Embryogenesis of cetaceans (whales, dolphins, porpoises) is best known inStenella attenuata, the pan-tropical spotted dolphin, based on a remarkably complete and well-studied prenatal ontogenetic series. Our study expands understanding of cetacean embryology by adding two additional cetacean taxa: the beluga whale (Delphinapterus leucas, Odontoceti), and the bowhead whale (Balaena mysticetus, Mysticeti). We identify key features that characterize these taxa at specific stages and highlight heterochrony between the odontocetes and mysticetes. The toothed whales are more similar in developmental timing to each other than either is to Balaena. The two odontocete taxa, Stenella and Delphinapterus, share similar developmental trajectories while early Balaena specimens differ from the odontocetes. This developmental variation proves challenging to ascribe to the existing Carnegie staging system. Most notably, flippers, hindlimbs, and flukes all provide morphological traits for characterization within the Carnegie staging system. A presomitic Delphinapterus embryo is also described. This study applies the Carnegie staging system to two more cetacean taxa and forms a framework for future research on cetacean developmental genetics and the modeling of fetal growth.
Two-toed (Choloepus sp.) and three-toed (Bradypus sp.) sloths possess short, rounded pisiforms that are rare among mammals and differ from other members of Xenarthra like the giant anteater (Myrmecophaga tridactyla) which retain elongated, rod-like pisiforms in common with most mammals. Using photographs, radiographs, and μCT, we assessed ossification patterns in the pisiform and the paralogous tarsal, the calcaneus, for two-toed sloths, three-toed sloths, and giant anteaters to determine the process by which pisiform reduction occurs in sloths and compare it to other previously studied examples of pisiform reduction in humans and orangutans. Both extant sloth genera achieve pisiform reduction through the loss of a secondary ossification center and the likely disruption of the associated growth plate based on an unusually porous subchondral surface. This represents a third unique mechanism of pisiform reduction among mammals, along with primary ossification center loss in humans and retention of two ossification centers with likely reduced growth periods in orangutans. Given the remarkable similarities between two-toed and three-toed sloth pisiform ossification patterns and the presence of pisiform reduction in fossil sloths, extant sloth pisiform morphology does not appear to represent a recent convergent adaptation to suspensory locomotion, but instead is likely to be an ancestral trait of Folivora that emerged early in the radiation of extant and fossil sloths.
Most mammalian pisiforms are large, elongated carpal bones with two ossification centers and an associated growth plate, similar to the calcaneus in the ankle. Short pisiforms are rare among mammals, but can be found in humans, orangutans (Primates: Pongo sp.), two‐toed sloths (Pilosa: Choloepus sp.), and three‐toed sloths (Pilosa: Bradypus sp.). These groups utilize diverse forms of locomotion; humans are bipedal, orangutans are quadrumanous climbers, and sloths are suspensory quadrupeds. Human pisiforms form from a single ossification center and have likely lost a primary ossification center and the associated growth plate. Given the rarity of short pisiforms among mammals, little is known about the functional implications or developmental mechanisms underlying this convergent morphology in species with such diverse locomotor modes and evolutionary histories. The purpose of this study is to compare ossification patterns in orangutans and sloths with the mechanism underlying human pisiform truncation. We compare pisiform ossification data from human, orangutan, and sloth museum specimens. Unlike humans, orangutan pisiforms retain two centers of ossification but appear to form the secondary center of ossification later than other apes, possibly shortening the growth period for the pisiform. Sloths form a primary center of ossification with an unusual, pitted surface, which may represent an abnormal subchondral surface. In non‐human primates (including orangutans) and giant anteaters (Pilosa: Myrmecophaga tridactyla), which represent the closest living taxonomic group to sloths, pisiform and calcaneus ossification is generally correlated with epiphyses forming at similar times within individuals. In contrast, we found only a single ossification center corresponding to sloth pisiforms at all stages of calcaneal epiphyseal formation. Thus, the single pisiform ossification center appears to precede calcaneal epiphysis formation. This indicates that the sloth pisiform is homologous to the primary center of ossification of the calcaneus and other mammalian pisiforms, and that it fails to form a secondary center. This is in contrast to human pisiforms, which fail to form the primary ossification center. Humans, orangutans, and sloths are all unusual among mammals for having short pisiforms and each group achieves pisiform reduction through unique mechanisms. Support or Funding Information This research was funded by the National Science Foundation (BCS‐1540418 and BCS‐1638812).
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