Why the long face? Comparative shape analysis of miniature, pony, and other horse skulls reveals changes in ontogenetic growth.
Abstract: Much of the shape variation found in animals is based on allometry and heterochrony. Horses represent an excellent model to investigate patterns of size-shape variation among breeds that were intentionally bred for extreme small and large sizes. Methods: We tested whether ponies (wither height < 148 cm) have a diverging size-shape relationship in skull shape as compared to regular-sized horse breeds (wither height > 148 cm, here-after called horses) during ontogenetic growth. We used a dataset of 194 specimens from 25 horse and 13 pony breeds, two of which are miniature breeds (wither height < 96.5 cm)-Falabella, Shetland. We applied three-dimensional geometric morphometrics, linear measurements, and multivariate analyses (Procrustes ANOVAs) to quantitatively examine and compare the ontogenetic trajectories between pony and horse breeds with an emphasis on the miniature breeds as an extreme case of artificial selection on size. Additionally, we tested for juvenile characteristics in adult horse and miniature breeds that could resemble "paedomorphosis"-retention of juvenile characteristics in adult stage; e.g. large eyes, large braincase-to-face-relationship, and large head-to-body relationship. Results: Allometric regression of size on shape revealed that 42% of shape variation could be explained by variation in size in all breeds. The ontogenetic trajectories of ponies and horses vary in slope and therefore in rate of change per unit size, and length. The differences in trajectory lengths and slopes result in ponies having a similar skull shape in an older age stage than horses of the same size in a younger age stage. This pattern could cause the generally perceived "paedomorphic" appearance of ponies. Miniature breeds have larger heads in relation to wither height compared to horses, a non-paedomorphic feature in horses specifically. Also, rostra (faces) are longer in adult individuals than in juveniles across all kinds of breeds. This pattern can be explained by the long-face hypothesis for grazing ungulates and could possibly be caused by the mismatch of selection by humans for shorter rostra and the dentition of ruminants. Conclusions: Miniature breed specimens do not exhibit any of the classical mammalian "paedomorphic" features (large orbits, large heads), except for the adult Falabella that has enlarged orbits, possibly because they are herbivorous ungulates that are affected by functional and metabolic constraints related to low nutrient-food consumption. Instead ponies, including miniature breeds, have faster and shorter ontogenetic growth compared to horses, resulting in adult pony skulls looking in part like juvenile horse skulls.
©2019 Heck et al.
Publication Date: 2019-09-16 PubMed ID: 31576240PubMed Central: PMC6752190DOI: 10.7717/peerj.7678Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
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.
The research investigates the variations in skull shape among different breeds of horses- particularly regular-sized, pony, and miniature breeds- and the effects of size and shape on their growth process. The study sheds light on some of the characteristics found in these horse breeds that could be attributed to “paedomorphosis” – the retention of juvenile traits in the adult stage.
Methods Used in the Research
- The researchers used a dataset of 194 specimens which included 25 horse breeds and 13 pony breeds, including two miniature breeds – Falabella and Shetland.
- They employed three-dimensional geometric morphometrics, linear measurements, and multivariate analyses (Procrustes ANOVAs) to quantitatively assess and compare the growth trajectories of pony and horse breeds, with a special emphasis on miniature breeds.
- The team also sought to identify any juvenile features present in adult horses and miniature breeds that could be an indication of “paedomorphosis”.
Key Findings of the Research
- It was discovered that 42% of shape variation within all breeds could be accounted for by variations in size.
- The pace of change per unit size, or rate, and the ontogenetic trajectories’ lengths varied between horses and ponies. As a result of these variations, older ponies had similar skull shapes to younger horses of the same size.
- The pattern mentioned above could be a potential explanation for the paedomorphic appearances often seen in ponies.
- Miniature breeds were found to possess larger heads in relation to wither height, a trait that is absent in regular-sized horses. Additionally, across all breeds, adults had longer faces than juveniles – a pattern possibly explained by the long-face hypothesis for grazing ungulates.
Conclusions of the Research
- The study concluded that miniature breeds do not display most traditional mammalian “paedomorphic” traits (apart from adult Falabellas having larger eye sockets).
- It was proposed that this lack of paedomorphic traits could be due to the metabolic and functional constraints faced by herbivorous ungulates who consume low nutrient-foods.
