Evolution of the patellar sesamoid bone in mammals

Abstract

The patella is a sesamoid bone located in the major extensor tendon of the knee joint, in the hindlimb of many tetrapods. Although numerous aspects of knee morphology are ancient and conserved among most tetrapods, the evolutionary occurrence of an ossified patella is highly variable. Among extant (crown clade) groups it is found in most birds, most lizards, the monotreme mammals and almost all placental mammals, but it is absent in most marsupial mammals as well as many reptiles. Here, we integrate data from the literature and first-hand studies of fossil and recent skeletal remains to reconstruct the evolution of the mammalian patella. We infer that bony patellae most likely evolved between four and six times in crown group Mammalia: in monotremes, in the extinct multituberculates, in one or more stem-mammal genera outside of therian or eutherian mammals and up to three times in therian mammals. Furthermore, an ossified patella was lost several times in mammals, not including those with absent hindlimbs: once or more in marsupials (with some re-acquisition) and at least once in bats. Our inferences about patellar evolution in mammals are reciprocally informed by the existence of several human genetic conditions in which the patella is either absent or severely reduced. Clearly, development of the patella is under close genomic control, although its responsiveness to its mechanical environment is also important (and perhaps variable among taxa). Where a bony patella is present it plays an important role in hindlimb function, especially in resisting gravity by providing an enhanced lever system for the knee joint. Yet the evolutionary origins, persistence and modifications of a patella in diverse groups with widely varying habits and habitats—from digging to running to aquatic, small or large body sizes, bipeds or quadrupeds—remain complex and perplexing, impeding a conclusive synthesis of form, function, development and genetics across mammalian evolution. This meta-analysis takes an initial step toward such a synthesis by collating available data and elucidating areas of promising future inquiry.

Gearing effects of the patella (knee extensor muscle sesamoid) of the helmeted guineafowl during terrestrial locomotion

“…The extent of inter‐individual versus inter‐species variation in patellar gearing is therefore unknown, and so more studies (particularly on lizards) involving more individuals are needed before both this and alternate hypotheses can be tested with confidence. A promising line of enquiry may stem from recent work inferring that patellae in birds (Regnault et al ., 2014), lizards (Regnault et al ., 2016) and mammals (Samuels, Regnault & Hutchinson, 2017) are unevenly phylogenetically distributed, even among quite closely related taxa. Direct comparison between the knee mechanics of closely related patella‐bearing and patella‐lacking species would be a logical next step in developing our understanding of the roles these sesamoid bones play in locomotion.…”

The baubellum is more developmentally and evolutionarily labile than the baculum

“…For example, mammals have independently lost their clavicles a minimum of four times, and digits in mammals have been independently lost dozens of times (Senter & Moch, 2015). The patella has been independently gained 4–6 times and lost twice in mammals (Samuels et al, 2017), gained multiple times in reptiles (Regnault et al, 2016), and has variable presence in amphibians (Abdala et al, 2017). Even in the face of these multiple independent transitions, clavicles, digits, and patella display the same trait in males and females across species.…”

Knee function through finite element analysis and the role of Miocene hominoids in our understanding of the origin of antipronograde behaviours: the Pierolapithecus catalaunicus patella as a case study

“…; Samuels et al . ). To create an easy‐to‐analyse, realistic and comparable model, the human knee joint was simplified in our modelling approach.…”

“…As mentioned above, the anatomy of the patella is still controversial, including the degree of differentiation of the quadriceps tendon into quadriceps and patellar tendons (Samuels et al . ). However, in order to implement the knee kinematic model virtually, we selected two areas of attachment (constrained regions) to fix the models: those of the QM and the PT (Fig.…”

“…In contrast, other authors advocate for differentiation of the quadriceps tendon into separate tendons, quadriceps and patellar (see a detailed summary in Samuels et al . and references therein). Since resolving anatomical knee issues is outside the scope of our study and this discussion does not directly affect our models, we consider the quadriceps and the patellar tendons as separate units in order to clearly limit the constraint areas of the model (see next subsection).…”