинов Ю.Н. Комбинирование генов и оценка конгруэнтности их филогенетических сигналов на основе геометрического подхода // Вавиловский журнал генетики и селекции. – 2016. – Т. 20. – № 6. – С. 816–822. [Efimov VM, Kovaleva VYu, Litvinov YuN. The combination of genes and their assessment of the congruence of phylogenetic signals based on geometric approach. Vavilov Journal of Genetics and Breeding.2016;20(6):816-822. (In Russ.)]. https://doi.org/10.18699/VJ16.153.
  66. Ковалева В.Ю. Блочно-модульная организация фенотипической изменчивости: Автореф. дис. … д-ра биол. наук. – Новосибирск, 2017. – 47 с. [Kovaleva VYu. Blochno-modulnaya organizatsiya fenotipicheskoi izmenchivosti. [dissertation] Novosibirsk; 2017. 47 p. (In Russ.)]. Доступно по: https://search.rsl.ru/ru/record/01006658833. Ссылка активна на 14.01.2019.
  67. Захаров В.М. Асимметрия животных: популяционно-феногенетический подход. – М.: Наука, 1987. – 216 с. [Zakharov VM. Asimmetriya zhivotnykh populyatsionno-fenogeneticheskii podkhod. Moscow: Nauka; 1987. 216 p. (In Russ.)]
  68. Bannikova AA, Lebedev VS, Lissovsky AA, et al. Molecular phylogeny and evolution of the Asian lineage of vole genus Microtus (Rodentia: Arvicolinae) inferred from mitochondrial cytochrome b sequence. Biol J Linnean Soc. 2010;99(3):595-613. https://doi.org/10.1111/j.1095-8312.2009.01378.x.
  69. Поздняков А.А., Ковалева В.Ю., Ефимов В.М., Литвинов Ю.Н. Сопряженность морфотипической и молекулярно-генетической изменчивости полевок группы родов МICROTUS // Териофауна России и сопредельных территорий / Международное совещание. X Съезд Териологического общества при РАН, 1–5 февраля 2016 г. – М.: Товарищество научных изданий КМК, 2016. – С. 333. [Pozdnyakov AA, Kovaleva VYu, Efimov VM, Litvinov YuN. Sopryazhennost’ morfotipicheskoi i molekulyarno-geneticheskoi izmenchivosti polevok gruppy rodov MICROTUS. In: Teriofauna of Russia and Adjacent Territories: International Conference. X Congress of the Teriological Society of the Russian Academy of Sciences, February 1-5, 2016. Moscow: Tovarishchestvo nauchnykh izdanii KMK; 2016. Р. 333. (In Russ.)]
  70. Шмидт В.М. Развитие представлений о корреляциях и корреляционной структуре биологических объектов // Исследование биологических систем математическими методами / Труды Биологического НИИ ЛГУ. – Л.: Изд-во Ленинградского ун-та, 1985. – № 37. – С. 5–18. [Shmidt VM. Razvitie predstavlenii o korrelyatsiyakh i korrelyatsionnoi strukture biologicheskikh obektov. In: Issledovanie biologicheskikh sistem matematicheskimi metodami. Tr. Boil. NII LGU. 1985;(37):5-18. (In Russ.)]
  71. Ефимов В.М. Проблемы многомерного анализа экологических данных: Автореф. дис ... д-ра биол. наук. – Томск: ТГУ; 2003. – 39 с. [Efimov VM. Problemy mnogomernogo analiza ekologicheskikh dannykh. [dissertation] Tomsk: TGU; 2003. 39 р. (In Russ.)]. Доступно по: https://search.rsl.ru/ru/record/01002652594. Ссылка активна на 14.01.2019.
  72. Ефимов В.М., Ковалева В.Ю. Многомерный анализ биологических данных: учебное пособие. – 2-е изд., испр. и доп. – СПб.: ВИЗР РАСХН, 2008. – 87 с. [Efimov VM, Kovaleva VYu. Mnogomernyi analiz biologicheskikh dannykh: uchebnoe posobie. 2nd ed. Saint Petersburg: VIZR RASKHN; 2008. 87 p. (In Russ.)]
  73. Gilbert SF. Developmental biology. 8th ed. Sunderland, MA; 2006. 751 p. https://doi.org/10.1162/biot.2006.1.2.209.
  74. Исаева В.В. Преобразования симметрии в онтогенезе и эволюции [интернет] // Морфогенез в индивидуальном и историческом развитии: симметрия и асимметрия. Серия: Геобиологические процессы в прошлом. – М.: ПИН РАН; 2013. – С. 22–43. [Isaeva VV. Preobrazovaniya simmetrii v ontogeneze i evolyutsii [Internet]. In: Morfogenez v individualnom i istoricheskom razvitii simmetriya i asimmetriya. Seriya: Geobiologicheskie protsessy v proshlom. Moscow: PIN RAN; 2013. P. 22-43. (In Russ.)]. Доступно по: http://os.x-pdf.ru/20biologiya/768960-1-preobrazovaniya-simmetrii-ontogeneze-evolyucii-2013-isaeva-institu.php. Ссылка активна на 12.12.2018.
