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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. 

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. 

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It is not that selection cannot act on individual characters unless they are independently heritable but rather independently heritable characters simplifies the understanding of character complexes.

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... were to span n cell diameters, and those cells defined the ultimate anteroposterior dimension of the presumptive ilium (superoinferior in the adult human), then a slight increase in the steepness of its slope would cause that signal to span fewer cells, ‘‘distorting’’ the presumptive anlagen and substantially altering downstream adult morphology. Fig. 1 is intended simply to illustrate this argument and is therefore necessarily restricted to two dimensions. In reality, condensations are three-dimensional, and iliac rotation would be equally subject to modification during field specification. In this manner, the breadth, height, and depth of the entire pelvic field could have been simultaneously altered. Our argument is not that a change in anlagen specification necessarily underlies hominid pelvic evolution. A variety of other kinds of PI ‘‘read-outs,’’ such as a substantial alteration of downstream growth rates in an otherwise unperturbed anlagen, could have had the same effects. Rather, we are suggesting that subtle shifts in the disposition of PI are the most probable morphogenetic mode of evolution of the hominid pelvis, and that such shifts are the primary source of most anatomical changes that have been achieved in mammalian bones. Consider how profoundly such a hypothesis affects the manner in which the differences between the pelves of Australopithecus and a chimpanzee (as an example) are interpreted (Fig. 1). In both functional and phylogenetic analyses of this transition using conventional methods, each of many anatomical differences would typically be isolated and treated independently (see, e.g., refs. 46–48). However, the fundamental differences are that the hominid ilium and sacrum are dramatically shorter (superoin- feriorly) and broader (mediolaterally). The neck of the hominid femur and the anterior parts of its pelvis (the pubic and ischial rami) have all participated in these same dimensional changes. Collectively, all are consistent either with a broadening and shortening of the morphogenetic field(s) responsible for the initial form of the entire pelvic region or by a systematic change in postanlagen growth with similar geometric effects. None of these individual differences is likely to have been specifically and separately fixed in the genome because virtually none is likely to have been a consequence of localized gene expression specific to each defined trait. Subtle changes in presumptive tissue fields such as those hypothesized here will typically yield many down- stream effects, but only the most prominent are likely to have had a sufficiently significant effect on function to actually affect fitness. Except in rare instances (which can possibly serve as examples of punctuated ‘‘breakthrough’’ adaptations), most others will merely be retained byproducts of the primary changes. The transverse distance between the hip joints of the early hominid pelvis can serve to illustrate this important point. A notable consequence of the overall broadening of the early hominid pelvis is that the relative distance between the two hip joints was also increased. This is an apparent disadvantage during bipedal locomotion because it requires greater abductor contraction during the single leg phase (i.e., it reduces the lever arm length of the pelvic stabilizers). Does this increased distance therefore ‘‘demand some special functional explanation’’ as several authors have insisted (ref. 49, p. 285; see also ref. 50)? The answer is very probably no, so long as consideration is given to the manner in which the ancestral–descendant transition is likely to have been achieved morphogenetically, and the entire pelvis is not atomized into component parts that, in fact, probably have no individual, separable, heritability (51). By what other genetic means than that outlined here was the hominid pelvis so systematically and rapidly altered? By separate, inde- pendent fixation of all of its novel anatomical features [broader ilium, broader sacrum, longer (i.e., broader) femoral neck, longer (i.e., broader) pubic rami, shorter ilium, shorter pubic joint, etc.]? Are we to presume that each such isolated change in pelvic structure had a sufficiently strong effect on reproductive success to have been independently altered and fixed in the genome, even if realistic genetic models for the individual specification of each such feature were available? Many such complicated (even labyrinthine) biomechanical explanations of these pelvic traits have been posited (49, 50), but, in light of what we have discovered about morphogenesis in limbs, such analyses have been rendered unreasonable. Cartilage Modeling and the Evolution of the Human Knee. As noted earlier, the tissues of the musculoskeletal system are exquisitely sensitive to mechanical loading. This sensitivity can be ‘‘exploit- ed’’ by selection to produce relatively profound anatomical changes with only minimal changes in PI. The evolution of the human knee (Fig. 2) can serve as an excellent example of the potential role of such SAMs in the evolution of the mammalian postcranium. When two or more bones that comprise a synovial joint move relative to one another, they must do so in a manner that generates velocity vectors that are continuously tangential to their contacting surfaces. If this is not the case, the two rigid bodies will deform and degrade their contacting surfaces. This results in their eventual destruction and further kinematic derangement (52, 53). In addition, the joint’s inherent tensile restraint system of ligaments and tendons must also be in exacting compliance with the joint’s pathway of motion, so that it can maintain that pathway in the face of any external forces that tend to dislodge it. Mammalian joints, therefore, must develop inviolate coordi- nation between their surface geometries and soft tissue restraint systems (54) (Fig. 2). It is virtually inconceivable that such exact conformity between the mating surfaces of a synovial joint could be dictated in some directly heritable fashion (i.e., by descriptive specification). This would require not only an exact ordination of the three-dimensional form of the mated surfaces but equally exacting construction of the network of individual fiber bundles that compose each of the joint’s ligaments, all of which would be in some way subject to the process of genetic recombination. Clearly, such exacting geometries are not directly heritable. We have long known, since the classic tissue culture experi- ments of Murray (55) and Fell (56), that cartilage exhibits considerable mechanical reactivity, and there is now substantial direct experimental evidence of its robust modeling capacity, including recent demonstrations that chondrocytes are ‘‘very sensitive to loading pattern’’ (ref. 57, p. 906) and that imposed loads act to calibrate their metabolic activity, including the up- and down-regulation of matrix synthesis (reviewed in ref. 57). It is therefore increasingly likely that joint geometry is quite plastic even though such plasticity ceases at adulthood (there are no repair mechanisms). This SAM has great import with respect to the evolution of joint structure. The human knee differs dramatically from that of other primates (Fig. 2), reflecting a highly specialized adaptation to bipedality. How were all of these dramatic changes acquired by humans and their ancestors? The bicondylar angle may simply be a modeling effect of differential induction of regional mitosis in the distal femoral growth plate, the chondral epiphysis, or both in response to a medial joint position required during habitual upright gait (58). Other unique characters, such as tibial dom- inance, however, would at first seem to require much more complicated origins. At the same time, given the plasticity of developing joint cartilage, relatively simple changes in pattern formation can underlie profound downstream changes. This type of pathway is the most probable means by which the generalized morphology of the hominoid distal femur was transformed into its highly specialized human form. Specifically, elongation of the lateral femoral condyle could have been introduced by a slight increase in the anteroposterior length of its prechondrogenic mesenchy- mal field by only a few cell diameters or by a slight respecification of postanlagen growth. Such a change, in conjunction with cartilage plasticity and a habitual bipedal gait (which generates continuously high levels of tibiofemoral force in and about full extension) (Fig. 2), can account for virtually the entirety of the unique morphology of the human knee. Therefore, what appears to be a profusion of separate traits may very well reflect a profoundly simpler, albeit highly influential, change in the pattern formation field of the human distal femur. Although the above examples have been restricted to issues of human evolution, expositions directly linking equally dramatic anatomical changes to pattern formation shifts are readily available for other mammals and even classes [the origin of the fibular crest of birds and of the elongated tarsus of frogs are particularly striking examples (59–62)]. Etiology. Let us summarize the discussion to this point. A mammalian bone is ultimately the product of coding specified in its positional information (PI). That PI is manifested down- stream by specific local growth and development regimens specific to each presumptive bone. Those regimens are in turn expressed by employment of a variety of highly conserved systemic assembly mechanisms (SAMs). Although subtle differ- ences in PI can be unique to a species, the SAMs are not. They are shared among large numbers of taxa, and probably do not differ significantly among most mammals. This is highly probable simply because any alteration of such tissue and cellular response protocols would systemically alter the entire skeleton whereas subtle, local changes in the growth of a ...
