Comment on "Sexual selection promotes giraffoid head-neck evolution and ecological adaptation".

Wang et al. (Research Articles, 3 June 2022, eabl8316) reported an early Miocene giraffoid that exhibited fierce head-butting behavior and concluded that sexual selection promoted head-neck evolution in giraffoids. However, we argue that this ruminant is not a giraffoid and thus that the hypothesis that sexual selection promoted giraffoid head-neck evolution is not sufficiently supported.

Low effective mechanical advantage of giraffes' limbs during walking reveals trade-off between limb length and locomotor performance.

Giraffes (Giraffa camelopardalis) possess specialized locomotor morphology, namely elongate and gracile distal limbs. While this contributes to their overall height and enhances feeding behavior, we propose that the combination of long limb segments and modest muscle lever arms results in low effective mechanical advantage (EMA, the ratio of in-lever to out-lever moment arms), when compared with other cursorial mammals. To test this, we used a combination of experimentally measured kinematics and ground reaction forces (GRFs), musculoskeletal modeling, and inverse dynamics to calculate giraffe forelimb EMA during walking. Giraffes walk with an EMA of 0.34 (±0.05 SD), with no evident association with speed within their walking gait. Giraffe EMA was about four times lower than expectations extrapolated from other mammals, ranging from 0.03 to 297 kg, and this provides further evidence that EMA plateaus or even diminishes in mammals exceeding horse size. We further tested the idea that limb segment length is a factor which determines EMA, by modeling the GRF and muscle moment arms in the extinct giraffid Sivatherium giganteum and the other extant giraffid, Okapia johnstoni. Giraffa and Okapia shared similar EMA, despite a four to sixfold difference in body mass (Okapia EMA = 0.38). In contrast, Sivatherium, sharing a similar body mass with Giraffa, had greater EMA (0.59), which we propose reflects behavioral differences, such as a somewhat increased capability for athletic performance. Our modeling approach suggests that limb length is a determinant of GRF moment arm magnitude and that unless muscle moment arms scale isometrically with limb length, tall mammals are prone to low EMA.

Sexual selection promotes giraffoid head-neck evolution and ecological adaptation.

The long neck of the giraffe has been held as a classic example of adaptive evolution since Darwin's time. Here we report on an unusual fossil giraffoid, Discokeryx xiezhi, from the early Miocene, which has an unusual disk-shaped headgear and the most complicated head-neck joints in known mammals. The distinctive morphology and our finite element analyses indicate an adaptation for fierce head-butting behavior. Tooth enamel isotope data suggest that D. xiezhi occupied a niche different from that of other herbivores, comparable to the characteristic high-level browsing niche of modern giraffes. The study shows that giraffoids exhibit a higher headgear diversity than other ruminants and that living in specific ecological niches may have fostered various intraspecific combat behaviors that resulted in extreme head-neck morphologies in different giraffoid lineages.

Pushing the boundary? Testing the "functional elongation hypothesis" of the giraffe's neck.

Although giraffes maintain the usual mammalian cervical number of seven vertebrae, their first thoracic vertebra (T1) exhibits aberrant anatomy and has been hypothesized to functionally elongate the neck. We test this "functional elongation hypothesis" by combining phylogenetically informed analyses of neck length, three-dimensional (3D) vertebral shape, and of the functional significance of shape differences across a broad sample of ruminants and camelids. Digital bone models of the cervicothoracic transition were subjected to 3D geometric morphometric analysis revealing how the shape of the seventh cervical (C7) has converged in several long-necked species. However, we find a unique "cervicalization" of the giraffe's T1. In contrast, we demonstrate a "thoracalization" of C7 for the European bison. Other giraffids (okapi and extinct Sivatherium) did not exhibit "cervicalized" T1 morphology. Quantitative range of motion (ROM) analysis at the cervicothoracic transition in ruminants and camelids confirms the "functional elongation hypothesis" for the giraffe in terms of increased mobility, especially with regard to dorsoventral flexion/extension. Additionally, other factors related to the unique morphology of the giraffe's cervicothoracic transition such as neck posture and intervertebral stability are discussed and should be considered in future studies of giraffe neck evolution.

Giraffes and hominins: reductionist model predictions of compressive loads at the spine base for erect exponents of the animal kingdom.

