Putative Locus for Cranial Size Variability of the Fox (Vulpes vulpes)

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Skull morphology was studied in three populations of red foxes (Vulpes vulpes): tame, which was produced by long-term selection for friendly behavior to humans; aggressive, which was produced by long-term selection for aggressive behavior to humans; and conventional farm-bred, which was not deliberately selected for behavior. We have collected skulls measurements from two sets of foxes: (1) 140 backcross foxes produced by breeding of tame and aggressive foxes to each other and then crossing F1 foxes to tame strain, and (2) 150 foxes from original populations (50 tame, 50 aggressive and 50 conventional farm-bred). The backcross foxes have been genotyped with 350 microsatellite markers and analyzed using 2B-PLS analysis. A significant correlation between microsatellite genotypes and skull shape was identified for three microsatellite markers on 10-th fox chromosome: FH2535, RVC1, REN193M22. The second set of foxes (tame, aggressive and conventional) was genotyped for these three markers and also analysed with 2B_PLS. Significant correlation was identified between genotypes and skull size for males, but not for females. The genomic region identified in this study contains IGF-1 gene, which is responsible for 15% of body size variation in dogs. Our findings suggest that IGF-1 gene is also involved in skull size regulation in red foxes.

About the authors

A. V. Kharlamova

Federal Research Center Institute of Cytology and Genetics,
Siberian Branch of the Russian Academy of Sciences

Author for correspondence.
Email: kharlam@bionet.nsc.ru
Russia, 630090, Novosibirsk

S. G. Shikhevich

Federal Research Center Institute of Cytology and Genetics,
Siberian Branch of the Russian Academy of Sciences

Email: kharlam@bionet.nsc.ru
Russia, 630090, Novosibirsk

A. V. Vladimirova

Federal Research Center Institute of Cytology and Genetics,
Siberian Branch of the Russian Academy of Sciences

Email: kharlam@bionet.nsc.ru
Russia, 630090, Novosibirsk

A. V. Kukekova

University of Illinois at Urbana-Champaign

Email: kharlam@bionet.nsc.ru
USA, 61801, Urbana

V. M. Efimov

Federal Research Center Institute of Cytology and Genetics,
Siberian Branch of the Russian Academy of Sciences; Novosibirsk State University; Tomsk State University

Email: kharlam@bionet.nsc.ru
Russia, 630090, Novosibirsk; Russia, 630090, Novosibirsk; Russia, 634050, Tomsk

