|Origin of Whales from Early Artiodactyls: Hands and Feet of Eocene Protocetidae from Pakistan|
P. D. Gingerich, M. ul Haq, I. S. Zalmout, I. H. Khan, M. Sadiq Malkani
Distinctive characteristics of artiodactyl ankle bones
A description of artiodactyl ankle bones follows. Italicized characteristics are found in artiodactyls and Rodhocetus described here but not in mesonychids or mammals generally.
The astragalus has a deeply grooved or trochleated body (tibial trochlea), a distinctly trochleated head (navicular trochlea) [developed to some extent in mesonychids and, rarely, other mammals], a proximodistally-elongate convex facet reflecting greater excursion on the ventral surface of the astragalus in contact with the calcaneum (sustentacular facet), a relatively small curved facet on the lateral surface for contact with the calcaneum (ectal facet), a narrow convex facet paralleling the navicular trochlea for articulation with the cuboid (cuboid facet), and a small flat facet on the lateral surface of the astragalus adjacent to the cuboid facet for articulation with the calcaneum (distal calcaneal facet).
The calcaneum has a long heel process (tuber), a prominent medial process or sustentaculum bearing a concave facet for articulation with the astragalus (sustentacular facet), a small facet on the medial surface for articulation with the astragalus (ectal facet), a relatively narrow convex facet on the dorsal surface above the ectal facet for articulation with the fibula (fibular facet), a relatively long distal process with a medial facet for articulation with the astragalus (distal astragalar facet), and an obliquely oriented concave distal facet for articulation with the cuboid (cuboid facet).
The navicular has a keeled concave proximal surface (astragalar facet) for articulation with the navicular trochlea of the astragalus, and three facets on its distal surface for articulation with stacked ento-, meso-, and ectocuneiforms. The ento-, meso-, and ectocuneiforms have simple proximal surfaces for articulation with the navicular and each has a simple distal surface for articulation with metatarsals I (when present), II, and III, respectively.
The cuboid has a divided proximal surface, with the medial part distinctly concave for articulation with the astragalus (astragalar facet) and the lateral part notched obliquely and convex for articulation with the distal process of the calcaneum (calcaneal facet), and a divided distal surface for articulation with metatarsals IV and V.
Specializations of artiodactyl tarsals serve the following purposes: (i) to stabilize the ankle joint by limiting motion to rotation in a parasagittal plane about a transverse axis (axes); (ii) to increase the number of transverse axes in the ankle from one to two, paralleling axes of cones or cylinders defined by curvature of crests of the tibial trochlea (upper ankle joint) and by curvature of the sustentacular facet (lower ankle joint), enabling the lower leg to be shortened and lengthened slightly relative to the foot (as part of the elastic mechanism involved in artiodactyl cursoriality); and (iii) to stabilize the transverse tarsal joint and limit its motion to rotation about a transverse axis compensating for rotation at the lower ankle joint.
Description of GSP-UM 3458, holotype of Artiocetus clavus
A field map of GSP-UM 3458 is shown in Web fig. 1. Salient features of the cranium are its completeness and quality of preservation (see text Fig. 1). The cranium is compared to skulls of other protocetids in Web fig. 2. The dorsal surface has nares positioned above the canines, well forward on the cranium. The frontals together form a shield as in other protocetids, but this is relatively narrow. The zygomatic arches are preserved intact and these flare laterally beyond what is already a relatively broad cranial base. On the ventral surface of the cranium the premaxillae are relatively short and the upper incisors closely spaced. In the maxilla C1 and P1 are single-rooted and P3-M3 are closely spaced. A protocone is well developed on M1 but less so on M2 and missing on M3. Molars decrease in size from M1 to M3. Auditory bullae are large and firmly attached with little development of pterygoid sinuses. Occipital condyles are large and face posteriorly. There is a narrow and deep mandibular foramen on the medial surface of the dentary, but the mandibular canal is shallow anterior to M1. The mandibular symphysis is unfused and extends as far back as the back of P2.
Cervical, thoracic, and lumbar centrum lengths are average for a protocetid. The sacrum was not recovered, and the only caudal centra are represented by pieces found on the surface. In the shoulder girdle the scapula was found in two pieces indicating total length by their spacing. The cranial and caudal borders of the scapula define an angle of arc of about 45°, with the spine running closer to the cranial border. The clavicle is a small flat bone like that of a dog (1), here preserved near the coracoid processes lying parallel to and slightly behind the acromion. The humerus was not found. The distal radius is only slightly wider than it is high. The carpus and manus were not recovered. In the pelvic girdle the ilium is preserved with part of the acetabular border. The medial surface indicates broad articulation with an auricular process of the sacrum (not recovered). The femoral shaft is roughly cylindrical, with a bilateral diameter only slightly greater than its anteroposterior diameter. The patella is tear-shaped and thick.
