Convergent metatarsal fusion in jerboas and chickens is mediated by similarities and differences in the patterns of osteoblast and osteoclast activities

In many vertebrate animals that run or leap, the metatarsals and/or metacarpals of the distal limb are fused into a single larger element, likely to resist fracture due to high ground‐reaction forces during locomotion. Although metapodial fusion evolved independently in modern birds, ungulates, and jerboas, the developmental basis has only been explored in chickens, which diverged from the mammalian lineage approximately 300 million years ago. Here, we use a bipedal rodent, the lesser Egyptian jerboa (Jaculus jaculus), to understand the cellular processes of metatarsal fusion in a mammal, and we revisit the developing chicken to assess similarities and differences in the localization of osteoblast and osteoclast activities. In both species, adjacent metatarsals align along flat surfaces, osteoblasts cross the periosteal membrane to unite the three elements in a single circumference, and osteoclasts resorb bone at the interfaces leaving a single marrow cavity. However, the pattern of osteoclast activity differs in each species; osteoclasts are highly localized to resorb bone at the interfaces of neighboring jerboa metatarsals and are distributed throughout the endosteum of chicken metatarsals. Each species, therefore, provides an opportunity to understand mechanisms that pattern osteoblast and osteoclast activities to alter bone shape during development and evolution.     

Genetic differentiation and relationship of the dipodidsAllactaga andJaculus (Mammalia, Rodentia) in Egypt based on protein variation

Genetic differentiation among 14 populations representing all Egyptian dipodid (jerboa) species and subspecies was examined at 25 structural loci and interspecific relationships are discussed. Of the 25 loci, only 3 were monomorphic, with the same allele fixed in all taxa, 9 loci were monomorphic, but demonstrated intertaxon variation, and only 13 loci were polymorphic. The overall mean number of alleles per locus (A) was 1.23 ± 0.02 and the average percentage of polymorphic loci per taxon (P) was 23%. The overall mean of observed heterozygosity (H _o) was found significantly higher than that of expected heterozygosity (He); the overall means per taxon were 0.25 ± 0.017 and 0.085 ± 0.007. Mean levels of genetic identity (I) were 0.970 ± 0.003 among geographic populations, 0.718 ± 0.022 between subspecies, 0.590 ± 0.030 between congeneric species, and 0.368 ± 0.020 between genera. Phenetic analysis of genetic distance matrix produced a phenogram indicating a close association ofJaculus orientalis Erxleben, 1777 toJaculus jaculus (Linnaeus, 1758), particularly to its subspeciesJaculus jaculus butleri (Thomas, 1922), and indicating a distinct affinity between these latter two species andAllactaga tetradactyla (Lichtenstein, 1823). Estimates of genetic divergence demonstrated that J. orientalis appears to have shared a more recent common ancestor withJ. jaculus thanA. tetradactyla. Divergence of these species would have occurred by Miocene (ca 9.6 to 18.7 million years ago). The pattern of relationships of the dipodid species indicated in this study was closely consistent with the hypotheses derived from morphological and chromosomal data.     

Articular to diaphyseal proportions of human and great ape metatarsals

This study proposes a new way to use metatarsals to identify locomotor behavior of fossil hominins. Metatarsal head articular dimensions and diaphyseal strength in a sample of chimpanzees, gorillas, orangutans, and humans (n = 76) are used to explore the relationships of these parameters with different locomotor modes. Results show that ratios between metatarsal head articular proportions and diaphyseal strength of the hallucal and fifth metatarsal discriminate among extant great apes and humans based on their different locomotor modes. In particular, the hallucal and fifth metatarsal characteristics of humans are functionally related to the different ranges of motion and load patterns during stance phase in the forefoot of humans in bipedal locomotion. This method may be applicable to isolated fossil hominin metatarsals to provide new information relevant to debates regarding the evolution of human bipedal locomotion. The second to fourth metatarsals are not useful in distinguishing among hominoids. Further studies should concentrate on measuring other important qualitative and quantitative differences in the shape of the metatarsal head of hominoids that are not reflected in simple geometric reconstructions of the articulation, and gathering more forefoot kinematic data on great apes to better understand differences in range of motion and loading patterns of the metatarsals. Am J Phys Anthropol 143:198–207, 2010. © 2010 Wiley‐Liss, Inc.     