References

  1. Belyaev D.K. Destabilizing selection as a factor of domestication // J. Hered. 1979. V. 70. P. 301–308.
  2. Coppinger R., Coppinger L. Dogs: A Startling New Understanding of Canine Origin, Behavior & Evolution. N.Y.: Scribner, 2001. 356 p.
  3. Trut L., Oskina I., Kharlamova A. Animal evolution during domestication: the domesticated fox as a model // BioEssays. 2009. V. 31. № 3. P. 349–360. https://doi.org/10.1002/bies.200800070
  4. Price E.O. Animal Domestication and Behavior. Wallingford, United Kingdom: CABI Publ., 2002. 297 p.
  5. Clutton-Brock J. Origins of the dog: the archaeological evidence // The Domestic Dog: Its Evolution, Behavior and Interactions with People. Second ed. Cambridge: Cambr. Univ. Press, 2017. P. 7–22.
  6. Lindblad-Toh K., Wade C.M., Mikkelsen T.S. et al. Genome sequence, comparative analysis and haplotype structure of the domestic dog // Nature. 2005 V. 8. № 438(7069). P. 803–819. https://doi.org/10.1038/nature04338
  7. Frantz L.A., Mullin V.E., Pionnier-Capitan M. et al. Genomic and archaeological evidence suggest a dual origin of domestic dogs // Science. 2016. V. 3. № 352(6290). P. 1228–1231. https://doi.org/10.1126/science.aaf3161
  8. Germonpré M., Lázničková-Galetová M., Sablin M.V., Bocherens H. Self-domestication or human control? The Upper Palaeolithic domestication of the wolf // Hybrid Communities. London: Routledge, 2018. 324 p.
  9. Bergström A., Frantz L., Schmidt R. et al. Origins and genetic legacy of prehistoric dogs // Science. 2020. V. 30. № 370(6516). P. 557–564. https://doi.org/10.1126/science.aba9572
  10. Pitulko V.V., Kasparov A.K. Archaeological dogs from the Early Holocene Zhokhov site in the Eastern Siberian Arctic // J. Archaeol. Sci.: Reports 13. 2017. P. 491–515. https://doi.org/10.1016/j.jasrep.2017.04.003
  11. Zeuner F.E. A History of Domesticated Animals. London: Hutchinson & Co. (Publishers) Ltd., 1963. 560 p.
  12. Harcourt R.A. The dog in prehistoric and early historic Britain // J. Archaeol. Sci. 1974. V. 1. P. 151–175.
  13. Clutton-Brock J. Domesticated Animals from Early Times. London: British Museum (Natural History) and William Heinemann Ltd., 1981. 208 p.
  14. Clutton-Brock J. Origins of the dog: domestication and early history // The Domestic Dog: Its Evolution, Behaviour, and Interactions with People. Cambridge: Cambr. Univ. Press, 1995. P. 7–20.
  15. Zedda M., Manca P., Chisu V. et al. Ancient pompeian dogs – morphological and morphometric evidence for different canine populations // Anat. Histol. Embryol. 2006. V. 35. № 5. P. 319–324. https://doi.org/10.1111/j.1439-0264.2006.00687.x
  16. Pionnier-Capitan M., Bemilli C., Bodu P. et al. New evidence for Upper Palaeolithic small domestic dogs in South-Western Europe // J. Archaeol. Sci. 2011. V. 38. № 9. P. 2123–2140. https://doi.org/10.1016/j.jas.2011.02.028
  17. Chase K., Carrier D.R., Adler F.R. et al. Genetic basis for systems of skeletal quantitative traits: Principal component analysis of the canid skeleton // PNAS 2002. V. 99. № 15. P. 9930–9935. https://doi.org/10.1073/pnas.152333099
  18. Parker H.G., Shearin A.L., Ostrander E.A. Man’s best friend becomes biology’s best in show: genome analyses in the domestic dog // Annu. Rev. Genet. 2010. V. 44. P. 309–336. https://doi.org/10.1146/annurev-genet-102808-115200
  19. Yengo L., Sidorenko J., Kemper K.E. et al. GIANT Consortium. Meta-analysis of genome-wide association studies for height and body mass index in ∼700 000 individuals of European ancestry // Hum. Mol. Genet. 2018. V. 27. № 20. P. 3641–3649. https://doi.org/10.1093/hmg/ddy271
  20. Rimbault M., Beale H.C., Schoenebeck J.J. et al. Derived variants at six genes explain nearly half of size reduction in dog breeds // Genome Research. 2013. № 23. P. 1985–1995. https://doi.org/10.1101/gr.157339.113
  21. Sutter N.B., Bustamante C.B., Chase K. et al. A single IGF1 allele is a major determinant of small size in dogs // Science. 2007. № 316. P. 112–115. https://doi.org/10.1126/science.1137045