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... growth rates in an otherwise unperturbed anlagen, could have had the same effects. Rather, we are suggesting that subtle shifts in the disposition of PI are the most probable morphogenetic mode of evolution of the hominid pelvis, and that such shifts are the primary source of most anatomical changes that have been achieved in mammalian bones. Consider how profoundly such a hypothesis affects the manner in which the differences between the pelves of Australopithecus and a chimpanzee (as an example) are interpreted (Fig. 1). In both functional and phylogenetic analyses of this transition using conventional methods, each of many anatomical differences would typically be isolated and treated independently (see, e.g., refs. 46–48). However, the fundamental differences are that the hominid ilium and sacrum are dramatically shorter (superoin- feriorly) and broader (mediolaterally). The neck of the hominid femur and the anterior parts of its pelvis (the pubic and ischial rami) have all participated in these same dimensional changes. Collectively, all are consistent either with a broadening and shortening of the morphogenetic field(s) responsible for the initial form of the entire pelvic region or by a systematic change in postanlagen growth with similar geometric effects. None of these individual differences is likely to have been specifically and separately fixed in the genome because virtually none is likely to have been a consequence of localized gene expression specific to each defined trait. Subtle changes in presumptive tissue fields such as those hypothesized here will typically yield many down- stream effects, but only the most prominent are likely to have had a sufficiently significant effect on function to actually affect fitness. Except in rare instances (which can possibly serve as examples of punctuated ‘‘breakthrough’’ adaptations), most others will merely be retained byproducts of the primary changes. The transverse distance between the hip joints of the early hominid pelvis can serve to illustrate this important point. A notable consequence of the overall broadening of the early hominid pelvis is that the relative distance between the two hip joints was also increased. This is an apparent disadvantage during bipedal locomotion because it requires greater abductor contraction during the single leg phase (i.e., it reduces the lever arm length of the pelvic stabilizers). Does this increased distance therefore ‘‘demand some special functional explanation’’ as several authors have insisted (ref. 49, p. 285; see also ref. 50)? The answer is very probably no, so long as consideration is given to the manner in which the ancestral–descendant transition is likely to have been achieved morphogenetically, and the entire pelvis is not atomized into component parts that, in fact, probably have no individual, separable, heritability (51). By what other genetic means than that outlined here was the hominid pelvis so systematically and rapidly altered? By separate, inde- pendent fixation of all of its novel anatomical features [broader ilium, broader sacrum, longer (i.e., broader) femoral neck, longer (i.e., broader) pubic rami, shorter ilium, shorter pubic joint, etc.]? Are we to presume that each such isolated change in pelvic structure had a sufficiently strong effect on reproductive success to have been independently altered and fixed in the genome, even if realistic genetic models for the individual specification of each such feature were available? Many such complicated (even labyrinthine) biomechanical explanations of these pelvic traits have been posited (49, 50), but, in light of what we have discovered about morphogenesis in limbs, such analyses have been rendered unreasonable. Cartilage Modeling and the Evolution of the Human Knee. As noted earlier, the tissues of the musculoskeletal system are exquisitely sensitive to mechanical loading. This sensitivity can be ‘‘exploit- ed’’ by selection to produce relatively profound anatomical changes with only minimal changes in PI. The evolution of the human knee (Fig. 2) can serve as an excellent example of the potential role of such SAMs in the evolution of the mammalian postcranium. When two or more bones that comprise a synovial joint move relative to one another, they must do so in a manner that generates velocity vectors that are continuously tangential to their contacting surfaces. If this is not the case, the two rigid bodies will deform and degrade their contacting surfaces. This results in their eventual destruction and further kinematic derangement (52, 53). In addition, the joint’s inherent tensile restraint system of ligaments and tendons must also be in exacting compliance with the joint’s pathway of motion, so that it can maintain that pathway in the face of any external forces that tend to dislodge it. Mammalian joints, therefore, must develop inviolate coordi- nation between their surface geometries and soft tissue restraint systems (54) (Fig. 2). It is virtually inconceivable that such exact conformity between the mating surfaces of a synovial joint could be dictated in some directly heritable fashion (i.e., by descriptive specification). This would require not only an exact ordination of the three-dimensional form of the mated surfaces but equally exacting construction of the network of individual fiber bundles that compose each of the joint’s ligaments, all of which would be in some way subject to the process of genetic recombination. Clearly, such exacting geometries are not directly heritable. We have long known, since the classic tissue culture experi- ments of Murray (55) and Fell (56), that cartilage exhibits considerable mechanical reactivity, and there is now substantial direct experimental evidence of its robust modeling capacity, including recent demonstrations that chondrocytes are ‘‘very sensitive to loading pattern’’ (ref. 57, p. 906) and that imposed loads act to calibrate their metabolic activity, including the up- and down-regulation of matrix synthesis (reviewed in ref. 57). It is therefore increasingly likely that joint geometry is quite plastic even though such plasticity ceases at adulthood (there are no repair mechanisms). This SAM has great import with respect to the evolution of joint structure. The human knee differs dramatically from that of other primates (Fig. 2), reflecting a highly specialized adaptation to bipedality. How were all of these dramatic changes acquired by humans and their ancestors? The bicondylar angle may simply be a modeling effect of differential induction of regional mitosis in the distal femoral growth