Exceptional Changes in Skeletal Anatomy under Domestication: The Case of Brachycephaly

Abstract

"Brachycephaly" is generally considered a phenotype in which the facial part of the head is pronouncedly shortened. While brachycephaly is characteristic for some domestic varieties and breeds (e.g., Bulldog, Persian cat, Niata cattle, Anglo-Nubian goat, Middle White pig), this phenotype can also be considered pathological. Despite the superficially similar appearance of "brachycephaly" in such varieties and breeds, closer examination reveals that "brachycephaly" includes a variety of different cranial modifications with likely different genetic and developmental underpinnings and related with specific breed histories. We review the various definitions and characteristics associated with brachycephaly in different domesticated species. We discern different types of brachycephaly ("bulldog-type," "katantognathic," and "allometric" brachycephaly) and discuss morphological conditions related to brachycephaly, including diseases (e.g., brachycephalic airway obstructive syndrome). Further, we examine the complex underlying genetic and developmental processes and the culturally and developmentally related reasons why brachycephalic varieties may or may not be prevalent in certain domesticated species. Knowledge on patterns and mechanisms associated with brachycephaly is relevant for domestication research, veterinary and human medicine, as well as evolutionary biology, and highlights the profound influence of artificial selection by humans on animal morphology, evolution, and welfare.

Fig. 1

Summary of brachycephalic varieties in domestic mammal species. Cladogram (branches contain no information on divergence times) shows ancient mammal domesticates (domesticated >500 YBP, see text; tree topology is according to Meredith et al. 2011 and Agnarsson and May-Collado 2008). Gray branches indicate species with at least one variety/breed where a brachycephalic phenotype is considered to occur relatively consistently or is breed defining and not just occurring occasionally, e.g., as a pathology (see text and Table 2). Skulls categorized as “normal” (left column) represent the non-brachycephalic condition in the respective domesticates. Skulls in the other columns represent brachycephalic varieties/breeds, according to the groupings as described in the text (“bulldog type,” “katantognathic,” and “allometric”). Numbers indicate discussed characteristics of the brachycephalic phenotype. It is evident that not all domestic species are represented by brachycephalic varieties and that the phenotype that is usually termed “brachycephalic” is variable in the different species. From left to right and top to bottom: Angora rabbit (Zoologisches Institut/Populationsgenetik [former Institut für Haustierkunde], Christian-Albrechts-Universität zu Kiel, Germany; I.f.H. 6489, mirrored); Polish rabbit (“Hermelinkaninchen,” I.f.H. 5348); domestic cat of unknown breed (I.f.H. 12689); Persian cat (I.f.H. 20428, mirrored); domestic dog of unknown breed (Paleontological Institute and Museum, University of Zurich; PIMUZ A/V 608); Boxer (PIMUZ A/V 2836, mirrored); Chihuahua (Albert Heim collection at the Naturhistorisches Museum Bern, Switzerland; NMBE 1052001); domestic pig of unknown breed (Zoological Museum, University of Zurich; ZMZH 17676); brachycephalic domestic pig of unknown breed (Nehring-Collection [Zoologische Sammlung der Königlichen Landwirtschaftlichen Hochschule zu Berlin] at the Museum für Naturkunde Berlin, Germany; ZMB_Mam_106884); domestic cattle of unknown breed (PIMUZ A/V 2, mirrored); Niata cattle (Natural History Museum of Denmark; NHMD-ZMK-MK-1109, mirrored; courtesy Kristian Murphy Gregersen); mixed breed goat (Center of Natural History, University of Hamburg; ZMH 10895, mirrored); and “Egyptian goat” (“Ägyptische Ziege”; Naturmuseum Wien, Austria; NMW 2074). “Normal” skulls are scaled to the same length across species and brachycephalic skulls are scaled to the non-brachycephalic ones of the same species; scale bars equal 1 cm. Specimens are dentally mature, except the brachycephalic pig. Cattles are shown with (graphically) cut horns. Erratum concerning figure 1e in Veitschegger et al. (2018): the schematic depiction of a brachycephalic cat skull (modified from Schlueter et al. 2009) shows a Persian cat, not a Siamese cat.

Fig. 2

Schematic depiction of systems to discern brachycephalic from non-brachycephalic dogs. Different systems have been suggested to distinguish mesocephalic/mesaticephalic (A and B) from brachycephalic (C and D) domestic dogs. For example, indices of skull length and width (white bars in panels A and C) can be used to quantify the relatively short and broad skulls of brachycephalic varieties/breeds. Further, the angle between cranial base and palate (white bars in panels B and D) can be used to quantify the dorsal rotation of the snout; angles >180° are indicative of airorhynchy. Skulls are scaled to the same length and are housed in the collection of the Albert Heim Foundation at the Naturhistorisches Museum Bern, Switzerland: A and B, NMBE 1050197; C and D, NMBE 1051908.

