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Journal of anatomy2018; 232(4); 657-673; doi: 10.1111/joa.12772

The impact of artificial selection on morphological integration in the appendicular skeleton of domestic horses.

Abstract: The relationships between the different component parts of organisms, such as the sharing of common development or function, produce a coordinated variation between the different traits. This morphological integration contributes to drive or constrain morphological variation and thus impacts phenotypic diversification. Artificial selection is known to contribute significantly to phenotypic diversification of domestic species. However, little attention has been paid to its potential impact on integration patterns. This study explores the patterns of integration in the limb bones of different horse breeds, using 3D geometric morphometrics. The domestic horse is known to have been strongly impacted by artificial selection, and was often selected for functional traits. Our results confirm that morphological integration among bones within the same limb is strong and apparently partly produced by functional factors. Most importantly, they reveal that artificial selection, which led to the diversification of domestic horses, impacts covariation patterns. The influence of selection on the patterns of covariation varies along the limbs and modulates bone shape, likely due to a differential ligament or muscle development. These results highlight that, in addition to not being constrained by a strong morphological integration, artificial selection has modulated the covariation patterns according to the locomotor specificities of the breeds. More broadly, it illustrates the interest in studying how micro-evolutionary processes impact covariation patterns and consequently contribute to morphological diversification of domestic species.
© 2018 Anatomical Society.
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Publication Date: 2018-01-08 PubMed ID: 29315551PubMed Central: PMC5835793DOI: 10.1111/joa.12772Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research investigates how artificial selection, such as breeding, affects the shape and function of the appendicular skeleton (limbs) of domestic horses, revealing that such selection significantly influences the patterns of covariation (changes in the structure) of the limbs, leading to changes in bone shape and function.

Research Objective

  • The research aims to understand the impact of artificial selection on the structural and functional relationships between different parts of organisms, in this case, the appendicular skeleton of domestic horses. The primary focus is on how variation in these structures is affected by artificial selection and what impact this process has on phenotypic diversification, i.e., the variation in physical characteristics within a species.

Methods

  • The researchers applied 3D geometric morphometrics, a method used to quantify shape in 3D space, to examine the patterns of integration, or how different traits function together, in the limb bones of various horse breeds.

Findings

  • The study found that artificial selection strongly influences covariation, or the degree to which physical traits change together, which in turn impacts the diversification of physical traits in domestic horses.
  • It was also discovered that this influence varies along the limb, causing modulations in the shape of the bones, possibly as a result of different ligament or muscle development.
  • The results revealed that, in addition to not being constrained by a strong morphological integration, artificial selection has modulated the covariation patterns according to the locomotor specificities of the breeds.

Significance

  • This research is significant as it not only reinforces the understanding that artificial selection contributes to phenotypic diversification, but also highlights how these micro-evolutionary processes impact covariation patterns. It emphasizes the need for further studies on how these changes contribute to the morphological diversification of domestic species.

Cite This Article

APA
Hanot P, Herrel A, Guintard C, Cornette R. (2018). The impact of artificial selection on morphological integration in the appendicular skeleton of domestic horses. J Anat, 232(4), 657-673. https://doi.org/10.1111/joa.12772

Publication

Journal of anatomy
ISSN: 1469-7580
NlmUniqueID: 0137162
Country: England
Language: English
Volume: 232
Issue: 4
Pages: 657-673

Researcher Affiliations

Hanot, Pauline
  • UMR 7209 Archéozoologie et Archéobotanique: Sociétés, Pratiques et Environnements (CNRS, MNHN), Muséum national d'Histoire naturelle, Sorbonne Universités, Paris, France.
Herrel, Anthony
  • UMR 7179 Mécanismes Adaptatifs et Évolution (CNRS, MNHN), Muséum national d'Histoire naturelle, Sorbonne Universités, Paris, France.
Guintard, Claude
  • École Nationale Vétérinaire, de l'Agroalimentaire et de l'Alimentation, Nantes Atlantique - ONIRIS, Nantes Cedex 03, France.
Cornette, Raphaël
  • UMR 7205 Institut de Systématique, Évolution, Biodiversité (CNRS, MNHN, UPMC, EPHE), Muséum national d'Histoire naturelle, Sorbonne Universités, Paris, France.