plate, the chondral epiphysis, or both in response to a medial joint position required during habitual upright gait (58). Other unique characters, such as tibial dom- inance, however, would at first seem to require much more complicated origins. At the same time, given the plasticity of developing joint cartilage, relatively simple changes in pattern formation can underlie profound downstream changes. This type of pathway is the most probable means by which the generalized morphology of the hominoid distal femur was transformed into its highly specialized human form. Specifically, elongation of the lateral femoral condyle could have been introduced by a slight increase in the anteroposterior length of its prechondrogenic mesenchy- mal field by only a few cell diameters or by a slight respecification of postanlagen growth. Such a change, in conjunction with cartilage plasticity and a habitual bipedal gait (which generates continuously high levels of tibiofemoral force in and about full extension) (Fig. 2), can account for virtually the entirety of the unique morphology of the human knee. Therefore, what appears to be a profusion of separate traits may very well reflect a profoundly simpler, albeit highly influential, change in the pattern formation field of the human distal femur. Although the above examples have been restricted to issues of human evolution, expositions directly linking equally dramatic anatomical changes to pattern formation shifts are readily available for other mammals and even classes [the origin of the fibular crest of birds and of the elongated tarsus of frogs are particularly striking examples (59–62)]. Etiology. Let us summarize the discussion to this point. A mammalian bone is ultimately the product of coding specified in its positional information (PI). That PI is manifested down- stream by specific local growth and development regimens specific to each presumptive bone. Those regimens are in turn expressed by employment of a variety of highly conserved systemic assembly mechanisms (SAMs). Although subtle differ- ences in PI can be unique to a species, the SAMs are not. They are shared among large numbers of taxa, and probably do not differ significantly among most mammals. This is highly probable simply because any alteration of such tissue and cellular response protocols would systemically alter the entire skeleton whereas subtle, local changes in the growth of a primordium have only limited effects. SAMs are therefore almost certainly highly conserved as they constitute a fundamental raw material of musculoskeletal evolution and mammalian ‘‘evolvability’’ (63). On the other hand, changes in such ‘‘rules’’ may have served to generate some major adaptive radiations. In many cases of anatomical trait analysis, it will be difficult to distinguish among possible etiological pathways for the features being studied. However, the difficulty of this task does not make it insoluble, nor does it permit us to merely ignore its potentially profound implications, as viable hypotheses can now be con- structed from our expanding knowledge of vertebrate develop- ment. For example, studies of the acquisition of the bicondylar angle in normal and myelodysplastic children suggest that this character is progressively acquired by responsive modeling in the joint cartilage, growth ...
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... fixed in the genome because virtually none is likely to have been a consequence of localized gene expression specific to each defined trait. Subtle changes in presumptive tissue fields such as those hypothesized here will typically yield many down- stream effects, but only the most prominent are likely to have had a sufficiently significant effect on function to actually affect fitness. Except in rare instances (which can possibly serve as examples of punctuated ‘‘breakthrough’’ adaptations), most others will merely be retained byproducts of the primary changes. The transverse distance between the hip joints of the early hominid pelvis can serve to illustrate this important point. A notable consequence of the overall broadening of the early hominid pelvis is that the relative distance between the two hip joints was also increased. This is an apparent disadvantage during bipedal locomotion because it requires greater abductor contraction during the single leg phase (i.e., it reduces the lever arm length of the pelvic stabilizers). Does this increased distance therefore ‘‘demand some special functional explanation’’ as several authors have insisted (ref. 49, p. 285; see also ref. 50)? The answer is very probably no, so long as consideration is given to the manner in which the ancestral–descendant transition is likely to have been achieved morphogenetically, and the entire pelvis is not atomized into component parts that, in fact, probably have no individual, separable, heritability (51). By what other genetic means than that outlined here was the hominid pelvis so systematically and rapidly altered? By separate, inde- pendent fixation of all of its novel anatomical features [broader ilium, broader sacrum, longer (i.e., broader) femoral neck, longer (i.e., broader) pubic rami, shorter ilium, shorter pubic joint, etc.]? Are we to presume that each such isolated change in pelvic structure had a sufficiently strong effect on reproductive success to have been independently altered and fixed in the genome, even if realistic genetic models for the individual specification of each such feature were available? Many such complicated (even labyrinthine) biomechanical explanations of these pelvic traits have been posited (49, 50), but, in light of what we have discovered about morphogenesis in limbs, such analyses have been rendered unreasonable. Cartilage Modeling and the Evolution of the Human Knee. As noted earlier, the tissues of the musculoskeletal system are exquisitely sensitive to mechanical loading. This sensitivity can be ‘‘exploit- ed’’ by selection to produce relatively profound anatomical changes with only minimal changes in PI. The evolution of the human knee (Fig. 2) can serve as an excellent example of the potential role of such SAMs in the evolution of the mammalian postcranium. When two or more bones that comprise a synovial joint move relative to one another, they must do so in a manner that generates velocity vectors that are continuously tangential to their contacting surfaces. If this is not the case, the two rigid bodies will deform and degrade their contacting surfaces. This results in their eventual destruction and further kinematic derangement (52, 53). In addition, the joint’s inherent tensile restraint system of