- The researchers noted that ponies, including miniature breeds, experience faster and shorter growth compared to regular horses, making adult pony skulls appear similar to juvenile horse skulls in some aspects.
Cite This Article
APA
Heck L, Sanchez-Villagra MR, Stange M.
(2019).
Why the long face? Comparative shape analysis of miniature, pony, and other horse skulls reveals changes in ontogenetic growth.
PeerJ, 7, e7678.
https://doi.org/10.7717/peerj.7678 Publication
Researcher Affiliations
- Palaeontologisches Institut und Museum, University of Zürich, Zürich, Switzerland.
- Palaeontologisches Institut und Museum, University of Zürich, Zürich, Switzerland.
- Department of Biology & Redpath Museum, McGill University, Montréal, Q, Canada.
Conflict of Interest Statement
The authors declare there are no competing interests.
References
This article includes 52 references
- Adams DC, Collyer ML. On the comparison of the strength of morphological integration across morphometric datasets.. Evolution 2016;70:2623–2631.
- Adams DC, Collyer ML, Kaliontzopoulou A, Sherratt E. Geomorph: software for geometric morphometric analyses. R package version 3.0.7. 2018.
- Adams DC, Nistri A. Ontogenetic convergence and evolution of foot morphology in European cave salamanders (Family: Plethodontidae). BMC Evolutionary Biology 2010;10:216.
- Adams DC, Rohlf FJ, Slice DE. A field comes of age: geometric morphometrics in the 21st century.. Hystrix 2013;24:7–14.
- Adams DC, Rohlf FJ, Slice DE, Adams DC, Rohlf FJ, Geometric DES, Adams DC. Geometric morphometrics: ten years of progress following the ‘revolution’.. Italian Journal of Zoology 2004;71:5–16.
- Alberch P, Gould S, Oster G, Wake D. Size and shape in ontogeny and phylogeny.. Paleobiology 1979;5:296–231.
- Böhmer C, Böhmer E. Shape variation in the craniomandibular system and prevalence of dental problems in domestic rabbits: a case study in evolutionary veterinary science.. Veterinary Sciences 2017;4.
- Bookstein FL. Introduction to methods for landmark data.. 1990. pp. 216–225.
- Budiansky S. The nature of horses: exploring equine evolution, intelligence, and behavior.. Simon & Schuster Inc; New York: 1997.
- Cardini A, Polly PD. Larger mammals have longer faces because of size-related constraints on skull form.. Nature Communications 2013;4:2458.
- Cardini A, Polly D, Dawson R, Milne N. Why the long face? Kangaroos and wallabies follow the same ‘rule’ of cranial evolutionary allometry (CREA) as placentals.. Evolutionary Biology 2015;42:169–176.
- Collyer ML, Adams DC. Phenotypic trajectory analysis: comparison of shape change patterns in evolution and ecology.. Hystrix 2013;24:75–83.
- Collyer ML, Sekora DJ, Adams DC. A method for analysis of phenotypic change for phenotypes described by high-dimensional data.. Heredity 2015;115:357–365.
- Drake AG, Klingenberg CP. The pace of morphological change: historical transformation of skull shape in St Bernard dogs.. Proceedings of the Royal Society B: Biological Sciences 2008;275(1630):71–76.
- Dryden IL. Shapes: statistical shape analysis. R package version 1.2.4. 2018.
- Evin A, Owen J, Larson G, Debiais-Thibaud M, Cucchi T, Vidarsdottir US, Dobney K. A test for paedomorphism in domestic pig cranial morphology.. Biology Letters 2017;13.
- Fédération Equestre Internationale. Veterinary regulations. 13th Edition. Chapter IV: ponies, article 1042: definitions; p. 60.. FEI Fédération Equestre Internationale; Lausanne: 2016.
- Geiger M, Evin A, Sánchez-Villagra MR, Gascho D, Mainini C, Zollikofer CPE. Neomorphosis and heterochrony of skull shape in dog domestication.. Scientific Reports 2017;7:1–9.
- Geiger M, Haussman S. Cranial suture closure in domestic dog breeds and its relationships to skull morphology.. The Anatomical Record 2016;299:412–420.