Are there two cryptic species of the lesser jerboa Jaculus jaculus (Rodentia: Dipodidae) in Tunisia? Evidence from molecular,morphometric, and cytogenetic data

Jerboas belonging to the genus Jaculus are widely distributed rodents inhabiting Palearctic desert and semi‐desert areas. Previous studies on the lesser Egyptian jerboa Jaculus jaculus showed the existence of various morphological forms of controversial taxonomic status. They were sometimes related to two different species, J. jaculus and Jaculus deserti, although this has not been recognized in recent taxonomic updates. To clarify the systematic status of J. jaculus in Tunisia, we performed molecular (phylogenetic analyses of cytochrome b sequences), morphological (multivariate analyses of 13 skull measurements) and karyotypic (standard preparations from bone marrow cells) analyses on a number of specimens collected from ten localities. Our analyses revealed two monophyletic, well differentiated clades, with a mean genetic divergence value (K2P = 10.9 ± 0.01%), which is within the range of distances generally observed between rodent species. Morphometric analyses clearly separated populations of the two genetic clades from each other. However, karyotypes of individuals from both clades appeared similar. Individuals from both molecular clades/morphometric groups were found in sympatry in most of the localities sampled. These results, as obtained from a restricted area of the total distribution, suggest that there are two separate species within the currently accepted J. jaculus in Tunisia. Alternative hypotheses such as the occurrence of a strong, ancient phylogeographic structure, or the presence of pseudogenes, are also considered to account for the results obtained. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 673–686.     

Metatarsophalangeal joint function and positional behavior in Australopithecus afarensis

Recent discussions of the pedal morphology of Australopithecus afarensis have led to conflicting interpretations of australopithecine locomotor behavior. We report the results of a study using computer aided design (CAD) software that provides a quantitative assessment of the functional morphology of australopithecine metatarsophalangeal joints. The sample includes A. afarensis, Homo sapiens, Pan troglodytes, Gorilla gorilla, and Pongo pygmaeus. Angular measurements of the articular surfaces relative to the long axes of the metatarsals and phalanges were taken to determine whether the articular surfaces are plantarly or dorsally oriented. Humans have the most dorsally oriented articular surfaces of the proximal pedal phalanges. This trait appears to be functionally associated with dorsiflexion during bipedal stride. Pongo has the most plantarly oriented articular surfaces of the proximal pedal phalanges, probably reflecting an emphasis on plantarflexion in arboreal positional behaviors, while the African hominoids are intermediate between Pongo and Homo for this characteristic. A. afarensis falls midway between the African apes and humans. Results from an analysis of metatarsal heads are inconclusive with regard to the functional morphology of A. afarensis. Overall, the results are consistent with other evidence indicating that A. afarensis was a capable climber. © 1994 Wiley-Liss, Inc.     

The tarsus of rhynchocephalian reptiles

A new reconstruction of the tarsus of Stenaulorhynchus stockleyi differs from that previously offered by von Huene (1938) and Schaeffer (1941), and leads to a revaluation of the tarsi of other rhynchosaurs and rhynchocephalians. The tarsi of the rhynchosaurs Stenaulorhynchus, Scaphonyx, Cephalonia, Rhynchosaurus, Hyperodapedon, Howesia and Mesosuchus appear to comprise a proximal row of three bones (tibiale, intermedium, and fibulare) and a distal row of three bones associated with metatarsals–4. The metatarsals increase in length but decrease in thickness from the first to fourth, and the fifth is "hooked". The first metatarsal of Stenaulorhynchus, Scaphonyx , and Rhynchosaurus is unusually short. Among the remaining rhynchocephalians, the tarsi of claraziids and pleurosaurids are simplified in accord with aquatic habits involving the use of the limbs as paddles, and those of sphenodontids and Sapheosaurus are alike in the following respects. An astragalus (intermedium+tibiale+ centrale) and calcaneum (fibulare), or a single conjoined bone, occupy the proximal row of the tarsus and the distal row comprises four (first to fourth), three (second to fourth), or but two (third and fourth) bones; the fourth is the largest. The metatarsals increase in length from first to fourth but do not decrease in thickness. In both rhynchosaurian and spheno-dontid types tarsal movement is largely mesotarsal, a condition derived from their eosuchian ancestors and not independently developed as Schaeffer (1941) has thought. The specialization of the sphenodontid tarsus parallels that seen in lizards which have the same eosuchian ancestry.     