ligaments and tendons must also be in exacting compliance with the joint’s pathway of motion, so that it can maintain that pathway in the face of any external forces that tend to dislodge it. Mammalian joints, therefore, must develop inviolate coordi- nation between their surface geometries and soft tissue restraint systems (54) (Fig. 2). It is virtually inconceivable that such exact conformity between the mating surfaces of a synovial joint could be dictated in some directly heritable fashion (i.e., by descriptive specification). This would require not only an exact ordination of the three-dimensional form of the mated surfaces but equally exacting construction of the network of individual fiber bundles that compose each of the joint’s ligaments, all of which would be in some way subject to the process of genetic recombination. Clearly, such exacting geometries are not directly heritable. We have long known, since the classic tissue culture experi- ments of Murray (55) and Fell (56), that cartilage exhibits considerable mechanical reactivity, and there is now substantial direct experimental evidence of its robust modeling capacity, including recent demonstrations that chondrocytes are ‘‘very sensitive to loading pattern’’ (ref. 57, p. 906) and that imposed loads act to calibrate their metabolic activity, including the up- and down-regulation of matrix synthesis (reviewed in ref. 57). It is therefore increasingly likely that joint geometry is quite plastic even though such plasticity ceases at adulthood (there are no repair mechanisms). This SAM has great import with respect to the evolution of joint structure. The human knee differs dramatically from that of other primates (Fig. 2), reflecting a highly specialized adaptation to bipedality. How were all of these dramatic changes acquired by humans and their ancestors? The bicondylar angle may simply be a modeling effect of differential induction of regional mitosis in the distal femoral growth plate, the chondral epiphysis, or both in response to a medial joint position required during habitual upright gait (58). Other unique characters, such as tibial dom- inance, however, would at first seem to require much more complicated origins. At the same time, given the plasticity of developing joint cartilage, relatively simple changes in pattern formation can underlie profound downstream changes. This type of pathway is the most probable means by which the generalized morphology of the hominoid distal femur was transformed into its highly specialized human form. Specifically, elongation of the lateral femoral condyle could have been introduced by a slight increase in the anteroposterior length of its prechondrogenic mesenchy- mal field by only a few cell diameters or by a slight respecification of postanlagen growth. Such a change, in conjunction with cartilage plasticity and a habitual bipedal gait (which generates continuously high levels of tibiofemoral force in and about full extension) (Fig. 2), can account for virtually the entirety of the unique morphology of the human knee. Therefore, what appears to be a profusion of separate traits may very well reflect a profoundly simpler, albeit highly influential, change in the pattern formation field of the human distal femur. Although the above examples have been restricted to issues of human evolution, expositions directly linking equally dramatic anatomical changes to pattern formation shifts are readily available for other mammals and even classes [the origin of the fibular crest of birds and of the elongated tarsus of frogs are particularly striking examples (59–62)]. Etiology. Let us summarize the discussion to this point. A mammalian bone is ultimately the product of coding specified in its positional information (PI). That PI is manifested down- stream by specific local growth and development regimens specific to each presumptive bone. Those regimens are in turn expressed by employment of a variety of highly conserved systemic assembly mechanisms (SAMs). Although subtle differ- ences in PI can be unique to a species, the SAMs are not. They are shared among large numbers of taxa, and probably do not differ significantly among most mammals. This is highly probable simply because any alteration of such tissue and cellular response protocols would systemically alter the entire skeleton whereas subtle, local changes in the growth of a primordium have only limited effects. SAMs are therefore almost certainly highly conserved as they constitute a fundamental raw material of musculoskeletal evolution and mammalian ‘‘evolvability’’ (63). On the other hand, changes in such ‘‘rules’’ may have served to generate some major adaptive radiations. In many cases of anatomical trait analysis, it will be difficult to distinguish among possible etiological pathways for the features being studied. However, the difficulty of this task does not make it insoluble, nor does it permit us to merely ignore its potentially profound implications, as viable hypotheses can now be con- structed from our expanding knowledge of vertebrate develop- ment. For example, studies of the acquisition of the bicondylar angle in normal and myelodysplastic children suggest that this character is progressively acquired by responsive modeling in the joint cartilage, growth plate, or both whereas the effects of a variety of HOX knockouts clearly imply that bony superstruc- tures such as the deltoid crest are at least partially read-outs of PI (23). We have known for years that the sagittal crest is merely a direct consequence of tension developed by fusion of the contralateral temporalis fascias (64). These represent the kinds of information that can be gleaned from investigations of development and applied toward a more informed interpreta- tion of the fossil record. We believe that the foregoing discussions provide the basis for a classification system that can greatly facilitate the decision- making process and thereby improve the accuracy of phyloge- netic and functional analyses. We propose that differences in adult traits between taxa be formally classified, whenever pos- sible, into the five categories defined in Table 1. Types 1 and 2 are traits that can, in theory, be traced to changes in PI. Type 3 traits are those that have systemic effects because of the alter- ation of a SAM or other systemic, genetically determined, effect. Alternatively, Type 3 traits may be the product of unmodified but currently poorly understood SAMs, such as allometric adjust- ments to simple changes in body size. Types 1 and 2 are true individually heritable genomic differences. Type 3 traits may be specific heritable changes or ...