  22. Fang X.B., Liu S.C., Wu Q.Y. et al. Linkage analysis of SNPs in IGFBP-6 and its relation with the body sizes of pig // Genet. Mol. Res. 2015. V. 14. № 4. P. 17273–17280. https://doi.org/10.4238/2015
  23. Makvandi-Nejad S., Hoffman G.E., Allen J.J. et al. Four loci explain 83% of size variation in the horse // PLoS One. 2012. V. 7. № 7. P. e39929. https://doi.org/10.1371/journal.pone.0039929
  24. Plassais J., Kim J., Davis B.W. et al. Whole genome sequencing of canids reveals genomic regions under selection and variants influencing morphology // Nat. Commun. 2019. V. 10. № 1. P. 1489. https://doi.org/10.1038/s41467-019-09373-w
  25. Bannasch D., Young A., Myers J. et al. Localization of canine brachycephaly using an across breed mapping approach // PLoS One. 2010. V. 5. № 3. P. e9632. https://doi.org/10.1371/journal.pone.0009632
  26. Boyko A.R., Quignon P., Li L., Schoenebeck J.J. et al. A simple genetic architecture underlies morphological variation in dogs // PLoS Biol. 2010. № 8. P. e1000451. https://doi.org/10.1371/journal.pbio.1000451
  27. Schoenebeck J.J., Hutchinson S.A., Byers A. et al. Variation of BMP3 contributes to dog breed skull diversity // PLoS Genet. 2012. V. 8. № 8. P. e1002849. https://doi.org/10.1371/journal.pgen.1002849
  28. Schoenebeck J.J., Ostrander E.A. Insights into morphology and disease from the dog genome project // Annu. Rev. Cell Dev. Biol. 2014. V. 30. P. 535–560. https://doi.org/10.1146/annurev-cellbio-100913-012927
  29. Wilson L.A.B., Balcarcel A., Geiger M. et al. Modularity patterns in mammalian domestication: Assessing developmental hypotheses for diversification // Evol. Lett. 2021. https://doi.org/10.1002/evl3.231
  30. Wright D., Henriksen R., Johnsson M. Defining the Domestication Syndrome: Comment on Lord et al. 2020 // Trends Ecol. Evol. 2020. V. 35. № 12. P. 1059–1060. https://doi.org/10.1016/j.tree.2020.08.009
  31. Trut L.N. Early Canid Domestication: The Farm-Fox Experiment: Foxes bred for tamability in a 40-year experiment exhibit remarkable transformations that suggest an interplay between behavioral genetics and development // Am. Sci. 1999. V. 87. № 2. P. 160–169.
  32. Wayne R.K. Consequences of domestication: Morphological diversity of the dog // The Genetics of the Dog. N.Y.: CABI Publ., 2001. P. 43–60.
  33. Evin A., Dobney K., Schafberg R. et al. Phenotype and animal domestication: A study of dental variation between domestic, wild, captive, hybrid and insular Sus scrofa // BMC Evol Biol. 2015. V. 15. P. 6. https://doi.org/10.1186/s12862-014-0269-x
  34. Трут Л.Н., Дзержинский Ф.Я., Никольский В.С. Компонентный анализ краниологических признаков серебристо-черных лисиц (Vulpes vulpes Desm) и их изменений, возникающих при доместикации // Генетика. 1991. Т. 27. № 8. С. 1440–1449.
  35. Трут Л.Н., Дзержинский Ф.Я., Никольский В.С. Внутричерепная аллометрия и краниологические изменения при доместикации серебристо-черных лисиц // Генетика. 1991. Т. 27. № 9. С. 1605–1612.
  36. Hecht E.E., Kukekova A.V., Gutman D.A. et al. Neuromorphological changes following selection for tameness and aggression in the Russian farm-fox experiment // J. Neurosci. 2021. V. 41. № 28. P. 6144–6156. https://doi.org/10.1523/JNEUROSCI.3114-20.2021
  37. Kukekova A.V., Trut L.N., Chase K. et al. Mapping loci for fox domestication: deconstruction/reconstruction of a behavioral phenotype // J. Behav. Genet. 2011. V.41. № 4. P. 593–606. https://doi.org/10.1007/s10519-010-9418-1
  38. Trut L.N., Kharlamova A.V., Kukekova A.V. et al. Morphology and behavior: Are they coupled at the genome level? // The Dog and Its Genome. Woodbury N.Y.: Cold Spring Harbor Lab. Press, 2006. P. 515–538.
  39. Jackson J.E. A User’s Guide to Principal Components. N.Y.: A Wiley Interscience Publ., 1991. 563 p.
  40. Kharlamova A.V., Trut L.N., Carrier D.R. et al. Genetic regulation of canine skeletal traits: Trade-offs between the hind limbs and forelimbs in the fox and dog // Integr. Comp. Biol. 2007. V. 47. P. 373–381. https://doi.org/10.1093/icb/icm023