- Geist V. Mountain sheep. A study in behavior and evolution.. The University of Chicago Press; Chicago and London: 1974.
- Goodwin D, Bradshaw JWS, Wickens SM. Paedomorphosis affects agonistic visual signals of domestic dogs.. Animal Behaviour 1997;53:297–304.
- Goodwin D, Levine M, McGreevy P. Paedomorphosis: a novel explanation of physical and behavioral differences in horses?.. In: Goodwin D, Heleski C, McGreevy P, McLean A, Randle H, Skelly C, Van Dierendonck M, Waran N, editors. Proceedings of the 3rd international equitation science symposium; Michigan. 2007. p. 21.
- Goodwin D, Levine M, McGreevy PD. Preliminary investigation of morphological differences between ten breeds of horses suggests selection for paedomorphosis.. Journal of Applied Animal Welfare Science 2008;11:204–212.
- Gould JS. The panda’s thumb: more reflections in natural history.. WW Norton & Company, Inc; New York and London: 1980.
- Habermehl K-H. Altersbestimmung bei Haus-und Labortieren.. P. Parey; Berlin and Hamburg: 1975.
- Hare B, Woods V. The genius of dogs.. OneWorld Publications; New York: 2013.
- Hendricks BL. International encyclopedia of horse breeds.. University of Oklahoma Press; Norman, Oklahoma: 2007.
- Hilzheimer M. Natürliche Rassengeschichte der Haussäugetiere.. Walter de Gruyter & co; Berlin and Leipzig: 1926.
- Klingenberg CP, Barluenga M, Meyer A. Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry.. Evolution; International Journal of Organic Evolution 2002;56:1909–1920.
- Kolamunnage R, Kent JT. Principal component analysis for shape variation about an underlying symmetric shape.. Stochastic geometry, biological structure and images, vol. 72; Wilson. 2003. pp. 137–139.
- Kruska DCT, Steffen K. Comparative allometric investigations on the skulls of wild cavies (Cavia aperea) versus domesticated guinea pigs (C. aperea f. porcellus) with comments on the domestication of this species.. Mammalian Biology 2013;78:178–186.
- MacLeod N. Landmarks and semilandmarks: differences without meaning and meaning without difference.. Palaeontological Association Newsletter 2013;82:32–43.
- Morey DF. Size, shape and development in the evolution of the domestic dog.. Journal of Archaeological Science 1992;19:181–204.
- Porto A, De Oliveira FB, Shirai LT, eD Conto V, Marroig G. The evolution of modularity in the mammalian skull I: morphological integration patterns and magnitudes.. Evolutionary Biology 2009;36:118–135.
- Prideaux G. Systematics and evolution of the sthenurine kangaroos.. University of California Publications in Geological Sciences; Berkeley, Los Angeles, London: 2004.
- Radinsky L. Ontogeny and phylogeny in horse skull evolution.. Evolution 1984;38:1–15.
- R Core Team. Vienna: R Foundation for Statistical Computing; 2018.. .
- Rohlf FJ, Slice D. Extensions of the procrustes method for the optimal superimposition of landmarks.. Systematic Biology 1990;39:40–59.
- Sánchez-Villagra MR, Segura V, Geiger M, Heck L, Veitschegger K, Flores D. On the lack of a universal pattern associated with mammalian domestication: differences in skull growth trajectories across phylogeny.. Royal Society Open Science 2017;4.
- Shea BT, Gomez AM. Tooth scaling and evolutionary dwarfism: an investigation of allometry in human pygmies.. American Journal of Physical Anthropology 1988;77:117–132.
- Spencer LM. Morphological Correlates of dietary resource partitioning in the african bovidae.. Journal of Mammalogy 1995;76:448–471.
- Tamagnini D, Meloro C, Cardini A. Anyone with a long-face? Craniofacial evolutionary allometry (CREA) in a family of short-faced mammals, the Felidae.. Evolutionary Biology 2017;44:476–495.
- Van Heel MCV, Kroekenstoel AM, Van Dierendonck MC, Van Weeren PR, Back W. Uneven feet in a foal may develop as a consequence of lateral grazing behaviour induced by conformational traits.. Equine Veterinary Journal 2006;38:646–651.