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... in which the ancestral–descendant transition is likely to have been achieved morphogenetically, and the entire pelvis is not atomized into component parts that, in fact, probably have no individual, separable, heritability (51). By what other genetic means than that outlined here was the hominid pelvis so systematically and rapidly altered? By separate, inde- pendent fixation of all of its novel anatomical features [broader ilium, broader sacrum, longer (i.e., broader) femoral neck, longer (i.e., broader) pubic rami, shorter ilium, shorter pubic joint, etc.]? Are we to presume that each such isolated change in pelvic structure had a sufficiently strong effect on reproductive success to have been independently altered and fixed in the genome, even if realistic genetic models for the individual specification of each such feature were available? Many such complicated (even labyrinthine) biomechanical explanations of these pelvic traits have been posited (49, 50), but, in light of what we have discovered about morphogenesis in limbs, such analyses have been rendered unreasonable. Cartilage Modeling and the Evolution of the Human Knee. As noted earlier, the tissues of the musculoskeletal system are exquisitely sensitive to mechanical loading. This sensitivity can be ‘‘exploit- ed’’ by selection to produce relatively profound anatomical changes with only minimal changes in PI. The evolution of the human knee (Fig. 2) can serve as an excellent example of the potential role of such SAMs in the evolution of the mammalian postcranium. When two or more bones that comprise a synovial joint move relative to one another, they must do so in a manner that generates velocity vectors that are continuously tangential to their contacting surfaces. If this is not the case, the two rigid bodies will deform and degrade their contacting surfaces. This results in their eventual destruction and further kinematic derangement (52, 53). In addition, the joint’s inherent tensile restraint system of ligaments and tendons must also be in exacting compliance with the joint’s pathway of motion, so that it can maintain that pathway in the face of any external forces that tend to dislodge it. Mammalian joints, therefore, must develop inviolate coordi- nation between their surface geometries and soft tissue restraint systems (54) (Fig. 2). It is virtually inconceivable that such exact conformity between the mating surfaces of a synovial joint could be dictated in some directly heritable fashion (i.e., by descriptive specification). This would require not only an exact ordination of the three-dimensional form of the mated surfaces but equally exacting construction of the network of individual fiber bundles that compose each of the joint’s ligaments, all of which would be in some way subject to the process of genetic recombination. Clearly, such exacting geometries are not directly heritable. We have long known, since the classic tissue culture experi- ments of Murray (55) and Fell (56), that cartilage exhibits considerable mechanical reactivity, and there is now substantial direct experimental evidence of its robust modeling capacity, including recent demonstrations that chondrocytes are ‘‘very sensitive to loading pattern’’ (ref. 57, p. 906) and that imposed loads act to calibrate their metabolic activity, including the up- and down-regulation of matrix synthesis (reviewed in ref. 57). It is therefore increasingly likely that joint geometry is quite plastic even though such plasticity ceases at adulthood (there are no repair mechanisms). This SAM has great import with respect to the evolution of joint structure. The human knee differs dramatically from that of other primates (Fig. 2), reflecting a highly specialized adaptation to bipedality. How were all of these dramatic changes acquired by humans and their ancestors? The bicondylar angle may simply be a modeling effect of differential induction of regional mitosis in the distal femoral growth plate, the chondral epiphysis, or both in response to a medial joint position required during habitual upright gait (58). Other unique characters, such as tibial dom- inance, however, would at first seem to require much more complicated origins. At the same time, given the plasticity of developing joint cartilage, relatively simple changes in pattern formation can underlie profound downstream changes. This type of pathway is the most probable means by which the generalized morphology of the hominoid distal femur was transformed into its highly specialized human form. Specifically, elongation of the lateral femoral condyle could have been introduced by a slight increase in the anteroposterior length of its prechondrogenic mesenchy- mal field by only a few cell diameters or by a slight respecification of postanlagen growth. Such a change, in conjunction with cartilage plasticity and a habitual bipedal gait (which generates continuously high levels of tibiofemoral force in and about full extension) (Fig. 2), can account for virtually the entirety of the unique morphology of the human knee. Therefore, what appears to be a profusion of separate traits may very well reflect a profoundly simpler, albeit highly influential, change in the pattern formation field of the human distal femur. Although the above examples have been restricted to issues of human evolution, expositions directly linking equally dramatic anatomical changes to pattern formation shifts are readily available for other mammals and even classes [the origin of the fibular crest of birds and of the elongated tarsus of frogs are particularly striking examples (59–62)]. Etiology. Let us summarize the discussion to this point. A mammalian bone is ultimately the product of coding specified in its positional information (PI). That PI is manifested down- stream by specific local growth and development regimens specific to each presumptive bone. Those regimens are in turn expressed by employment of a variety of highly conserved systemic assembly mechanisms (SAMs). Although subtle differ- ences in PI can be unique to a species, the SAMs are not. They are shared among large numbers of taxa, and probably do not differ significantly among most mammals. This is highly probable simply because any alteration of such tissue and cellular response protocols would systemically alter the entire skeleton whereas subtle, local changes in the growth of a primordium have only limited effects. SAMs are therefore almost certainly highly conserved as they constitute a fundamental raw material of musculoskeletal evolution and mammalian ‘‘evolvability’’ (63). On the other hand, changes in such ‘‘rules’’ may have served to generate some major adaptive radiations. In many cases of anatomical trait analysis, it will be difficult to distinguish among possible etiological pathways for the features being studied. However, the difficulty of this task does not make it insoluble, nor does it permit us to merely ignore its potentially profound implications, as viable hypotheses can now be con- structed from our expanding knowledge of vertebrate develop- ment. For example, studies of the acquisition of the bicondylar angle in normal and myelodysplastic children suggest that this character is progressively acquired by responsive modeling in the joint cartilage, growth plate, or both whereas the effects of a variety of HOX knockouts clearly imply that bony superstruc- tures such as the deltoid crest are at least partially read-outs of PI (23). We have known for years that the sagittal crest is merely a direct consequence of tension developed by fusion of the contralateral temporalis fascias (64). These represent the kinds of information that can be gleaned from investigations of development and applied toward a more informed interpreta- tion of the fossil record. We believe that the foregoing discussions provide the basis for a classification system that can greatly facilitate the decision- making process and thereby improve the accuracy of phyloge- netic and functional analyses. We propose that differences in adult traits between taxa be formally classified, whenever pos- sible, into the five categories defined in Table 1. Types 1 and 2 are traits that can, in theory, be traced to changes in PI. Type 3 traits are those that have systemic effects because of the alter- ation of a SAM or other systemic, genetically determined, effect. Alternatively, Type 3 traits may be the product of unmodified but currently poorly understood SAMs, such as allometric adjust- ments to simple changes in body size. Types 1 and 2 are true individually heritable genomic differences. Type 3 traits may be specific heritable changes or conversely, as just noted, the product of the interplay of SAMs with Types 1 and ͞ or 2. Types 4 and 5 reflect the nonheritable effects of the interplay between unmodified SAMs, local mechanical environments, and the epigenetic effects of changes at other sites. How are traits to be allocated to one of these five categories, given that virtually nothing is known about their actual genetic basis and that such knowledge is virtually unobtainable for extinct organisms? Our proposed classification is not intended to require such knowledge, but only to encourage observers to formally state the presumed morphogenetic basis of each of the traits they choose to include in a functional or phyletic analysis. Such basis should be consistent with our current understanding of postcranial morphogenesis; i.e., a hypothesis should be con- gruent with possible morphogenetic pathways, such as changes in the distribution pattern of PI, alterations of anlagen shape, or the composition of compartments. Resulting classifications may then be treated as hypotheses for further study and analysis. Conclusion. The recognition of biologically independent characters is fundamental to the analysis of fossils, and character atomization can lead to serious errors of over (or under) weighting in both ...

Citations

... association with the acquisition of a bipedal gait through the conjugate action of gravity and muscular forces (Amtmann, 1979;Lovejoy et al., 2000;Tardieu, 1999Tardieu, , 2010Tardieu et al., 2013). ...