The body of the astragalus resembles a short spool, set transversely, with a higher keel of greater diameter at its lateral margin separated by a shallow trochlea from a lower keel of lesser diameter at its medial margin. The astragalar neck is long, and the head is convex and distinctly trochleated, with the plane of trochleation of the head everted about 15° relative to that of the astragalar body. The sustentacular facet is a proximodistally elongate oval on the ventral surface of the astragalus, and the ectal facet is a relatively small oval concavity on the lateral surface. A fragment of calcaneum preserves an oval sustentacular facet for articulation with the corresponding facet on the astragalus. The cuboid is as distinctly artiodactyl in form as the astragalus. There is a posterior process for articulation with the lateral margin of the head of the astragalus, and lateral to this a deep oblique notch or sulcus for articulation with the distal and medial surfaces of the distal extremity of the calcaneum. The distal surface of the cuboid has a curved facet for articulation with metatarsals IV and V. The astragalus and cuboid of Artiocetus clavis are compared to those of Diacodexis metsiacus and Sinonyx jiashanensis in Web fig. 3.
Representative measurements of the skeleton of GSP-UM 3458 are listed in Web table 1.
Description of GSP-UM 3485, holotype of Rodhocetus balochistanensis
A field map of GSP-UM 3485 is shown in Web fig. 4. The braincase was found on the surface. It is weathered and typically protocetid but provides little detailed information about the cranium. A piece of dentary found on the surface shows that the mandibular symphysis was unfused as it is in Rodhocetus kasrani.
Cervical, thoracic, and caudal centrum lengths are average for a protocetid, with the proximal caudals being large. A piece of a middle caudal was found on the surface. The sacrum was not recovered. The distal humerus is well preserved and this can be matched to proximal humeri of other protocetids to estimate length. The ulna and radius are well preserved, and the ulna has a large and deep olecranon. The distal radius is much broader than it is high (unlike that of Artiocetus clavis described here).
Hands and feet were removed from the field in a plaster jacket (Web fig. 5) and prepared in the laboratory. The hand is illustrated in text Fig. 2 and Web fig. 6. Carpal bones of the wrist are all separate, tightly-packed, and alternating, with no centrale. The pisiform is long and narrow, and oriented downward perpendicular to the palmar surface. The hand is mesaxonic with metacarpal III dominating and lengths decreasing in the sequence III-IV-II-V-I [as in Diacodexis, (2)]. Similarly, digit III has the largest phalanges. Flat distal surfaces on Mc II, III, IV, and large sesamoids indicate that the central metacarpal-phalangeal joints were habitually extended slightly. Distal phalanges are preserved on digits II and IV: these are short with a flat base, unfissured, and a central rib of bone on the dorsal surface flanked on both sides by thinner bone. Digit III almost certainly had a similar distal phalanx, only larger, and all three central digits appear to have borne hooves in life (see below). Digit I has a simple pointed distal phalanx, as is inferred for digit V, and these flanking digits of the hand appear not to have been weight-bearing.
The femur is relatively short and robust, with medial and lateral ridges of bone running the length of the shaft, giving it roughly a diamond shape in cross section. Greater and lesser trochanters are present but not well preserved, and there is a distinct third trochanter at the level of the midshaft. The patellar groove is high and narrow, angling to the lateral condyle. The patella itself is massive but flatter than that of Artiocetus. The tibia is 10% longer than the femur. A piece of long bone found with the tibia may be the midshaft of a fibula; if so, the fibula was of much smaller diameter than the tibia.
The foot is illustrated in text Fig. 2 and Web fig. 7. The astragalus of Rodhocetus is larger and relatively higher than that of Artiocetus, with larger and more closely spaced medial and lateral ridges bordering the tibial trochlea on the body. The neck is similarly long, but deeper. The distal trochlea is similar to that of Artiocetus. The calcaneum has a long tuber, an anteriorly oriented transverse sustentacular facet, an enormous curved fibular facet, and a typically artiodactyl distal process with a large distal facet and a small medial facet articulation with the cuboid. The navicular is short anteroposteriorly, narrow, and very deep. Proximally it has a large longitudinally ridged concave facet for articulation with the distal trochlea of the astragalus. Distally it articulates with a dorsoplantarly-stacked set of ecto-, meso-, and entocuneiforms. The ectocuneiform has a large distal facet for articulation with metatarsal III, while the mesocuneiform has a smaller facet for the base of Mt II. The entocuneiform is large and platelike like that of an anthracothere or extant hippopotamus and fits tightly against the anterior surface of the ventral process of the navicular, bearing a small distal facet for articulation with a nodule-like Mt I. The cuboid is longer proximodistally than that of Artiocetus and, while the notch for articulation with the calcaneum is similar, this occupies a much smaller proportion of the bone. The distal surface of the cuboid has facets for Mt IV and V. The foot is paraxonic with metatarsals III and IV dominating. All four metatarsals are long (Mt III is 60% longer than Mc III) and relatively delicate, and lengths decrease in sequence from IV-III-V-II [again, approximately like Diacodexis, (3, 4)]. Proximal and medial pedal phalanges are similarly long and delicate. Distal phalanges are preserved on digits II and III. Both are similar in form to distal phalanges of the hand, unfissured, but much longer and hence more pointed (see below).