MeSH Terms

  • Animals
  • Biodiversity
  • Body Size
  • Bone and Bones / anatomy & histology
  • Breeding
  • Extremities / anatomy & histology
  • Extremities / growth & development
  • Female
  • Horses / anatomy & histology
  • Horses / growth & development
  • Ligaments / growth & development
  • Ligaments / physiology
  • Locomotion / physiology
  • Male
  • Muscle Development / physiology
  • Phenotype

References

This article includes 68 references
  1. Adams DC. Evaluating modularity in morphometric data: challenges with the RV coefficient and a new test measure.. Methods Ecol Evol 7, 565–572.
  2. Adams DC, Otárola‐Castillo E. geomorph: an R package for the collection and analysis of geometric morphometric shape data.. Methods Ecol Evol 4, 393–399.
    doi: 10.1111/2041-210X.12035google scholar: lookup
  3. Baylac M. Rmorph: A R Geometric and Multivariate Morphometrics Library.. .
  4. Bertram JE, Biewener AA. Bone curvature: sacrificing strength for load predictability?. J Theor Biol 1988 Mar 7;131(1):75-92.
    doi: 10.1016/S0022-5193(88)80122-Xpubmed: 3419194google scholar: lookup
  5. Biewener AA. Allometry of quadrupedal locomotion: the scaling of duty factor, bone curvature and limb orientation to body size.. J Exp Biol 1983 Jul;105:147-71.
    pubmed: 6619724doi: 10.1242/jeb.105.1.147google scholar: lookup
  6. Biewener AA. Muscle-tendon stresses and elastic energy storage during locomotion in the horse.. Comp Biochem Physiol B Biochem Mol Biol 1998 May;120(1):73-87.
    pubmed: 9787779doi: 10.1016/s0305-0491(98)00024-8google scholar: lookup
  7. Bookstein FL, Gunz P, Mitteroecker P, Prossinger H, Schaefer K, Seidler H. Cranial integration in Homo: singular warps analysis of the midsagittal plane in ontogeny and evolution.. J Hum Evol 2003 Feb;44(2):167-87.
    pubmed: 12662941doi: 10.1016/s0047-2484(02)00201-4google scholar: lookup
  8. Brooks SA, Makvandi-Nejad S, Chu E, Allen JJ, Streeter C, Gu E, McCleery B, Murphy BA, Bellone R, Sutter NB. Morphological variation in the horse: defining complex traits of body size and shape.. Anim Genet 2010 Dec;41 Suppl 2:159-65.
    pubmed: 21070291doi: 10.1111/j.1365-2052.2010.02127.xgoogle scholar: lookup
  9. Cheverud JM. PHENOTYPIC, GENETIC, AND ENVIRONMENTAL MORPHOLOGICAL INTEGRATION IN THE CRANIUM.. Evolution 1982 May;36(3):499-516.
    pubmed: 28568050doi: 10.1111/j.1558-5646.1982.tb05070.xgoogle scholar: lookup
  10. Cox MC. The Shetland Pony.. .
  11. Crook TC, Cruickshank SE, McGowan CM, Stubbs N, Wakeling JM, Wilson AM, Payne RC. Comparative anatomy and muscle architecture of selected hind limb muscles in the Quarter Horse and Arab.. J Anat 2008 Feb;212(2):144-52.
    pmc: PMC2408980pubmed: 18194205doi: 10.1111/j.1469-7580.2007.00848.xgoogle scholar: lookup
  12. Cruz CD, Thomason JJ, Faramarzi B. Changes in shape of the Standardbred distal phalanx and hoof capsule in response to exercise.. Equine Comp Exerc Physiol 3, 199–208.
  13. . On the 150(th) Anniversary of Darwin's Submission of One of his "Five Great Books", The Variation of Animals and Plants Under Domestication, to his publisher John Murray.. Alzheimers Dement 2016 Jan;12(1):1.
    pubmed: 26710324doi: 10.1016/j.jalz.2015.12.004google scholar: lookup
  14. Denis B. Les races de chevaux en France au XVIIIe siècle. Et les idées relatives à leur amélioration.. Situ Rev Patrim 18, [online].