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Article
The acquisition of habitual bipedal locomotion, which resulted in numerous modifications of the skeleton was a crucial step in hominid evolution. However, our understanding of the inherited skeletal modifications versus those acquired while learning to walk remains limited. We here present data derived from X-rays and CT scans of quadrupedal adult humans and compare the morphology of the vertebral column, pelvis and femur to that of a bipedal brother. We show how a skeleton forged by natural selection for bipedal locomotion is modified when used to walk quadrupedally. The quadrupedal brother is characterised by the absence of femoral obliquity, a very high anteversion angle of the femoral neck, a very high collo-diaphyseal angle and a very reduced lordosis. The differences in the pelvis are more subtle and complex, yet of functional importance. The modification of the ischial spines to an ischial ridge and the perfectly rounded shape of the sacral curvature are two unique features that can be directly attributed to a quadrupedal posture and locomotion. We propose a functional interpretation of these two exceptional modifications. Unexpectedly, the quadrupedal brother and sister show a greater angle of pelvic incidence compared to their bipedal brother, a trait previously shown to increase with learning to walk in bipedal subjects. Moreover, the evolution from an occasional towards a permanent bipedality has given rise to a functional association between the angle of pelvic incidence and the lumbar curvature, with high angles of incidence and greater lumbar curvature promoting stability during bipedal locomotion. The quadrupedal brother and sister with a high angle of incidence and a very reduced lordosis thus show a complete decoupling of this complex functional integration.
... Since similar angulation is also present in anatomically modern humans, but is not seen in early fossil hominids, 1 they concluded that this morphology is homoplastic in Gorilla, Pan, and humans. They further surmised that the ulnarly deviated MC3 found in African apes and humans was either a consequence of selection for a power grip in humans and for suspension and/or vertical climbing (sensu stricto) in African apes (type 1), or the result of cartilage modeling imposed by differential loading during development while performing such activities (type 4) (developmental morphotype classifications and their definitions are provided in Lovejoy et al., 1999Lovejoy et al., , 2000Lovejoy et al., , 2009a. ...
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Article
Previously, we described several features of the carpometacarpal joints in extant large-bodied apes that are likely adaptations to the functional demands of vertical climbing and suspension. We observed that all hominids, including modern humans and the 4.4 million-year-old hominid Ardipithecus ramidus, lacked these features. Here, we assess the uniqueness of these features in a large sample of monkey, ape, and human hands. These new data provide additional insights into the functional adaptations and evolution of the anthropoid hand. Our survey highlights a series of anatomical adaptations that restrict motion between the second and third metacarpals (MC2, MC3) and their associated carpals in extant apes, achieved via joint reorganization and novel energy dissipation mechanisms. Their hamate-MC4 and -MC5 joint surface morphologies suggest limited mobility, at least in Pan. Gibbons and spider monkeys have several characters (angled MC3, complex capitate-MC3 joint topography, variably present capitate-MC3 ligaments), that suggest functional convergence in response to suspensory locomotion. Baboons have carpometacarpal morphology suggesting flexion/extension at these joints beyond that observed in most other Old World monkeys, probably as an energy dissipating mechanism minimizing collision forces during terrestrial locomotion. All hominids lack these specializations of the extant great apes, suggesting that vertical climbing was never a central feature of our ancestral locomotor repertoire. Furthermore, the reinforced carpo-metacarpus of vertically climbing African apes was likely appropriated for knuckle-walking in concert with other novel potential energy dissipating mechanisms. The most parsimonious explanation of the structural similarity of these carpo-metacarpal specializations in great apes is that they evolved independently. This article is protected by copyright. All rights reserved.
... These are described in relation to the upper ankle joint interface rather than standard anatomical nomenclature. The end-point morphology encountered among the taxa examined reflect multiple factors related to the joint's biological role (sensu Bock and von Wahlert, 1965) including phylogeny, physical attributes, and behavior, which have been related to articular shape (Lovejoy et al., 2000;Lieberman et al., 2001;Pearson, 2004;Hall, 2005;Turley et al., 2011). The influence of each on shape and their interdependence were assessed in this study (Lovejoy et al., 2000;Lieberman et al., 2001;Pearson, 2004;Hall, 2005;Turley et al., 2011). ...
... The end-point morphology encountered among the taxa examined reflect multiple factors related to the joint's biological role (sensu Bock and von Wahlert, 1965) including phylogeny, physical attributes, and behavior, which have been related to articular shape (Lovejoy et al., 2000;Lieberman et al., 2001;Pearson, 2004;Hall, 2005;Turley et al., 2011). The influence of each on shape and their interdependence were assessed in this study (Lovejoy et al., 2000;Lieberman et al., 2001;Pearson, 2004;Hall, 2005;Turley et al., 2011). ...
... This study centered on the articular component of talar joint morphology, as did our previous study of the tibia (Turley et al., 2011). The influence of substrate preference identified here reinforces the findings in the distal tibia, that in the talo-crural joint, homoplasy of the talar proximal articular morphology may be observed in distantly related taxa (at least between Catarrhine superfamilies), and differences in proximal talar form of closely related taxa may reflect variation due to environmentally induced change in substrate use (Lovejoy et al., 2000;Retallack, 2001;Wagner, 2001;Hall, 2005;Begun, 2007;Turley et al., 2011;Singleton, 2012). ...
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Conference Paper
Understanding talar functional morphology is pivotal to understand the evolution of hominin bipedalism due to its role during locomotion, in part controlling dorsi-plantar flexion, ab-adduction and in-eversion of the foot. Despite recent contributions having utilized increasingly advanced digital methods, further work is warranted to quantify talar shape variation in hominoid primates. Here we apply a geometric morphometric landmark based method, to explore morphological differences in hominoid tali. A template of 251 landmarks (n=15) and semilandmarks (n=236) was digitized on 3D digital models of 80 hominoid tali (H. sapiens=20, Pan=20, Gorilla=20, Pongo=20). The models were superimposed with Generalized Procrustes Analysis (GPA), which translates and rotates to minimize the squared distances between homologous landmarks and scales to unit centroid size. Principal Component Analysis (PCA) was used to explore morphological variation of the sample. The first three PCs describe 52,1% of sample variance. Great apes and modern humans separate on PC1 (30,5%), where specimens with positive scores (great apes) exhibited a shorter neck and an overall rounder shape, those with negative scores (H. sapiens) exhibited a longer neck and shallow groove for the flexor hallucis longus tendon area, with an overall stretched shape. PC2 (13,5%) is less informative, though a trend within the great apes sample can be observed from a flatter, longer positive shape to a rounder, shorter negative shape. Future work will include early hominin tali to shed light on the functional demands experienced by the ankle and the hindfoot during the evolution of hominin bipedalism.