In humans, compressive stress on intervertebral discs is commonly deployed as a measurand for assessing the loads that act within the spine. Examining this physical quantity is crucially beneficial: the intradiscal pressure can be directly measured in vivo in humans, and is immediately related to compressive stress. Hence, measured intradiscal pressure data are very useful for validating such biomechanical animal models that have the spine incorporated, and can, thus, compute compressive stress values. Here, we use human intradiscal pressure data to verify the predictions of a reductionist spine model, which has in fact only one joint degree of freedom. We calculate the pulling force of one lumped anatomical structure that acts past this (intervertebral) joint at the base of the spine, lumbar in hominins, cervical in giraffes, to compensate the torque that is induced by the weight of all masses located cranially to the base. Given morphometric estimates of the human and australopith trunks, respectively, and the giraffe's neck, as well as the respective structures' lever arms and disc areas, we predict, for all three species, the compressive stress on the intervertebral disc at the spine base, while systematically varying the angular orientation of the species' spinal columns with respect to gravity. The comparison between these species demonstrates that hominin everyday compressive disc stresses are lower than those in big quadrupedal animals. Within each species, erecting the spine from being bent forward by, for example, thirty degrees to fully upright posture reduces the compressive disc stress roughly to a third. We conclude that erecting the spine immediately allows the carrying of extra loads of the order of body weight, and yet the compressive disc stress is lower than in a moderately forward-bent posture with no extra load.

Formation, structure, and function of extra-skeletal bones in mammals.

This review describes the formation, structure, and function of bony compartments in antlers, horns, ossicones, osteoderm and the os penis/os clitoris (collectively referred to herein as AHOOO structures) in extant mammals. AHOOOs are extra-skeletal bones that originate from subcutaneous (dermal) tissues in a wide variety of mammals, and this review elaborates on the co-development of the bone and skin in these structures. During foetal stages, primordial cells for the bony compartments arise in subcutaneous tissues. The epithelial-mesenchymal transition is assumed to play a key role in the differentiation of bone, cartilage, skin and other tissues in AHOOO structures. AHOOO ossification takes place after skeletal bone formation, and may depend on sexual maturity. Skin keratinization occurs in tandem with ossification and may be under the control of androgens. Both endochondral and intramembranous ossification participate in bony compartment formation. There is variation in gradients of density in different AHOOO structures. These gradients, which vary according to function and species, primarily reduce mechanical stress. Anchorage of AHOOOs to their surrounding tissues fortifies these structures and is accomplished by bone-bone fusion and Sharpey fibres. The presence of the integument is essential for the protection and function of the bony compartments. Three major functions can be attributed to AHOOOs: mechanical, visual, and thermoregulatory. This review provides the first extensive comparative description of the skeletal and integumentary systems of AHOOOs in a variety of mammals.

Comparative study of the eyelids and orbital glands morphology in the okapi (Okapia johnstoni, Giraffidae), Père David's deer (Elaphurus davidianus, Cervidae) and the Philippine mouse-deer (Tragulus nigricans, Tragulidae).

The accessory organs of the eye represent part of the protective system of the eyeball. In the present study, an examination of the accessory organs of the eye of three species of captive ruminants was performed using light microscopy. In the okapi, the superficial gland of the third eyelid and lacrimal gland were complex branched multilobar tubular glands formed by mucous units with tubular secretory portions and no plasma cells. The deep gland of the third eyelid was absent in the okapi and present in both the Père David's deer and the Philippine mouse-deer. In the Philippine mouse-deer, the deep gland had a very thick connective capsule and thick interlobar septae. It contained fewer lobes forming the gland parenchyma compared to Père David's deer and other ruminants. Organized lymphoid follicles were present within the upper and lower eyelids only in the okapi and Père David's deer, while diffuse lymphocytes were observed in the Philippine mouse-deer. The orbital glands in the Père David's deer had a multilobar tubuloacinar structure with numerous plasma cells and a mucoserous character. In contrast to the Philippine mouse-deer, these glands had a serous character. The presence of several macroscopic and microscopic structural differences of the examined accessory organs of the eye in the three captive ruminant species may be understood within an ecological context and may be associated with different habitat-specific environmental conditions.

Ruminants (Giraffidae and Bovidae) from Kanapoi.

We update here our recent revision of the Kanapoi ruminants and describe recently collected material. We now regard the occurrence of reduncins as doubtful, we revise the identification of a large raphicerin as being more probably Gazella, and we add Gazella cf. janenschi and the Cephalophini to the faunal list. New material of Tragelaphus kyaloi suggests that this species held its head unlike other tragelaphins, and was not an exclusive dedicated browser, but Kanapoi pre-dates the Pliocene change of Sivatherium, Aepyceros, Alcelaphini, and even Tragelaphini toward more grazing diets. Kanapoi shares several ruminant taxa with sites in Ethiopia and Tanzania, attesting to latitudinal exchanges.

Comparisons of Schansitherium tafeli with Samotherium boissieri (Giraffidae, Mammalia) from the Late Miocene of Gansu Province, China.