  15. Drake AG, Klingenberg CP. Large-scale diversification of skull shape in domestic dogs: disparity and modularity.. Am Nat 2010 Mar;175(3):289-301.
    pubmed: 20095825doi: 10.1086/650372google scholar: lookup
  16. Dudley AT, Ros MA, Tabin CJ. A re-examination of proximodistal patterning during vertebrate limb development.. Nature 2002 Aug 1;418(6897):539-44.
    pubmed: 12152081doi: 10.1038/nature00945google scholar: lookup
  17. Dutto DJ, Hoyt DF, Clayton HM, Cogger EA, Wickler SJ. Moments and power generated by the horse (Equus caballus) hind limb during jumping.. J Exp Biol 2004 Feb;207(Pt 4):667-74.
    pubmed: 14718509doi: 10.1242/jeb.00808google scholar: lookup
  18. Dyson SJ, Tranquille CA, Collins SN, Parkin TD, Murray RC. An investigation of the relationships between angles and shapes of the hoof capsule and the distal phalanx.. Equine Vet J 2011 May;43(3):295-301.
    pubmed: 21492206doi: 10.1111/j.2042-3306.2010.00162.xgoogle scholar: lookup
  19. Fabre A‐C, Cornette R, Peigné S. Influence of body mass on the shape of forelimb in musteloid carnivorans.. Biol J Linn Soc 110, 91–103.
  20. Fabre AC, Goswami A, Peigné S, Cornette R. Morphological integration in the forelimb of musteloid carnivorans.. J Anat 2014 Jul;225(1):19-30.
    pmc: PMC4089343pubmed: 24836555doi: 10.1111/joa.12194google scholar: lookup
  21. Fédération Equestre Internationale. Rules for dressage events, 23rd edn. Lausanne: Fédération Equestre Internationale.
  22. Gabriel A, Detilleux J, Jolly S. Etude morphométrique du sabot et du petit sésamoïde du cheval.. Ann Méd Vét 147, 319–340.
  23. Goswami A, Polly PD. The influence of modularity on cranial morphological disparity in Carnivora and Primates (Mammalia).. PLoS One 2010 Mar 3;5(3):e9517.
    pmc: PMC2831076pubmed: 20209089doi: 10.1371/journal.pone.0009517google scholar: lookup
  24. 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 Aug 19;369(1649):20130254.
    pmc: PMC4084539pubmed: 25002699doi: 10.1098/rstb.2013.0254google scholar: lookup
  25. Hallgrímsson B, Willmore K, Hall BK. Canalization, developmental stability, and morphological integration in primate limbs.. Am J Phys Anthropol 2002;Suppl 35:131-58.
    pmc: PMC5217179pubmed: 12653311doi: 10.1002/ajpa.10182google scholar: lookup
  26. Hallgrímsson B, Jamniczky H, Young NM, Rolian C, Parsons TE, Boughner JC, Marcucio RS. Deciphering the Palimpsest: Studying the Relationship Between Morphological Integration and Phenotypic Covariation.. Evol Biol 2009 Dec;36(4):355-376.
    pmc: PMC3537827pubmed: 23293400doi: 10.1007/s11692-009-9076-5google scholar: lookup
  27. Hanot P, Herrel A, Guintard C, Cornette R. Morphological integration in the appendicular skeleton of two domestic taxa: the horse and donkey.. Proc Biol Sci 2017 Oct 11;284(1864).
    pmc: PMC5647294pubmed: 28978726doi: 10.1098/rspb.2017.1241google scholar: lookup
  28. Hanot P, Guintard C, Lepetz S. Identifying domestic horses, donkeys and hybrids from archaeological deposits: a 3D morphological investigation on skeletons.. J Archaeol Sci 78, 88–98.
  29. Henderson K, Pantinople J, McCabe K, Richards HL, Milne N. Forelimb bone curvature in terrestrial and arboreal mammals.. PeerJ 2017;5:e3229.
    pmc: PMC5408721pubmed: 28462036doi: 10.7717/peerj.3229google scholar: lookup