Representative measurements of GSP-UM 3485 are listed in Web table 1.
Hooves on the manus of Rodhocetus balochistanensis
Distal phalanges belonging to digits II and IV are well preserved in the hand of Rodhocetus balochistanensis. As described above, these are short proximodistally and broad mediolaterally, with a flat base and a thick central rib of bone on the dorsal surface. The apex is blunt and unfissured. Digit III almost certainly had a similar distal phalanx, only larger, and all three central digits of the hand appear to have borne hooves in life. Inference of hooves is based on comparison to distal phalanges of primitive artiodactyls of similar size [anthracotheres, and oreodonts, (5)], which are not like the trihedral and pointed unguals of most living artiodactyls. Hippos are said to have 'nail-like' hooves [(6), p. 1067], and this seems an apt description of hooves in similarly digitigrade (rather than unguligrade) Rodhocetus, anthracotheres, and oreodonts.
Distal phalanges preserved on digit I of the hand (and inferred for digit V) and preserved on digits II and III (and inferred for IV and V) of the foot are longer compared to the breadth of their bases. These are consequently much more pointed, and while they probably bore a keratinous covering of some kind it does not seem appropriate to call this a hoof.
The presence of webbing on a hoofed manus is not without precedent as living hippos show this combination of characteristics to some degree [(7), p. 46; (8), p. 511; (9), p. 60; (10), p. 3].
- M. E. Miller, G. C. Christensen, H. E. Evans, Anatomy of the Dog (W. B. Saunders, Philadelphia, 1964).
- J. G. M. Thewissen, S. T. Hussain, Anat. Histol. Embryol. Zentralbl. Veterinarmed. C 19, 37 (1990).
- K. D. Rose, Science216, 621 (1982).
- K. D. Rose, J. Paleont.59, 1203 (1985).
- W. B. Scott, Trans. Am. Phil. Soc.28, 363 (1940).
- R. M. Nowak, Walker's Mammals of the World, Sixth Edition. Volume 2. (Johns Hopkins University Press, Baltimore, 1999).
- A. Milne-Edwards, in Recherches pour Servir à l'Histoire Naturelle des Mammif�res (G. Masson, Paris, 1868), pp. 43-66.
- S. Frechkop, in Traité de Zoologie, P.-P. Grassé, Ed. (Masson, Paris, 1955), pp. 508-535.
- H. Klingel, in Grzimek's Encyclopedia of Mammals (McGraw-Hill, New York, 1990), pp. 60-61.
- S. K. Eltringham, The Hippos: Natural History and Conservation (Poyser/Academic Press, London, 1999).
- P. D. Gingerich, in The Emergence of Whales: Evolutionary Patterns in the Origin of Cetacea, J. G. M. Thewissen, Ed. (Plenum Publishing Corporation, New York, 1998), pp. 423-449.
- P. D. Gingerich, S. M. Raza, M. Arif, M. Anwar, X. Zhou, Nature368, 844 (1994).
- P. D. Gingerich, M. Arif, W. C. Clyde, Contrib. Mus. Paleont. Univ. Mich.29, 291 (1995).
- E. Fraas, Geol. Paläont. Abh. Jena6, 197 (1904).
Supplemental Figure 1. Map of holotype of Artiocetus clavis new genus and species, Geological Survey of Pakistan-University of Michigan [GSP-UM] specimen 3458, as found and excavated in the field. North is at the top of the figure and land surface here dips approximately 10° toward the southeast. Right innominate and lumbar vertebra were exposed at the surface before excavation; remainder of skeleton shown here was excavated on a bedding plane dipping at about 50° toward the southeast. Astragalus, cuboid, and other weathered bone pieces were found downslope on the land surface within two meters of the right innominate.
Supplemental Figure 2. Diversity of cranial morphology in early Protocetidae, ordered from oldest (left) to youngest (right). Cranium of Artiocetus clavis, new genus and species [(A), late early Lutetian], is compared to those of Rodhocetus kasrani [(B), early middle Lutetian, (12)], Takracetus simus [(C), early middle Lutetian, (13)], Gaviacetus razai [(D), middle Lutetian, (13)], and Protocetus atavus (D) (14). Schematic drawings, in dorsal view, are scaled to same condylobasal length (original skulls are close to the same size). Note anterior position of external nares, narrow frontal shield, and relatively wide cranial base distinguishing cranium of Artiocetus from those of other genera. Differences in rostral shape shown here reflect the range of feeding specializations represented by early protocetids.