... Type 4: A trait that differs between taxa because its presence/absence and/or " grade " are attributable exclusively to phenotypic effects of the interaction of " systematic assembly mechanisms " [11] fluctuating degree states ( " particularism " ) as it is to avoid its parent fallacy of " adaptationism " [3,4]. As we have detailed elsewhere [11,12] , it is now possible to construct reasonable hypotheses of the probable developmental etiology of many mammalian musculoskeletal traits. Such traits are divisible into two primary categories—those which have a distinct genic basis fixed and integrated during pattern formation and those which are largely the product of connective tissues' response to their environment, sensu lato. ...
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... Variation in presentation and articular morphology reflect natural selection for its genetically canalized state and the response of the organism to the biomechanical stresses encountered during ontogeny. Both of these factors produce the endpoint morphology encountered in the individual (Lovejoy et al., 2000;Lieberman et al., 2001;Pearson, 2004;Hall, 2005). Variation in this endpoint morphology allows for the differences in functional morphology of this joint complex among taxa. ...
... It demonstrated both differences and similarities among the studied taxa in both proximal presentation and appositional articular morphology (Conroy and Rose, 1983;Meldrum, 1991;Stern and Susman, 1991;Lockwood and Fleagle, 1999). The influence of substrate preferences on variation observed suggests that within this highly constrained character state, homoplasty of presentation and articular shape may allow adaptation of phylogenetically distant taxa to comparable substrate demands (Lovejoy et al., 2000;Wagner, 2001;Hall, 2005;Begun, 2007). ...
Article
The proximal component of the talo-crural joint, the tibia, was compared, using geometric morphometrics, in 240 specimens from 10 extant taxa to identify differences in shape and the factors influencing them. The specimens were laser scanned, digitally reconstructed, and landmarked. Regression analysis was used to evaluate tibial shape, and significant amounts of shape variation among taxa were due to body mass, tibial size, superfamily, and substrate preference in the whole tibia, as well as, separate analysis of the distal tibial articular facets, and the medial malleolar facet. The most important factor for whole tibial shape was tibial robusticity, which closely correlated with body mass. However, substrate preference was also a significant factor in tibial shape and independent from body mass. Substrate preference was also the most important factor defining distal articular morphology. Principal components analysis and pairwise permutation tests were used to compare differences in morphology among taxa. Nearly all were significantly different in overall tibial shape, and distal morphology. Shape and presentational morphology associated with body mass, tibial size, superfamily, and substrate preference were identified, along with the similarities and differences among individual taxa. These were visualized by TPS deformation of an exemplar surface. Relationships among these factors were assessed with their dot-product. Results demonstrated that size significantly influenced proximal presentation, while substrate preference influenced articular morphology.
... Despite a relatively rich, well-dated fossil record and many methodological improvements (e.g., Chamberlain and Wood, 1987; Skelton and McHenry, 1992; Lieberman et al., 1996; Strait et al., 1997; Strait and Grine, 1999 ), cladistic analyses have so far been unable to estimate the phylogenetic relationships of several fossil hominin species with a reasonable level of confidence (Corruccini, 1994; Lieberman et al., 1996; Wood and Collard, 1999; Strait and Grine, 2004). Our inability to reliably reconstruct these relationships has frequently been attributed to taxonomic uncertainties, to the use of incorrect characters, and/or to the way in which the cladistic methodology has been implemented (e.g., Chamberlain and Wood, 1987; Skelton and McHenry, 1992; Lieberman, 1995 Lieberman, , 1999 Strait et al., 1997; Skelton and McHenry, 1998; Strait and Grine, 1998; Lovejoy et al., 1999 Lovejoy et al., , 2000 McCollum, 1999; McCollum and Sharpe, 2001). In recent years, however, attention has focused on the confounding effects of homoplasies (e.g., Wood and Chamberlain, 1986; Skelton and McHenry, 1992; McHenry, 1994 McHenry, , 1996 Lieberman, 1997 Lieberman, , 1999 Lieberman, , 2000 Lieberman et al., 1996; Lockwood and Fleagle, 1999; Wood, 2000, 2001 ). ...
... characters used in the analysis are random with regard to the relationships they suggest and some of them necessarily must yield the correct relationships because there are so few ways in which the extant hominoid genera can be linked. Alternatively, the moderate-to-high-strain characters may constitute a complex of highly integrated, nonindependent characters whose phenotypic expression merely correlates well with the correct cladogram (Lieberman 1999; Lovejoy et al., 1999 Lovejoy et al., , 2000 McCollum, 1999; McCollum and Sharpe, 2001; Naylor and Adams, 2001; Strait 2001; see also Strait et al., 2007). Currently, there is little evidence to support either of these explanations. ...
... However, when analyzing characters from different species, the situation is almost certainly more complicated because of morphological integration. As has been noted by a number of authors, few skeletal features are independent; instead, they are integrated at numerous hierarchical levels of development (Olsen and Miller, 1958; Cheverud, 1982; Lieberman, 1999; Lovejoy et al., 1999 Lovejoy et al., , 2000 McCollum, 1999; McCollum and Sharpe, 2001; Naylor and Adams, 2001; Strait, 2001; Lockwood, 2007; Strait et al., 2007). Thus, while the mechanisms by which bone tissue responds to strain may be conservative across species, the morphological effects of such responses may differ depending on a wide variety of other developmental and structural factors. ...