天津蓟州区桃花园墓地明清时期缠足女性的足骨形变

本文通过量化方法,对桃花园墓地明清时期101例女性足骨形变方式、程度、对称性等进行了系统分析。研究结果表明,双侧足骨形变总体上是对称的。缠足对跗骨的影响主要在于整体尺寸缩小和关节面改变。第1跖骨除整体尺寸缩小外,还存在诸多明显的骨体形态改变;第2、3跖骨头部和底部尺寸缩小,但形变不大。第3至第5近节趾骨骨体长度和高度的侧别差异明显,特别是第3近节趾骨双侧整体不对称。该群体至少在18岁时已经缠足,25岁以后足骨已发生形变,35岁之后形变较明显。部分个体足骨形变程度较轻,其生前可能仅束足纤直,未经裹弯。足骨形变程度与陪葬品多寡并无相关性,其形变差异很可能与身体疾病、劳作需要、缠足方法或缠足观念差异有关。     

Allometric patterning in the limb skeleton of bats: Implications for the mechanics and energetics of powered flight

Allometric analysis was employed to compare linear dimensions of forelimb and hindlimb bones (humeri, radii, third and fifth metacarpals, third and fifth manual phalanges, femora, and tibiae) of 227 species of bats and 105 species of nonvolant mammals of varying degrees of phylogenetic affinity to bats. After accounting for body size, all forelimb bones are longer in bats than in nonvolant species, with the exception of humeri and radii of a few highly arboreal primates. Hindlimb bones are generally, but not uniformly, shorter in bats than in other mammals. For the humerus, radius, and metacarpals, midshaft diameters are greater in bats than in their comparably sized relatives. Proximal phalangeal midshaft diameters are statistically indistinguishable from those of other mammals, and distal phalanges show significantly reduced outer diameters. The pattern of relative reduction in wing bone diameters along the wing's proximodistal axis parallels the reduction in bone mineralization along the same axis, and a similar pattern of change in cortical thickness from the smallest wall thicknesses among mammals in the humerus and radius to the greatest wall thicknesses among mammals in the phalanges. The combination of altered cross-sectional geometry and mineralization appears significantly to reduce the mass moment of inertia of the bat wing relative to a theoretical condition in which elongated bones preserve primitive mammalian mineralization levels and patterns of scaling of long bone diameters. This intercorrelated suite of skeletal specializations may significantly reduce the inertial power of flight, contributing significant energetic savings to the total energy budgets of the only flying mammals. J. Morphol. 234: 277–294, 1997. © 1997 Wiley-Liss, Inc.     

突尼斯非洲跳鼠(Jaculus jaculus)和埃及跳鼠(J.orientalis)群体的等位酶多态及遗传分化(英文)

运用16种酶蛋白编码的23个遗传座位对突尼斯非洲跳鼠(Jaculus jaculus)和埃及跳鼠(J. orientalis)自然群体的遗传变异和分化进行了电泳分析。结果表明,与其他啮齿动物等哺乳动物的相关数据比较,发现这两个种群体的遗传变异水平较低。非洲跳鼠群体的观测杂合度 (H_obs) 为0.08—0.19,多态座位百分比(P)为26.2%—45.2%,每个座位的平均等位基因数(A)为1.1—1.4;埃及跳鼠的H_obs为0.10—0.15,P为29.3%—44.1%,A为1.1—1.7。两个种群体各自的遗传分化程度较低(非洲跳鼠和埃及跳鼠的F_st分别为0.0017和0.0019)。而两个种群体间的F_st为0.607（P<0.05）,表明两个种之间高度的遗传分化。本研究支持这两个种分类地位的合法性,并强调了地理因素（环境类型和生物气候阶段）对两个种遗传结构的影响。     

Ontogenetic,intraspecific, and interspecific variation of the prehallux in primates: Implications for its utility in the assessment of phylogeny

The prehallux is a sesamoid bone occurring in the region of the hallucial tarso-metatarsal joint in a number of metatherian and eutherian orders and in some nonmammalian tetrapods. Within the order Primates, it occurs invariably in ceboids and Hylobates, with extreme infrequency in pongids and Homo, and is absent in other primates groups. It has been suggested that, first, the prehallux is homologous both within and across the infraclasses Metatheria and Eutheria; second, it has functional significance in that it contributes to joint stability and is an adaptation to arboreality; third, its presence results in diagnostic features on the entocuneiform and hallucial metatarsal, so that original presence or absence can be unambiguously assessed in instances when the bone itself is not preserved; and fourth, because of presumed homology, it may be employed in the reconstruction of phylogenetic relationships. The present study concludes that the homologous nature of the bone is open to reasonable doubt, the assumption of homology does not yield significantly more parsimonious phylogeny reconstructions than does the assumption of analogy, there are no invariant diagnostic features associated with its presence, and functional explanations currently offered are of questionable validity. Thus, the prehallux is at present of little utility in either establishing or precluding phylogenetic relationships among primates.     

Autopodial skeleton evolution in side-necked turtles (Pleurodira)

Carpal and tarsal anatomy was documented based on the observation of dry skeletons of adult specimens representing 25 species in 15 genera and on data taken from the literature. In addition, histological sections and cleared and double‐stained autopodia of recently hatched and juvenile specimens representing seven chelid and pelomedusoid species were studied. There is much more morphological diversity in the manus than in the pes. Variation in autopodial skeletons includes: the astragalus and calcaneum are either separated or fused; fusion of distal carpals 3–4−5 or just 4–5; number of centralia in the carpus; and presence/absence of a pisiform and of an accessory radial element. The widespread and probably basal phalangeal formula for Pleurodira is 2.3.3.3.3. Deviations are Pelomedusa subrufa, exhibiting a reduction to 2.2.2.2.2, Pelusios spp. with one phalanx less in digit I and for one species in digit V as well, and Acanthochelys pallidipectoris with an additional phalanx in the fourth finger. Six discrete characters itemizing some of the morphological variation observed were plotted on a composite pleurodire phylogeny, revealing not only homoplastic patterns but also the utility of some characters in supporting the monophyly of several clades. The pisiform is the last carpal element to ossify in Chelus fimbriatus. We hypothesize that the so‐called fifth hooked metatarsal represents the fusion of distal tarsal 5 with metatarsal V. The accessory radial element that was occasionally present in the turtles examined may represent an atavism of the otherwise lost radiale of turtles.     

天津蓟县桃花园墓地明清时期缠足女性足骨的形态观察

本文对天津蓟县桃花园墓地明清时期101例缠足女性足骨形变情况进行了观察和分析。结果显示,不同个体的同名骨骼形变类型和程度不同,有的个体两侧足骨呈不对称状。跗骨在整体尺寸上缩小,且部分跗骨会产生形变。跖骨和近节趾骨因受缠足外力的影响在形态上会产生剧烈的变化,主要变现为跖骨和近节趾骨纤细、弓弯,关节面改变,其近、远端以及跖骨体和趾骨体的上下径和横径均产生形变。总体而言,跖骨和近节趾骨的形变程度较跗骨而言更大。本文总结了判断某个体是否缠足的依据,特别指出需要同时观察距骨和跟骨的形态改变。鉴于其他疾病(如高弓足、麻风病、风湿性关节炎)也可导致足骨的畸形样貌,在进行个体缠足判定时,需要进行综合成因分析。缠足由文化行为所导致,其足骨形变特征有别于因病理原因导致的足部畸形。功能压力分析能够有效地解释缠足个体足骨形变的成因及过程。     

The evolution of the reptilian hindfoot and the homology of the hooked fifth metatarsal

The homology of the fifth metatarsal in turtles and in diapsid reptiles is reassessed in the light of new phylogenetic studies. The two nearest outgroups to turtles — pareiasaurs and procolophonoids — both lack a fifth distal tarsal but retain a normal fifth metatarsal. The fifth distal tarsal was therefore lost at the base of the clade that contains turtles. Thus, the hooked fifth metatarsal in turtles must consist entirely of a modified fifth metatarsal: it does not include contributions from the fifth distal tarsal, as commonly supposed. In diapsids, loss of the fifth distal tarsal appears to have occurred at the base of crown-clade diapsids, hooking of the fifth metatarsal subsequently occurring within lepidosauromorphs, and in archosauromorphs. If so, the hooked fifth metatarsal in archosauromorphs, and some lepidosauromorphs, consists entirely of a modified fifth metatarsal. In both turtles and diapsids, integration of the elements distal to the mesotarsal joint precedes evolution of the hooked fifth metatarsal, supporting the view that the latter element evolved to perform a lever function (analogous to the “heel bone” of mammals).     

Erratum

Feet of two-toed sloths (Choloepus) are long, narrow, hook-like appendages with only three functional digits, numbers II, III, and IV; Rays I and V are represented by metatarsals. Proximal phalanges of complete digits are little more than proximal and distal articulating surfaces. All interphalangeal joints are restricted, by interlocking surfaces, to flexion and extension. Ankle and transverse tarsal joints, however, allow extreme flexion and inversion of foot. Powerful digital flexion is augmented by several muscles from extensor compartment of leg. Intrinsic foot musculature is reduced to flexors and extensors but these, with the exception of lumbricals, are large and well developed. Choloepus uses its feet much like hooks with distal phalanges and covering claws forming the “hook” element. These hook-like appendages are seemingly best suited for supports less than 50 mm in diameter suggesting that two-toed sloths may prefer supports of this size in their natural habitat.     

The Olduvai Hominid 8 foot: Adult or subadult?

Olduvai Hominid 8 (OH 8), an articulating set of fossil hominin tarsal and metatarsal bones, is critical to interpretations of the evolution of hominin pedal morphology and bipedal locomotion. It has been suggested that OH 8 may represent the foot of a subadult and may be associated with the OH 7 mandible, the type specimen of Homo habilis. This assertion is based on the presence of what may be unfused distal metatarsal epiphyses. Accurately assessing the skeletal maturity of the OH 8 foot is important for interpretations of the functional morphology and locomotor behavior of Plio-Pleistocene hominins. In this study, we compare metatarsal fusion patterns and internal bone morphology of the lateral metatarsals among subadult hominines (85 modern humans, 48 Pan, and 25 Gorilla) to assess the likelihood that OH 8 belonged to either an adult or subadult hominin. Our results suggest that if OH 8 is indeed from a subadult, then it displays a metatarsal developmental pattern that is unobserved in our comparative sample. In OH 8, the fully fused base of the first metatarsal and the presence of trabecular bone at the distal ends of the second and third metatarsal shafts make it highly improbable that it belonged to a subadult, let alone a subadult that matches the developmental age of the OH 7 mandible. In total, the results of this study suggest that the OH 8 foot most likely belonged to an adult hominin.     

Evolutionary selection and morphological integration in the foot of modern humans

Objectives

To advance our understanding of the evolution of the hominin foot by quantifying integration and responses to selection in the foot of modern humans.