We are describing and figuring for the first time skulls of Schansitherium tafeli, which are abundant in the Gansu area of China from the Late Miocene. They were animals about the size of Samotherium with shorter necks that had two pairs of ossicones that merge at the base, which is unlike Samotherium. The anterior ossicones consist of anterior lineations, which may represent growth lines. They were likely mixed feeders similar to Samotherium. Schansitherium is tentatively placed in a very close position to Samotherium. Samotherium and Schansitherium represent a pair of morphologically very similar species that likely coexisted similarly to pairs of modern species, where the main difference is in the ossicones. Pairs of ruminants in Africa, for example, exist today that differ mostly in their horn shape but otherwise are similar in size, shape, and diet. The absence of Schansitherium from Europe is interesting, however, as Samotherium is found in both locations. While is it challenging to interpret neck length and ossicone shape in terms of function in combat, we offer our hypothesis as to how the two species differed in their fighting techniques.

Evaluation of somatotype in the reticulated giraffe (Giraffa camelopardalis reticulata) using three-dimensional laser measurement.

The giraffe (Giraffa camelopardalis) is a difficult animal to keep in captivity as it has high mortality due to nutrition-related disorders, perhaps because the giraffe's condition is difficult to evaluate. Image analysis techniques have recently become popular and may be useful for evaluating the giraffe's somatotype. The present study aimed to evaluate the giraffe somatotype using a three-dimensional laser measurement device, and to examine the usefulness of this method. First, ten zoo staff members visually evaluated the somatotypes of three giraffes housed at Kanazawa Zoological Gardens, Japan. Next, three-dimensional point cloud datasets were obtained from these giraffes using the device. The point cloud datasets indicated that the cross-sectional area and width of the largest giraffe's body were large in the abdominal region in the transverse sections. However, by visual examination, the ten zoo staff members deemed a different giraffe to be the largest. These results indicated that the three-dimensional laser measurement device could be used to evaluate giraffe somatotype in detail, and that this method may be an alternative to visual evaluation.

Glycosylation and immunocytochemistry of binucleate cells in pronghorn (Antilocapra americana, Antilocapridae) show features of both Giraffidae and Bovidae.

Although the pronghorn (Antilocapra americana) resembles an antelope, its nearest relatives are the giraffe and okapi. In this study we have examined the placentae of 6 pronghorns using lectin- and immunocytochemistry to identify giraffid and bovid features. Binucleate cells (BNC) of the placenta exhibited features intermediate between those of the giraffe and bovine; Dolichos biflorus agglutinin binding - strong in the bovine BNC and absent in the giraffe - was evident in only a subpopulation of BNC while binding to blood vessels, as in the giraffe. Binding of Phytolacca americana agglutinin resembled that of the giraffe and okapi whereas many other glycans were found in all four clades. PAG antigens were similar to bovine and okapi but not giraffe. In summary, although the pronghorn outwardly resembles an antelope, placental BNC show giraffid features. Although each clade has its own individual characteristics, there are far more similarities than differences between them, emphasizing the common ancestry of all four clades.

The earliest ossicone and post-cranial record of Giraffa.

The oldest Giraffa material presently known consists of dental specimens. The oldest post-cranial Giraffa material belongs to the Plio-Pleistocene taxon Giraffa sivalensis, where the holotype is a third cervical vertebra. We describe three non-dental specimens from the Early Late Miocene of the Potwar Plateau, including an 8.1 million year old ossicone, 9.4 million year old astragalus, and 8.9 million year old metatarsal and refer them to Giraffa. The described ossicone exhibits remarkable similarities with the ossicones of a juvenile modern giraffe, including the distribution of secondary bone growth, posterior curvature, and concave pitted undersurface where the ossicone would attach to the skull. The astragalus has a notably flat grove of the trochlea, medial twisting between the trochlea and the head, and a square-shaped sustentacular facet, all of which characterize the astragalus of Giraffa camelopardalis. The newly described astragalus is narrow and rectangular, unlike the boxy shaped bone of the modern giraffe. The metatarsal is large in size and has a shallow central trough created by thin medial and lateral ridges, a feature unique to Giraffa and Sivatherium. Our described material introduce the earliest non-dental material of Giraffa, a genus whose extinct representation is otherwise dominated by teeth, and demonstrate that the genus has been morphologically consistent over 9 million years.

The Brain of the Giraffe (Giraffa Camelopardalis): Surface Configuration, Encephalization Quotient, and Analysis of the Existing Literature.