  75. Ковалева В.Ю., Фалеев В.И. Морфологическая изменчивость полевки-экономки Microtus oeconomus (Rodentia, Cricetidae) в различных температурных условиях среды // Зоологический журнал. – 1994. – Т. 73. – № 9. – С. 139–145. [Kovaleva VYu, Faleev VI. Morphological variability of Microtus oeconomus (Rodentia, Cricetidae) in different temperature conditions. Russian journal of zoology. 1994;73(9):139-145. (In Russ.)]
  76. Ковалева В.Ю., Ефимов В.М., Фалеев В.И. Краниометрическая изменчивость сеголеток водяной полевки Arvicola terrestris (Rodentia, Cricetidae) в связи с факторами среды // Зоологический журнал. – 1996. – Т. 75. – № 10. – С. 1558–1559. [Kovaleva VYu, Efimov VM, Faleev VI. Craniometric variation of non-wintering water voles Arvicola terrestris (Rodentia, Cricetidae) in different environmental conditions. Russian journal of zoology.1996;75(10):1551-1559. (In Russ.)]
  77. Поздняков А.А. Морфотипическая изменчивость серых полевок (Rodentia, Arvicolidae, Microtus) в связи с температурными условиями среды // Успехи современной биологии. – 2003. – Т. 123. – № 2. – С. 187–194. [Pozdnyakov AA. Morphotypical variability of voles of the subgenus Alexandromys (Rodentia, Arvicolidae, Microtus) related to temperature conditions. Biol Bull Reviews. 2003;1:471. (In Russ.)]. https://doi.org/10.1134/S2079086411050070.
  78. dos Reis M, Savva R, Wernisch L. Solving the riddle of codon usage preferences: a test for translational selection. Nucleic Acids Res. 2004;32:5036-5044. https://doi.org/10.1093/nar/gkh834.
  79. Krisko A, Copic T, Gabaldon T, et al. Inferring gene function from evolutionary change in signatures of translation efficiency. Genome Biol. 2014;15(3):R44. https://doi.org/10.1186/gb-2014-15-3-r44.
  80. Novoa EM, Ribas de Pouplana L. Speeding with control: codon usage, tRNAs, and ribosomes. Trends Genet. 2012;28(11):574-581. https://doi.org/10.1016/j.tig.2012.07.006.
  81. Pechmann S, Frydman J. Evolutionary conservation of codon optimality reveals hidden signatures of cotranslational folding. Nat Struct Mol Biol. 2013;20:237-243. https://doi.org/10.1038/nsmb.2466.
  82. Buhr F, Jha S, Thommen M, et al. Synonymous codons direct cotranslational folding toward different protein conformations. Molecular Cell. 2016;61(3):341-351. https://doi.org/10.1016/j.molcel.2016.01.008.
  83. Hershberg R, Petrov DA. Selection on codon bias. Annu Rev Genet. 2008;42:287-299. https://doi.org/10.1146/annurev.genet.42.110807.091442.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. The locations of the most representative samples for each species. Species: 1 – A. fortis, 2 – A. maximowiczii, 3 – A. middendorffii, 4 – A. mongolicus, 5 – A. oeconomus, 6 – L. gregalis, 7 – M. agrestis, 8 – M. paradoxus, 9 – M. rossiaemeridionalis, 10 – N. juldaschi

Download (110KB)
Indexing metadata
3. Fig. 2. The configuration of ten species of the gray voles Microtus s.l. on the plane of the first two PCs of the morphogenetic distances matrix

Download (72KB)
Indexing metadata
4. Fig. 3. The configuration of ten species of the gray voles Microtus s.l. on the plane of the first two PCs of the synonymous distances matrix

Download (80KB)
Indexing metadata
5. Fig. 4. Correlation (r = 0,847, n = 10, p = 0,002) between PC1 of the synonymous distances matrix and PC2 of the morphogenetic distances matrix

Download (73KB)
Indexing metadata
6. Fig. 5. Correlation (r = 0,788, n = 10, p = 0,0068) between PC1 of the climatic variability and PC1 of the synonymous distances matrix

Download (73KB)
Indexing metadata

Copyright (c) 2019 Kovaleva V.Y., Pozdnyakov A.A., Litvinov Y.N., Efimov V.M.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
 


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies