Abstract
BackgroundThe pisiform and calcaneus are paralogous bones of the wrist and ankle and are the only carpal and tarsal, respectively, to develop from two ossification centers with an associated growth plate in mammals. Human pisiforms and calcanei have undergone drastic evolutionary changes since our last common ancestor with chimpanzees and bonobos. The human pisiform is truncated and has lost an ossification center with the associated growth plate, while the human calcaneus has expanded and retained two ossification centers and a growth plate. Mammalian pisiforms represent a wide range of morphologies but extremely short pisiforms are rare and ossification center loss is even rarer. This raises the question of whether the sole human pisiform ossification center is homologous to the primary center or the secondary center of other species. We performed an ontogenetic study of pisiform and calcaneus ossification patterns and timing in macaques, apes, and humans (n = 907) from museum skeletal collections to address this question.ResultsHuman pisiforms ossify irregularly and lack characteristic features of other primates while they develop. Pisiform primary and secondary center ossification timing typically matches that of the calcaneus of non-human primates, while the human pisiform corresponds with calcaneal secondary center ossification. Finally, human pisiforms ossify at the same dental stages as pisiform and calcaneal secondary centers in other hominoids.ConclusionsThese data indicate that the human pisiform is homologous to the pisiform epiphysis of other species, and that humans have lost a primary ossification center and associated growth plate while retaining ossification timing of the secondary center. This represents an exceptional evolutionary event and demonstrates a profound developmental change in the human wrist that is unusual not only among primates, but among mammals.
Highlights
The pisiform and calcaneus are paralogous bones of the wrist and ankle and are the only carpal and tarsal, respectively, to develop from two ossification centers with an associated growth plate in mammals
Human pisiform ossification begins between 9 and 12 years of age [5]. This appears to be later in development than the primary ossification center of chimpanzees or gorillas; the comparative ossification timing across species and relationship between the primary and secondary centers remain unknown [4]. We address these questions of human pisiform homology and their potential coordinated evolution with the human calcaneus through a comparative analysis of the ossification of these bones
Human pisiform ossification resembles an epiphysis We surveyed museum skeletal collections to determine dental eruption and ossification stage of pisiforms and calcanei in juvenile humans (Homo sapiens), chimpanzees (Pan troglodytes), bonobos (Pan paniscus), gorillas (Gorilla sp.), orangutans (Pongo sp.), hylobatids (Hoolock sp., Hylobates sp., and Nomascus sp. [53] and Symphalangus syndactylus), and macaques (Macaca sp.) (n = 907, Table 1). This sample represents the full range of pisiform and calcaneus postnatal development
Summary
The pisiform and calcaneus are paralogous bones of the wrist and ankle and are the only carpal and tarsal, respectively, to develop from two ossification centers with an associated growth plate in mammals. The pisiform is an elongated, rod-shaped bone in the proximal carpal row that forms a rigid articulation between the triquetral and ulnar styloid process in almost all mammals [1, 2] It serves as an attachment for the tendon of the flexor carpi ulnaris muscle and is the only carpal to possess two ossification centers with an associated growth plate [3,4,5]. The pisiform and calcaneus are the only carpals or tarsals to possess two ossification centers with an associated growth plate [4] These functional, developmental, and embryological similarities indicate that the calcaneus is likely paralogous to the pisiform and triquetral in the forelimb [6]
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