  30. Hendricks BL. International Encyclopedia of Horse Breeds.. Norman, OK: University of Oklahoma Press.
  31. Ishizaki S, Honzawa S, Shinohara A. Relation between body weight and work power in the horse.. Nihon Chikusan Gakkaiho 25, 168–173.
  32. Kashiwamura F, Avgaandorj A, Furumura K. Relationships among body size, conformation, and racing performance in Banei draft racehorses.. J Equine Sci 12, 1–7.
  33. Klingenberg CP. Morphometric integration and modularity in configurations of landmarks: tools for evaluating a priori hypotheses.. Evol Dev 2009 Jul-Aug;11(4):405-21.
    pmc: PMC2776930pubmed: 19601974doi: 10.1111/j.1525-142x.2009.00347.xgoogle scholar: lookup
  34. Klingenberg CP. Cranial integration and modularity: insights into evolution and development from morphometric data.. Hystrix Ital J Mammal 24, 43–58.
  35. Klingenberg CP. Size, shape, and form: concepts of allometry in geometric morphometrics.. Dev Genes Evol 2016 Jun;226(3):113-37.
    pmc: PMC4896994pubmed: 27038023doi: 10.1007/s00427-016-0539-2google scholar: lookup
  36. Langlois B, Froidevaux J, Lamarche L, Legault C, Legault P, Tassencourt L, Théret M. Analyse des liaisons entre la morphologie et l'aptitude au galop au trot et au saut d'obstacles chez le Cheval.. Ann Genet Sel Anim 1978;10(3):443-74.
    pmc: PMC2718918pubmed: 22896112doi: 10.1186/1297-9686-10-3-443google scholar: lookup
  37. Lanyon LE. The influence of function on the development of bone curvature. An experimental study on the rat tibia.. J Zool 192, 457–466.
  38. Lawler RR. Morphological integration and natural selection in the postcranium of wild verreaux's sifaka (Propithecus verreauxi verreauxi).. Am J Phys Anthropol 2008 Jun;136(2):204-13.
    pubmed: 18322916doi: 10.1002/ajpa.20795google scholar: lookup
  39. Leach DH. Treatment and pathogenesis of navicular disease ('syndrome') in horses.. Equine Vet J 1993 Nov;25(6):477-81.
    pubmed: 8275993doi: 10.1111/j.2042-3306.1993.tb02997.xgoogle scholar: lookup
  40. Lizet B. La Bête noire: À la recherche du cheval parfait.. Paris: Les Editions de la MSH.
  41. Lynghaug F. The Official Horse Breeds Standards Guide: The Complete Guide to the Standards of All North American Equine Breed Associations.. Saint Paul: MBI Publishing Company.
  42. Magwene PM. New tools for studying integration and modularity.. Evolution 2001 Sep;55(9):1734-45.
    pubmed: 11681729doi: 10.1111/j.0014-3820.2001.tb00823.xgoogle scholar: lookup
  43. Marroig G, Cheverud JM. A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of new world monkeys.. Evolution 2001 Dec;55(12):2576-600.
    pubmed: 11831671doi: 10.1111/j.0014-3820.2001.tb00770.xgoogle scholar: lookup
  44. Martín-Serra A, Figueirido B, Pérez-Claros JA, Palmqvist P. Patterns of morphological integration in the appendicular skeleton of mammalian carnivores.. Evolution 2015 Feb;69(2):321-40.
    pubmed: 25403786doi: 10.1111/evo.12566google scholar: lookup
  45. Milne N. Curved bones: An adaptation to habitual loading.. J Theor Biol 2016 Oct 21;407:18-24.
    pubmed: 27444401doi: 10.1016/j.jtbi.2016.07.019google scholar: lookup
  46. Mitteroecker P, Bookstein F. The conceptual and statistical relationship between modularity and morphological integration.. Syst Biol 2007 Oct;56(5):818-36.
    pubmed: 17934997doi: 10.1080/10635150701648029google scholar: lookup
