Morphological analysis of the mammalian postcranium: a developmental perspective

Abstract

The past two decades have greatly improved our knowledge of vertebrate skeletal morphogenesis. It is now clear that bony morphology lacks individual descriptive specification and instead results from an interplay between positional information assigned during early limb bud deployment and its "execution" by highly conserved cellular response programs of derived connective tissue cells (e.g., chondroblasts and osteoblasts). Selection must therefore act on positional information and its apportionment, rather than on more individuated aspects of presumptive adult morphology. We suggest a trait classification system that can help integrate these findings in both functional and phylogenetic examinations of fossil mammals and provide examples from the human fossil record.

Figure 1

Hypothetical transitional emergence of the hominid pelvis. Anterior photographs of a chimpanzee pelvis (lower right) and that of A.L. 288-1 (“Lucy”) (lower left) were scanned. Using a sliding scale, the upper left image was then obtained by digital morphing to a transitional stage 75% of the distance between the chimpanzee and A.L. 288-1. The upper right image is a simple superoinferior digital distortion of the chimpanzee without any reference to a known “end product” (Photoshop “scale function”). Image breadth was not altered; its superoinferior height was simply reduced by 2/3. (Note: the upper right image appears somewhat less “transitional” than the one at the upper left because the latter benefits from the three-dimensionality of the two images being morphed; i.e., our distortion was only two-dimensional.) We do not suggest that either image constitutes an actual “intermediate” pelvic form. We wish only to demonstrate that a simple dimensional change in one hypothetical adult form is very similar to that which has been morphed by using the known adult “final outcome” and that it might be achieved by a simple underlying mechanism such as a progressive increase or decrease in the slopes of cell response gradients (see text). We suggest that this is the most probable morphogenetic mode by which the many anatomical differences between A.L.-288-1 and the chimpanzee pelves evolved. Therefore, the isolated definition and separate analysis of each of the many traits that differ between these pelves is likely to greatly distort their functional and phyletic significance (see especially ref. , pp. 359–361 for discussion). Note, for example, that a number of the unusual distinguishing characters of the australopithecine pelvis, including its exceptionally broad sacrum, platypelloid birth canal (i.e., anteroposterior dimension/mediolateral dimension × 100 ≈ 50–60), short pubic symphysis, elongated superior and inferior pubic rami, ovoid obturator foramina, etc., have all been reproduced by this simple, relatively crude, linear distortion.

Figure 2

The human knee exhibits specialized features that can be directly attributed to its role in upright walking. These include a bicondylar angle [the knee angle that places the foot beneath the trunk’s center of mass (A)], an elevated lateral condylar lip [which counteracts the tendency for patellar dislocation by the quadriceps (C Upper)], and elliptically shaped femoral condyles [which increase cartilage contact in full extension during the primary periods of ground contact]. In addition, human knees are tibial dominant (C Upper) whereas those of quadrupedal primates are patellar dominant (C Lower). The latter features require more explanation. The patella is lodged within the quadriceps, which is the principal extensor of the knee (A). When the knee is in flexion, a large component of extensor force compresses the patella against the femur. The resultant stress is determined by the congruity of the two mated surfaces. However, in extension, knee extensor force (plus body mass) generates compression between the femur and tibia; in this position, their area of contact determines joint stress (These relationships are graphed in B). Primates have a great range of motion in the knee. Therefore, unlike many other mammals, there is a significant part of their distal femoral surface that must contact the patella during flexion and the tibia in extension. The shape of this “shared” region (C) differs radically in chimpanzee and human distal femora. In chimpanzees (C Lower and Inset), it is simple and mirror images the discoid surface of the patella (not shown). In the human (C Upper and Inset), it instead conforms to the shapes of the medial and lateral tibial condyles (as deepened by their respective menisci). There is also a dramatic anteroposterior elongation of the human lateral condyle (not shown). This increases the area of cartilage contact in the last 20 degrees or less of knee extension [the chimpanzee’s is circular and does not reflect any single joint position of increased cartilage contact]. The chimpanzee knee is clearly patellar dominant whereas the human knee is tibial dominant. Given the plasticity of developing joint cartilage, all of these individual morphological differences could have been elicited by elongating the presumptive prechondrogenic condylar mesenchyme (especially that of the lateral condyle) by a few cell diameters. This, in conjunction with a habitual bipedal gait (which generates continuously high levels of tibiofemoral force in full extension), can account for virtually all of these unique human characters. What at first appears to be a profusion of separate traits more probably reflects a profoundly simpler change in the pattern formation field of the human femur.