Materials and Methods

The sample includes 247 female and male adult individuals from Euro-American, Afro-American, European, and Amerindian populations. We collected 190 linear measurements from the 26 skeletal elements that constitute the modern human foot. With these data, we calculated the magnitudes of integration and the ability of the foot to respond to selection demands.

Results

The results revealed that distal phalanges are less integrated, more evolvable, and more flexible than proximal elements (i.e., proximal phalanges and metatarsals). Also, bones from the medial ray (e.g., hallux) show stronger integration and weaker evolvability than their counterparts from the lateral column (e.g., fifth ray), following this trend from medial to lateral positions. Among the tarsals, the talus and calcaneus are the most integrated, least evolvable, and flexible elements from that module.

Discussion

These results suggest that selection for bipedalism would have reorganized the variance/covariance matrix of the foot. The hallux might have been under strong functional selection pressures for bipedal requirements, resulting in a strong integration and low evolvability. Also, differences in the developmental process of each bone seem to have played an essential role in the degree of evolvability, showing those elements that develop earlier have less ability to respond to selection demands.     

Paleobiological implications of new material of Platybelodon danovi from the Dingjiaergou Fauna,western China

We report on a newly born mandible and an adult pes of Platybelodon danovi from the Dingjiaergou fauna, China. Tooth succession in Platybelodon is very specialised, including a tendency to lose the dp2, an early loss of the di2 perhaps at the foetal stage, a tendency to lose the p3 and a tendency to reduce the P4 and the p4. The pes is also specialised, with metatarsals IV and III nearly equal in length, metatarsal IV less twisted than metatarsal III, metatarsals IV and III more anteroposteriorly compressed and metatarsals aligned nearly at the same level. These findings have important paleobiological significance. First, the relatively derived tooth succession of Platybelodon occurred at a relatively early geological time, thus representing an early evolution of tooth succession independent from other proboscideans. Second, the gravity vector of the hind limb of Platybelodon shifted towards metatarsal IV, and the modified standing posture may imply a lightly built body and rapid locomotion relative to other gomphotheres and elephants. These new paleobiological data add to our knowledge of the life history of Platybelodon and the diverse adaptations of ancient proboscideans.     

Prey Preference and Life Table of Amblyseius orientalis on Bemisia tabaci and Tetranychus cinnabarinus

Amblyseius orientalis (Ehara) (Acari: Phytoseiidae) is a native predatory mite species in China. It used to be considered as a specialist predator of spider mites. However, recent studies show it also preys on other small arthropod pests, such as Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Experiments were conducted to investigate (1) prey preference of A. orientalis between Tetranychus cinnabarinus (Boisd.) (Acari: Tetranychidae) and B. tabaci, and (2) development, consumption and life table parameters of A. orientalis when reared on T. cinnabarinus, B. tabaci or a mix of both prey species. When preying on different stages of T. cinnabarinus, A. orientalis preferred protonymphs, whereas when preying on different stages of B. tabaci, A. orientalis preferred eggs. When these two most preferred stages were provided together (T. cinnabarinus protonymphs and B. tabaci eggs), A. orientalis randomly selected its prey. Amblyseius orientalis was able to complete its life cycle on B. tabaci eggs, T. cinnabarinus protonymphs, or a mix of both prey. However, its developmental duration was 53.9% and 30.0% longer when reared on B. tabaci eggs than on T. cinnabarinus and a mix of both prey, respectively. In addition, it produced only a few eggs and its intrinsic rate of increase was negative when reared on B. tabaci eggs, which indicates that B. tabaci is not sufficient to maintain A. orientalis population. The intrinsic rates of increase were 0.16 and 0.23 when A. orientalis was fed on the prey mix and T. cinnabarinus, respectively. These results suggest that although B. tabaci is a poor food resource for A. orientalis in comparison to T. cinnabarinus, A. orientalis is able to sustain its population on a mix of both prey. This predatory mite may thus be a potential biological control agent of B. tabaci when this pest co-occurs with the alternative minor pest T. cinnabarinus.