  41. Харламова А.В., Чейз К., Ларк К.Г. и др. Сопоставление вариации параметров скелетной системы лисиц (Vulpes vulpes), отбираемых по поведению, и собак (Canis familiaris) // Вестник ВОГиС. 2008. Т. 12. № 1/2. С. 32–38.
  42. Маниатис Т., Фрич Э., Сэмбрук Дж. Методы генетической инженерии. Молекулярное клонирование. М.: Мир, 1984. 545 с.
  43. Kukekova A.V., Trut L.N., Oskina I.N. et al. A marker set for construction of a genetic map of the silver fox (Vulpes vulpes) // J. Hered. 2004. V. 95. № 3. P. 185–194. https://doi.org/10.1093/jhered/esh033
  44. Kukekova A.V., Trut L.N., Oskina I.N. et al. A meiotic linkage map of the silver fox, aligned and compared to the canine genome // Genome Res. 2007. V. 17. P. 387–399. https://doi.org/10.1101/gr.5893307
  45. Rohlf F.J., Corti M. Use of two-block partial least squares to study covariation in shape // System. Biology. 2000. V. 49. P. 740–753. https://doi.org/10.1080/106351500750049806
  46. Polunin D., Shtaiger I., Efimov V. JACOBI4 software for multivariate analysis of biological data // bioRxiv. 2019. P. 803684. https://doi.org/10.1101/803684
  47. Wold H. Path models with latent variables: The NIPALS approach // Quantitative Sociology: International Perspectives on Mathematical and Statistical Model Building. N.Y.: Acad. Press, 1975. P. 307–357.
  48. Rosipal R., Krämer N. Overview and recent advances in partial least squares // International Statistical and Optimization Perspectives Workshop “Subspace, Latent Structure and Feature Selection”. Berlin; Heidelberg: Springer, 2005. P. 34–51.
  49. Baab K.L., Freidline S.E., Wang S.L., Hanson T. Relationship of cranial robusticity to cranial form, geography and climate in Homo sapiens // Am. J. Phys. Anthropol. 2010. V. 141. № 1. P. 97–115. https://doi.org/10.1002/ajpa.21120
  50. Goswami A., Polly P.D. Methods for studying morphological integration, modularity and covariance evolution // Quantitative Methods in Paleobiology. Ithaca; N.Y.: Paleontol. Society Papers Series, 2010. V. 16. P. 213–243. https://doi.org/10.1017/S1089332600001881
  51. Goswami A., Polly P.D. The influence of modularity on cranial morphological disparity in carnivora and primates (Mammalia) // PLoS One. 2010. V. 5. № 3. P. e9517. https://doi.org/10.1371/journal.pone.0009517
  52. Goswami A., Smaers J.B., Soligo C., Polly P.D. The macroevolutionary consequences of phenotypic integration: From development to deep time // Phil. Trans. R. Soc. B. 2014. V. 369. № 1649. P. 20130254. https://doi.org/10.1098/rstb.2013.0254
  53. Álvarez A., Perez S.I., Verzi D.H. The role of evolutionary integration in the morphological evolution of the skull of caviomorph rodents (Rodentia: Hystricomorpha) // Evol. Biol. 2015. V. 42. № 3. P. 312–327. https://doi.org/10.1111/j.1420-9101.2011.02395.x
  54. Goswami A., Watanabe A., Felice R.N. et al. High-density morphometric analysis of shape and integration: the good, the bad, and the not-really-a-problem // Integr. Comp. Biol. 2019. V. 59. № 3. P. 669–683. https://doi.org/10.1093/icb/icz120
  55. Alhajeri B.H. Cranial variation in geographically widespread dwarf gerbil Gerbillus nanus (Gerbillinae, Rodentia) populations: Isolation by distance versus adaptation to local environments // J. Zool. Systematics and Evol. Res. 2019. V. 57. № 1. P. 191–203. https://doi.org/10.1111/jzs.12247
  56. Brassard C., Merlin M., Guintard C. et al. Interrelations between the cranium, the mandible and muscle architecture in modern domestic dogs // Evol. Biol. 2020. V. 47. № 4. P. 308–324. https://doi.org/10.1007/s11692-020-09515-9
  57. Ковалева В.Ю., Абрамов С.А., Дупал Т.А., Ефимов В.М. Анализ соответствия и комбинирование молекулярно-генетических и морфологических данных в зоологической систематике // Изв. РАН. Серия биол. наук. 2012. № 4. С. 404–414.
  58. 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 // Зоол. журн. 2013. Т. 92. № 11. С. 1383–1398. https://doi.org/10.7868/S0044513413110081