The anatomy of the giraffe (Giraffa camelopardalis Linnaeus, 1758) has been poorly studied, except for the circulatory system. In particular, only a handful of studies have concerned the brain of this species since the first description in 1839. Accordingly, only a very few articles discussing encephalization mentioned the giraffe or used it in their calculations. In this article, we performed a thorough examination of the literature including old and grey, regarding the central nervous system of the giraffe. Furthermore, we examined the brain of 3 giraffes, and calculated the encephalization quotient (EQ) of the species, based on our own data and the values found in the literature. We also revised the pre-existing literature and re-mapped the main sulci based on current comparative interpretation and anatomical nomenclature. Our results were compared to those of other selected significant mammals. The mean brain weight was of 719.9 ± 12.5 g. Our data indicate that the EQ of the giraffe is 0.64 and matches that of the typical ungulate, despite having the largest brain among terrestrial Cetartiodactyla. This emphasizes that the giraffe is a highly specialized mammal, within the limitations of its clad. Anat Rec, 300:1502-1511, 2017. © 2017 Wiley Periodicals, Inc.

Histological features of the vomeronasal organ in the giraffe, Giraffa camelopardalis.

The vomeronasal organ (VNO) that preferentially detects species-specific substances is diverse among animal species, and its morphological properties seem to reflect the ecological features of animals. This histological study of two female reticulated giraffes (Giraffa camelopardalis reticulata) found that the VNO is developed in giraffes. The lateral and medial regions of the vomeronasal lumen were covered with sensory and nonsensory epithelia, respectively. The vomeronasal glands were positive for periodic acid-Schiff and alcian blue (pH 2.5) stains. The VNO comprises several large veins like others in the order Cetartiodactyla, suggesting that these veins function in a pumping mechanism in this order. In addition, numerous thin-walled vessels located immediately beneath the epithelia covering the lumen entirely surrounded the vomeronasal lumen. This sponge-like structure might function as a specific secondary pump in giraffes.

Quantitative Macroscopic Anatomy of the Giraffe (Giraffa camelopardalis) Digestive Tract.

Quantitative data on digestive anatomy of the world's largest ruminant, the giraffe, are scarce. Data were collected from a total of 25 wild-caught and 13 zoo-housed giraffes. Anatomical measures were quantified by dimension, area or weight and analysed by allometric regression. The majority of measures scaled positively and isometrically to body mass. Giraffes had lower tissue weight of all stomach compartments and longer large intestinal length than cattle. When compared to other ruminants, the giraffe digestive tract showed many of the convergent morphological adaptations attributed to browsing ruminants, for example lower reticular crests, thinner ruminal pillars and smaller surface area of the omasal laminae. Salivary gland weight of the giraffe, however, resembled that of grazing ruminants. This matches a previous finding of similarly small salivary glands in the other extant giraffid, the okapi (Okapia johnstoni), suggesting that not all convergent characteristics need be expressed in all species and that morphological variation between species is a combination of phylogenetic and adaptational signals.

Giraffe genome sequence reveals clues to its unique morphology and physiology.

The origins of giraffe's imposing stature and associated cardiovascular adaptations are unknown. Okapi, which lacks these unique features, is giraffe's closest relative and provides a useful comparison, to identify genetic variation underlying giraffe's long neck and cardiovascular system. The genomes of giraffe and okapi were sequenced, and through comparative analyses genes and pathways were identified that exhibit unique genetic changes and likely contribute to giraffe's unique features. Some of these genes are in the HOX, NOTCH and FGF signalling pathways, which regulate both skeletal and cardiovascular development, suggesting that giraffe's stature and cardiovascular adaptations evolved in parallel through changes in a small number of genes. Mitochondrial metabolism and volatile fatty acids transport genes are also evolutionarily diverged in giraffe and may be related to its unusual diet that includes toxic plants. Unexpectedly, substantial evolutionary changes have occurred in giraffe and okapi in double-strand break repair and centrosome functions.

Astragalar Morphology of Selected Giraffidae.

The artiodactyl astragalus has been modified to exhibit two trochleae, creating a double pullied structure allowing for significant dorso-plantar motion, and limited mediolateral motion. The astragalus structure is partly influenced by environmental substrates, and correspondingly, morphometric studies can yield paleohabitat information. The present study establishes terminology and describes detailed morphological features on giraffid astragali. Each giraffid astragalus exhibits a unique combination of anatomical characteristics. The giraffid astragalar morphologies reinforce previously established phylogenetic relationships. We find that the enlargement of the navicular head is a feature shared by all giraffids, and that the primitive giraffids possess exceptionally tall astragalar heads in relation to the total astragalar height. The sivatheres and the okapi share a reduced notch on the lateral edge of the astragalus. We find that Samotherium is more primitive in astragalar morphologies than Palaeotragus, which is reinforced by tooth characteristics and ossicone position. Diagnostic anatomical characters on the astragalus allow for giraffid species identifications and a better understanding of Giraffidae.