  47. Monteiro LR. Multivariate regression models and geometric morphometrics: the search for causal factors in the analysis of shape.. Syst Biol 1999 Mar;48(1):192-9.
    pubmed: 12078640doi: 10.1080/106351599260526google scholar: lookup
  48. Mulliez J. Les Chevaux du Royaume. Histoire de l’élevage du cheval et de la création des haras.. Paris:Montalba.
  49. Musset R. L’élevage du cheval en France.. Paris:Librairie Agricole de la Maison Rustique.
  50. Olson EC, Miller RL. Morphological Integration.. Chicago, IL: University of Chicago Press.
  51. Olson EC, Miller RL. A Mathematical Model Applied to a Study of the Evolution of Species.. Evolution 5, 325–338.
  52. Pagnier C‐J. Théorie de l'extérieur du cheval: Précédée d'un abrégé des os qui forment le squelette, et d'une nomenclature des principaux organes.. Paris: Madame Huzard.
  53. Rohlf FJ, Corti M. Use of two-block partial least-squares to study covariation in shape.. Syst Biol 2000 Dec;49(4):740-53.
    pubmed: 12116437doi: 10.1080/106351500750049806google scholar: lookup
  54. Rohlf FJ, Slice D. Extensions of the procrustes method for the optimal superimposition of landmarks.. Syst Biol 39, 40–59.
  55. Rolian C. Integration and evolvability in primate hands and feet.. Evol Biol 36, 100–117.
  56. Ruff C. Hindlimb articular surface allometry in hominoidea and Macaca, with comparisons to diaphyseal scaling.. J Hum Evol 17, 687–714.
  57. Schlager S. Morpho and Rvcg–shape analysis in R. In: Statistical Shape and Deformation Analysis (eds Zheng G, Li S, Szekely G.), pp. 217–256. Cambridge: Academic Press.
  58. Sponenberg DP. Genetic resources and their conservation. In: The Genetics of the Horse (eds Bowling AT, Ruvinsky A.), pp. 387–438. Wallingford: CABI.
  59. Sponenberg DP, Christman C. A Conservation Breeding Handbook.. Pittsboro:American Livestock Breeds Conservancy.
  60. Sun X, Mariani FV, Martin GR. Functions of FGF signalling from the apical ectodermal ridge in limb development.. Nature 2002 Aug 1;418(6897):501-8.
    pubmed: 12152071doi: 10.1038/nature00902google scholar: lookup
  61. Tickle C, Wolpert L. The progress zone -- alive or dead?. Nat Cell Biol 2002 Sep;4(9):E216-7.
    pubmed: 12205485doi: 10.1038/ncb0902-e216google scholar: lookup
  62. Van Valen L. The study of morphological integration.. Evolution 19, 347–349.
  63. Wagner GP, Altenberg L. PERSPECTIVE: COMPLEX ADAPTATIONS AND THE EVOLUTION OF EVOLVABILITY.. Evolution 1996 Jun;50(3):967-976.
    pubmed: 28565291doi: 10.1111/j.1558-5646.1996.tb02339.xgoogle scholar: lookup
  64. Wagner GP, Pavlicev M, Cheverud JM. The road to modularity.. Nat Rev Genet 2007 Dec;8(12):921-31.
    pubmed: 18007649doi: 10.1038/nrg2267google scholar: lookup
  65. Wiley DF, Amenta N, Alcantara DA. Evolutionary morphing. In: VIS 05. IEEE Visualization, 2005. Presented at the VIS 05. IEEE Visualization, 2005, pp. 431–438.
  66. Wolpert L. The progress zone model for specifying positional information.. Int J Dev Biol 2002;46(7):869-70.
    pubmed: 12455622
  67. Young NM, Hallgrímsson B. Serial homology and the evolution of mammalian limb covariation structure.. Evolution 2005 Dec;59(12):2691-704.
    pubmed: 16526515
  68. Young NM, Wagner GP, Hallgrímsson B. Development and the evolvability of human limbs.. Proc Natl Acad Sci U S A 2010 Feb 23;107(8):3400-5.
    pmc: PMC2840520pubmed: 20133636doi: 10.1073/pnas.0911856107google scholar: lookup