Article
Homoiologies are phylogenetically misleading morphological similarities that are due to nongenetic factors. It has been claimed that homoiologies are common in the hominin skull, especially in regions affected by masticatory strain, and that their prevalence is one reason why reconstructing hominin phylogenetic relationships is difficult. To evaluate this "homoiology hypothesis," we performed analyses on a group of extant primates for which a robust molecular phylogeny is available--the hominoids. We compiled a data set from measurements that developmental considerations and experimental evidence suggest differ in their likelihood of exhibiting masticatory-strain-induced phenotypic plasticity. We then used the coefficient of variation and t-tests to evaluate the phenotypic plasticity of the measurements. We predicted that, if the hypothesis is correct, the measurements of skeletal features that do not remodel and therefore are unaffected by phenotypic plasticity should be less variable than the measurements of skeletal features that remodel and are subject to low-to-moderate strains, and that the latter should be less variable than the measurements of skeletal features that remodel and are subject to moderate-to-high strains. Subsequently, we performed phylogenetic analyses on character state data derived from the measurements and compared the resulting phylogenetic hypotheses to the consensus molecular phylogeny for the hominoids. We predicted that, if the hypothesis is correct, agreement between the phylogenies should be best for the non-phenotypically-plastic characters, intermediate for the low-to-moderate-strain characters, and worst for the moderate-to-high-strain characters. The results of the coefficient of variation/t-test analyses were consistent with the predictions of the hypothesis to the extent that the moderate-to-high-strain measurements exhibited significantly more variability than the non-phenotypically-plastic and low-to-moderate-strain measurements. In contrast, the results of the phylogenetic analyses were not those predicted. The phylogeny derived from the moderate-to-high-strain characters matched the molecular phylogeny better than those obtained using the non-phenotypically-plastic and low-to-moderate-strain characters. Thus, our study supports the suggestion that mechanical loading results in phenotypic plasticity in the hominin skull, but it does not support the notion that homoiologies have a significant negative impact on hominin phylogenetics.
... Although it has been argued that specimens from Australopithecus afarensis retain the more primitive, chimpanzee-like, morphology [34,35], the meniscal attachment topography of hominoid proximal tibias is simply too ambiguous to confirm or refute this claim. In any case, the shift is almost certainly a type 2 trait (i.e., a nonsignificant developmental ''byproduct'') [36] of either anteroposterior elongation of the condyle for increased cartilage contact, clearly present in A. afarensis, or for further elongation of the patellar moment arm, absent in A. afarensis (see below). In either case it is sagittal elongation of the lateral femoral condyle that is the key adaptive trait here, and this can be easily assessed. ...
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Article
The human fossil record is one of the most complete for any mammal. A basal ancestral species, Australopithecus afarensis, exhibits a well-preserved postcranium that permits reconstruction of important events in the evolution of our locomotor skeleton. When compared to those of living apes and humans, it provides insights into the origin and design of the modern human frame. Evolutionary aspects of the human knee are reviewed, including its highly specialized design with respect to upright walking and running. Design elements include increased tibial cartilage contact derived by both genomic and epigenetic mechanisms, valgus stance angulation, a mechanism for patellar retention, and a somewhat increased patellar moment arm. The history of these features in early hominids and their fundamental differences from their counterparts in apes are discussed.
... However, these investigators suggest that positional information becomes less important once the bone anlage is established. In contrast, a growing body of data supports the possibility that pattern formation continues to dominate through a broad range of development, and that the proposed early shift from pattern formation to mechanobiologic regulation probably does not occur (Lovejoy et al., 2000); mechanical forces remain perpetually secondary influences on the emergence of bone structure. This minimizes the traditional importance of mechanical stimuli in the emergence of morphology in accordance with Wolff 's law of the functional adaptation of bone. ...
Article
Experimental models are needed for resolving relative influences of genetic, epigenetic, and nonheritable functionally induced (extragenetic) factors in the emergence of developmental adaptations in limb bones of larger mammals. We examined regional/ontogenetic morphologic variations in sheep calcanei, which exhibit marked heterogeneity in structural and material organization by skeletal maturity. Cross-sections and lateral radiographs of an ontogenetic series of domesticated sheep calcanei (fetal to adult) were examined for variations in biomechanically important structural (cortical thickness and trabecular architecture) and material (percent ash and predominant collagen fiber orientation) characteristics. Results showed delayed development of variations in cortical thickness and collagen fiber orientation, which correlate with extragenetic factors, including compression/tension strains of habitual bending in respective dorsal/plantar cortices and load-related thresholds for modeling/remodeling activities. In contrast, the appearance of trabecular arches in utero suggests strong genetic/epigenetic influences. These stark spatial/temporal variations in sheep calcanei provide a compelling model for investigating causal mechanisms that mediate this construction. In view of these findings, it is also suggested that the conventional distinction between genetic and epigenetic factors in limb bone development be expanded into three categories: genetic, epigenetic, and extragenetic factors.
... When analysing the relationships among superspecific taxa, the situation may be more complicated because of morphological integration. As has been widely noted, few features of the skull are likely to be Table 6 Goodness-of-fit statistics associated with the most parsimonious cladograms recovered from the mixed-sex datasets, and those obtained when the consensus molecular topology for the papionins was imposed on the same datasets, after removal of characters that remain significantly correlated with the geometric mean after size-correction 1 (Olsen and Miller, 1958;Cheverud, 1982;Lieberman, 1999;Lovejoy et al., 1999Lovejoy et al., , 2000McCollum, 1999;Lieberman et al., 2000;McCollum and Sharpe, 2001;Strait, 2001). Thus, while the mechanisms by which bone tissue responds to strain may be conservative across species, the morphological effects of such responses may differ markedly depending on a wide variety of other developmental and structural factors. ...
Article
Homoiologies are phylogenetically misleading resemblances among taxa that can be attributed to phenotypic plasticity. Recently, it has been claimed that homoiologies are widespread in the hominid skull, especially in those regions affected by mastication-related strain, and that their prevalence is a major reason why researchers have so far been unable to obtain a reliable estimate of hominid phylogeny. To evaluate this “homoiology hypothesis,” we carried out analyses of a group of extant primates for which a robust molecular phylogeny is available—the papionins.
... For example, femoral anteversion. a For further discussion, see [11,12,15]. ...
... As we have detailed elsewhere [11,12], it is now possible to construct reasonable hypotheses of the probable developmental etiology of many mammalian musculoskeletal traits. Such traits are divisible into two primary categories-those which have a distinct genic basis fixed and integrated during pattern formation and those which are largely the product of connective tissues' response to their environment, sensu lato. ...
Full-text available
Article
The human fossil record is one of the most complete for any mammal. A basal ancestral species, Australopithecus afarensis, exhibits a well-preserved postcranium that permits reconstruction of important events in the evolution of our locomotor skeleton. When compared with those of living apes and modern humans, this species provides a number of insights into the origin and design of the modern human frame as well as the selective agencies that have guided its evolution during the past three million years. Evolutionary aspects of the human spine and pelvis are reviewed, including their impact on several clinically relevant aspects of human gait and posture.