Fig. 3

Facial shape variation and brachycephaly in domestic ruminants. Certain varieties and breeds of sheep (A; Valais Blacknose sheep) and goats (B; breed unknown, Bangalore, India) exhibit a convex profile of the nose, which is termed “roman nose” (shown as a dashed line in panel C). These variations are mostly relatively mild and do not result in discordance between maxilla and mandible length, as shown on the example of the skull of a Valais Blacknose sheep (C; Musée de la Nature du Valais, Switzerland; HN 2010511). However, in certain goat varieties and breeds, such as Jamnapari/Etawah goats (D), extreme “roman nose” may be associated with an overshot lower jaw and dental malocclusion. The overshot lower jaw and dental malocclusion (dashed circles in panel E) are shown on the example of the skull of an “Egyptian goat” (E; “Ägyptische Ziege”; Naturmuseum Wien, Austria; NMW 2074). These varieties/breeds could be classified as “katantognathic” brachycephalic, where, in addition to the extremely convex nasal bones, parts of the snout (premaxilla) are foreshortened and downward tilted (Fig. 1 and Table 1). In other domestic ruminants, such as cattle, no cases of “katantognathic” brachycephaly are known. Instead, the extinct Niata cattle from South America (F, reconstruction) is characterized by shortened and upward tilted facial bones (G), which is indicative of “bulldog-type” brachycephaly (Fig. 1), and may also lead to dental malocclusion (G). Pictures are not to scale. Credits: A, Benjamin Jost; B, C, E: Madeleine Geiger; D, Shutterstock: Ibenk_88; F, G: Artwork by Jorge González.

Fig. 4

Hypothetical scaling relationship between body size and facial length in any wild animal (white dots) and its domestic counterpart (black dots). The latter exhibit larger intragroup variation of body size and facial length, visualized via more scattering of dots along the common scaling axis (straight line). This comparison exemplifies the difference between “short snoutedness,” i.e., brachycephaly (black dots incorporated into the horizontal box), due to small size (“allometric” brachycephaly) and due to shortening of facial bones not directly resulting from small body size (“bulldog-type” brachycephaly or “katantognathic” brachycephaly). The latter is usually associated with skull modifications, including changes of facial inclination, whereas the former is not per se. Brachycephalic skull proportions may not occur in the respective wild forms. Photographs of skulls depict domestic dogs as an example (for details on specimens, see Fig. 1). The skulls are to scale.

Fig. 5

Examples of craniodental anomalies that may cooccur with “bulldog-type” and “allometric” brachycephaly. (A) An example of a brachycephalic pug (left ventral aspect of cranium; Naturhistorisches Museum Bern, collection of the Albert Heim Foundation, Switzerland; NMBE 1062021) showing crowding of the postcanine teeth and a rotation of the third and fourth upper premolars (P3 and P4) relative to the longitudinal axis of the cranium. Additionally, the second upper molar (M2) is missing (note that there is little space caudal to M1 to house such a tooth). As a comparison, the example of a non-brachycephalic Bernese Mountain Dog (right ventral aspect of skull; NMBE 1050197) below shows the wild-type dental formula and much less to absent dental crowding and rotation. (B) An example of a cleft palate (bony portion) in the cranium of a puppy of a bulldog (photo by R.A.S. of specimen from his personal collection). (C) An example of a 2-year-old Chihuahua (NMBE 1051992) exhibiting persistent open fontanelles and a deciduous canine tooth (dC), next to the permanent canine (C). Usually in dogs, the fontanelle fuses a few days or weeks after birth (De Lahunta and Glass 2009) and the deciduous canines are usually replaced by about a half a year of age (Habermehl 1975). (D) Osseous defects in the parietal and frontal bones of a 5-day-old Persian kitten (Schmidt et al. 2017). Skulls are not to scale. Please note that this list of characteristics is not exhaustive. For more craniodental anomalies associated with brachycephaly, also including soft tissue, see text.

Fig. 6

“Bulldog-type” brachycephaly and its relation to the postcranial skeleton. Although brachycephaly most conspicuously concerns the facial part of the cranium (green) and the mandible (yellow), it may also be correlated with shape variation of the vertebrae (purple, red; note that the brachycephalic dog exhibits a vertebral malformation), scapula (pink), pelvis (olive), and the long bones of the limbs (femur, blue). Most of these bones are stouter in the brachycephalic than in the non-brachycephalic varieties/breeds. Genetic and developmental processes affecting head shape in “bulldog-type” brachycephaly thus also affect the postcranial skeleton to a greater or lesser degree.

Fig. 7

Example of an imaginary variety, the brachycephalic domestic horse. In some domestic species, such as the horse as depicted here, brachycephalic varieties/breeds are not known and might even be perceived grotesque. Artwork by Jaime Chirinos.