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This article has been cited 11 times.
  1. Landry Z, Roloson MJ, Fraser D. Investigating the reliability of metapodials as taxonomic Indicators for Beringian horses. J Mamm Evol 2022;29(4):863-875.
    doi: 10.1007/s10914-022-09626-4pubmed: 36438779google scholar: lookup
  2. Conaway MA, Adams DC. An effect size for comparing the strength of morphological integration across studies. Evolution 2022 Oct;76(10):2244-2259.
    doi: 10.1111/evo.14595pubmed: 35971251google scholar: lookup
  3. Hanot P, Bayarsaikhan J, Guintard C, Haruda A, Mijiddorj E, Schafberg R, Taylor W. Cranial shape diversification in horses: variation and covariation patterns under the impact of artificial selection. BMC Ecol Evol 2021 Sep 21;21(1):178.
    doi: 10.1186/s12862-021-01907-5pubmed: 34548035google scholar: lookup
  4. Kelly EM, Marcot JD, Selwood L, Sears KE. The Development of Integration in Marsupial and Placental Limbs. Integr Org Biol 2019;1(1):oby013.
    doi: 10.1093/iob/oby013pubmed: 33791518google scholar: lookup
  5. Feiner N, Jackson ISC, Stanley EL, Uller T. Evolution of the locomotor skeleton in Anolis lizards reflects the interplay between ecological opportunity and phylogenetic inertia. Nat Commun 2021 Mar 9;12(1):1525.
    doi: 10.1038/s41467-021-21757-5pubmed: 33750763google scholar: lookup
  6. MacLaren JA. Biogeography a key influence on distal forelimb variation in horses through the Cenozoic. Proc Biol Sci 2021 Jan 13;288(1942):20202465.
    doi: 10.1098/rspb.2020.2465pubmed: 33434465google scholar: lookup
  7. Pelletier M, Kotiaho A, Niinimäki S, Salmi AK. Identifying early stages of reindeer domestication in the archaeological record: a 3D morphological investigation on forelimb bones of modern populations from Fennoscandia. Archaeol Anthropol Sci 2020;12(8):169.
    doi: 10.1007/s12520-020-01123-0pubmed: 32704330google scholar: lookup
  8. Mallet C, Billet G, Houssaye A, Cornette R. A first glimpse at the influence of body mass in the morphological integration of the limb long bones: an investigation in modern rhinoceroses. J Anat 2020 Oct;237(4):704-726.
    doi: 10.1111/joa.13232pubmed: 32519813google scholar: lookup
  9. 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 Oct 15;19(1):188.
    doi: 10.1186/s12862-019-1520-2pubmed: 31615394google scholar: lookup
  10. López-Aguirre C, Hand SJ, Koyabu D, Son NT, Wilson LAB. Postcranial heterochrony, modularity, integration and disparity in the prenatal ossification in bats (Chiroptera). BMC Evol Biol 2019 Mar 12;19(1):75.
    doi: 10.1186/s12862-019-1396-1pubmed: 30866800google scholar: lookup
  11. Mallet C, Houssaye A. Deciphering the influence of evolutionary legacy and functional constraints on the patella: an example in modern rhinoceroses amongst perissodactyls. PeerJ 2024;12:e18067.
    doi: 10.7717/peerj.18067pubmed: 39469593google scholar: lookup
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