Supplemental Figure 3. Comparison of left astragali and cuboids of early Eocene artiodactyl Diacodexis, early middle Eocene protocetid Artiocetus, and late Paleocene mesonychid Sinonyx. (A) through (C), Diacodexis metsiacus, UM 95446. (D) through (F), Artiocetus clavis, GSP-UM 3458. (G) through (I), Sinonyx jiashanensis, Institute for Vertebrate Paleontology and Paleoanthropology, Beijing [IVPP] 10760. All specimens are shown in dorsal, lateral, and plantar views. Note more distinctly trochleated navicular facet, laterally placed ectal facet, and more anteriorly placed sustentacular facet on the astragalus, and notched calcaneal facet on the cuboid shared by Diacodexis and Artiocetus but not Sinonyx. Abbreviations: Ast., astragalus; ast., astragalar facet on cuboid; cal., calcaneal facet on cuboid; Cub., cuboid; cub., cuboid facet on astragalus; ect., ectal facet on astragalus; fib., fibular facet on astragalus; nav., navicular facet on astragalus; sus., sustentacular facet on astragalus; tib., tibial facet on astragalus.
Supplemental Figure 4. Map of holotype of Rodhocetus balochistanensis new species, GSP-UM 3485, as found and excavated in the field. North is at the lower left corner of the figure and land surface
here is a bedding plane dipping approximately 60° toward the bottom of the figure (northwest). Cervical-thoracic vertebrae
(C2-T2), lumbar vertebrae (L1-L3 and L4-L6), brain case of skull (not shown here), and other pieces of bone were found in
a gully below the excavation. Remainder of skeleton was found in situ as shown. Hands and feet were removed in a plaster jacket
(Web fig. 5).
Supplemental Figure 5. Plaster jacket with hands and feet of Rodhocetus balochistanensis holotype, GSP-UM 3485, before preparation of individual bones. See map in Web fig. 4 for identification of elements. Scale is in cm.
Supplemental Figure 6. Left manus of Rodhocetus balochistanensis, GSP-UM 3485, in anterior view. The hand is mesaxonic with three central weight-bearing toes that evidently bore nail-like hooves (distal phalanges preserved on digits II and IV) flanked by more gracile lateral toes that lacked hooves (distal phalanx preserved on digit I). See text Fig. 2 for identification of elements.
Supplemental Figure 7. Left pes of Rodhocetus balochistanensis, GSP-UM 3485 (reversed from right side), in anterior view. Note artiodactyl characteristics in the well developed navicular trochlea on the head of the astragalus, convex fibular facet on the calcaneum, and concave astragalar facet paired with a convex calcaneal facet notched into the cuboid. The foot is paraxonic with four long toes, flanges of bone on the medial or lateral bases of the middle phalanges providing leverage for opening the feet to maximum breadth during extension, and narrowly pointed ungules (distal phalanges preserved on digits II and III). See text Fig. 2 for identification of elements.
|Supplemental Table 1.Artiocetus clavis, new genus and species, and Rodhocetus balochistanensis, new species. Asterisks mark estimates. Body weight was estimated from centrum size of available cervical, thoracic, and lumbar vertebrae, using multiple regression and a reference set of 13 marine mammal skeletons of known weight (eight cetaceans and five pinnipeds) spanning a range from 85 to 23,500 kg (11).|
|Artiocetus clavis||Rodhocetus balochistanensis|
|Measurement (cm)||GSP-UM 3458 (holotype)||GSP-UM 3485 (holotype)|
|Tympanic bulla length||6.5||-|
|Tympanic bulla width||4.8||-|
|Mandibular foramen height||6.0||-|
|Cervical vertebra C4 length||2.8||3.2|
|Thoracic vertebra T4 length||3.2||3.9|
|Lumbar vertebra L4 length||4.3||-|
|Caudal vertebra Ca4 length||-||5.5|
|Radius distal width||2.7||3.0|
|Radius distal thickness||2.3||1.8|
|Metacarpal length (Mc III)||-||7.6|
|Manual phalanx length (III-1)||-||6.3|
|Manual phalanx length (III-2)||-||3.3*|
|Manual phalanx length (III-3)||-||1.3*|
|Ilium length, from acetabular margin||12.4||-|
|Femur midshaft diameter (ant.-post.)||2.2||2.3|
|Femur midshaft diameter (bilateral)||2.5||3.2|
|Metatarsus length (Mt III)||-||12.2|
|Pedal phalanx length (III-1)||-||9.0|
|Pedal phalanx length (III-2)||-||7.0|
|Pedal phalanx length (III-3)||-||2.3|
|Body weight (kg)||420*||450*|