  59. Klingenberg C.P., Spence J.R., Mirth C.K. Introgressive hybridization between two species of waterstriders (Hemiptera: Gerridae: Limnoporus): Geographical structure and temporal change of a hybrid zone // J. Evol. Biol. 2000. V. 13. № 5. P. 756–765.
  60. Myers E.M., Janzen F.J., Adams D.C., Tucker J.K. Quantitative genetics of plastron shape in slider turtles (Trachemys scripta) // Evolution. 2006. V. 60. № 3. P. 563–572. https://doi.org/10.1111/j.0014-3820.2006.tb01137.x
  61. Claverie T., Patek S.N. Modularity and rates of evolutionary change in a power-amplified prey capture system // Evolution. 2013. V. 67. № 11. P. 3191–3207. https://doi.org/10.1111/evo.12185
  62. Hanot P., Herrel A., Guintard C., Cornette R. Unravelling the hybrid vigor in domestic equids: the effect of hybridization on bone shape variation and covariation // BMC Evol. Biol. 2019. V. 19. № 1. P. 1–13. https://doi.org/10.1186/s12862-019-1520-2
  63. Hanot P., Bayarsaikhan J., Guintard C. et al. Cranial shape diversification in horses: Variation and covariation patterns under the impact of artificial selection // BMC Ecol. Evol. 2021. V. 21. № 1. P. 1–19. https://doi.org/10.1186/s12862-021-01907-5
  64. Benjamini Y., Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing // J. Royal Stat. Society. Series B. 1995. № 57. P. 289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
  65. Hammer Ø., Harper D.A.T., Ryan P.D. PAST: Paleontological statistics software package for education and data analysis // Palaeontol. Electronica. 2001. V. 4. № 1. P. 9.
  66. Rimbault M., Beale H.C., Schoenebeck J.J. et al. Derived variants at six genes explain nearly half of size reduction in dog breeds // Gen. Res. 2013. № 23. P. 1985–1995. 113https://doi.org/10.1101/gr.15733
  67. Fang X.B., Liu S.C., Wu Q.Y. et al. Linkage analysis of SNPs in IGFBP-6 and its relation with the body sizes of pig // Genet. Mol. Res. 2015. V. 14. № 4. P. 17273–17280. https://doi.org/10.4238/2015
  68. Makvandi-Nejad S., Hoffman G.E., Allen J.J. et al. Four loci explain 83% of size variation in the horse // PLoS One. 2012. V. 7. № 7. P. e39929. https://doi.org/10.1371/journal.pone.0039929
  69. Baker J., Liu J.P., Robertson E.J., Efstratiadis A. Role of insulin-like growth factors in embryonic and postnatal growth // Cell. 1993. V. 75. P. 73–82. https://doi.org/10.1016/S0092-8674(05)80085-6
  70. Kawai M., Rosen C.J. Insulin-like growth factor-I and bone: lessons from mice and men // Pediatr. Nephrol. 2009. V. 24. P. 1277–1285. https://doi.org/10.1007/s00467-008-1040-6
  71. Bérubé S.C., Johnsson P.R., Bunimov N. et al. Two length variants of the microsatellite FH2295 as markers for body size of female Portuguese water dogs // J. Appl. Genetics. 2012. V. 53. P. 121–123. https://doi.org/10.1007/s13353-011-0076-7
  72. Plassais J., vonHoldt B.M., Parker H.G. et al. Natural and human-driven selection of a single noncoding body size variant in ancient and modern canids // Current Biol. 2022. V. 32. P. 1–9. https://doi.org/10.1016/j.cub.2021.12.036
  73. Sánchez-Villagra M.R., Geiger M., Schneider R.A. The taming of the neural crest: A developmental perspective on the origins of morphological covariation in domesticated mammals // Royal Soc. Open Sci. 2016. V. 3. № 6. P. 160107. https://doi.org/10.1098/rsos.160107
  74. Zapata I., Lilly M.L., Herron M.E. et al. Genetic testing of dogs predicts problem behaviors in clinical and nonclinical samples // BMC Genomics. 2022. V. 23. P. 1–19. https://doi.org/10.1186/s12864-022-08351-9
  75. Nelson R.M., Temnykh S.V., Johnson J.L. et al. Genetics of interactive behavior in silver foxes (Vulpes vulpes) // Behavior Genet. 2017. V. 47. № 1. P. 88–101.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2.

Download (1MB)
Indexing metadata
3.

Download (251KB)
Indexing metadata
4.

Download (111KB)
Indexing metadata
5.

Download (89KB)
Indexing metadata
6.

Download (95KB)
Indexing metadata

Copyright (c) 2023 А.В. Харламова, С.Г. Шихевич, А.В. Владимирова, А.В. Кукекова, В.М. Ефимов

This website uses cookies

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

About Cookies