- Veitschegger K, Wilson LAB, Nussberger B, Camenisch G, Keller LF, Wroe S, Sánchez-Villagra MR. Resurrecting Darwin’s Niata—anatomical, biomechanical, genetic, and morphometric studies of morphological novelty in cattle.. Scientific Reports 2018;8:9129.
- Verzani J. Using R for introductory statistics.. CRC Press, Taylor & Francis; New York: 2014.
- Waller BM, Peirce K, Caeiro CC, Scheider L, Burrows AM, McCune S, Kaminski J. Paedomorphic facial expressions give dogs a selective advantage.. PLOS ONE 2013;8:e82686.
- Wayne RK. Cranial morphology of domestic and wild canids: the influence of development on morphological change.. Evolution 1986;40:243–261.
- Wayne KW. Consequences of domestication: morphological diversity of the dog.. In: Ruvinsky A, Sampson J, editors. The genetics of the dog. CAB International; Wallingford: 2001. pp. 43–59.
- Werneburg I, Geiger M. Ontogeny of domestic dogs and the developmental foundations of carnivoran domestication.. Journal of Mammalian Evolution 2017;24:323–343.
- Wilson G. Commissurotomy for oral access and tooth extraction in a dwarf miniature pony.. Journal of Veterinary Dentistry 2012;29:250–252.
- Wilson LAB. The evolution of ontogenetic allometric trajectories in mammalian domestication.. Evolution 2018;72:867–877.
- World Class Miniature Horse Registry 2018. https://www.wcmhr.org/main.sc. [20 July 2018]. https://www.wcmhr.org/main.sc
Citations
This article has been cited 11 times.- Matos JI, Pitti L, Parra-Quijano M, Arencibia A, Ramírez G, Díaz-Bertrana ML. Integrative anatomical and two-dimensional ultrasonographic assessment of the heart in Shetland ponies. Front Vet Sci 2025;12:1721000.
- Ming KM, Le Verger K, Geiger M, Schmelzle T, Georgalis GL, Shimbo G, Sasaki M, Ohdachi SD, Sánchez-Villagra MR. Insular dwarfism in horses from the Aegean Sea and the Japanese archipelago. Mamm Biol 2024;104(4):345-361.
- Bordin C, Raspa F, Greppi M, Harris P, Ellis AD, Roggero A, Palestrini C, Cavallini D, Bergero D, Valle E. Pony feeding management: the role of morphology and hay feeding methods on intake rate, ingestive behaviors and mouth shaping. Front Vet Sci 2024;11:1332207.
- Tani T. Immortalization of American miniature horse-derived fibroblast by cell cycle regulator with normal karyotype. PeerJ 2024;12:e16832.
- Tinsley T, Fogle C, Means E, Robertston J. The prevalence and risk factors of dental disease found in 100 miniature horses. Front Vet Sci 2023;10:1239809.
- Salamanca-Carreño A, Parés-Casanova PM, Monroy-Ochoa NI, Vélez-Terranova M. Would the Cephalic Development in the Purebred Arabian Horse and Its Crosses Indicate a Paedomorphic Process?. Animals (Basel) 2022 Nov 16;12(22).
- Geiger M, Sánchez-Villagra MR, Sherratt E. Cranial shape variation in domestication: A pilot study on the case of rabbits. J Exp Zool B Mol Dev Evol 2022 Dec;338(8):532-541.
- Clauss M, Heck L, Veitschegger K, Geiger M. Teeth out of proportion: Smaller horse and cattle breeds have comparatively larger teeth. J Exp Zool B Mol Dev Evol 2022 Dec;338(8):561-574.
- 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.
- Geiger M, Schoenebeck JJ, Schneider RA, Schmidt MJ, Fischer MS, Sánchez-Villagra MR. Exceptional Changes in Skeletal Anatomy under Domestication: The Case of Brachycephaly. Integr Org Biol 2021;3(1):obab023.
- Parés-Casanova PM, Salamanca-Carreño A, Crosby-Granados RA, Bentez-Molano J. A Comparison of Traditional and Geometric Morphometric Techniques for the Study of Basicranial Morphology in Horses: A Case Study of the Araucanian Horse from Colombia. Animals (Basel) 2020 Jan 10;10(1).
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists