Anatomy, morphology and evolution of the patella in squamate lizards and tuatara (Sphenodon punctatus)

Abstract

The patella (kneecap) is the largest and best‐known of the sesamoid bones, postulated to confer biomechanical advantages including increasing joint leverage and reinforcing the tendon against compression. It has evolved several times independently in amniotes, but despite apparently widespread occurrence in lizards, the patella remains poorly characterised in this group and is, as yet, completely undescribed in their nearest extant relative Sphenodon (Rhynchocephalia). Through radiography, osteological and fossil studies we examined patellar presence in diverse lizard and lepidosauromorph taxa, and using computed tomography, dissection and histology we investigated in greater depth the anatomy and morphology of the patella in 16 lizard species and 19 Sphenodon specimens. We have found the first unambiguous evidence of a mineralised patella in Sphenodon, which appears similar to the patella of lizards and shares several gross and microscopic anatomical features. Although there may be a common mature morphology, the squamate patella exhibits a great deal of variability in development (whether from a cartilage anlage or not, and in the number of mineralised centres) and composition (bone, mineralised cartilage or fibrotendinous tissue). Unlike in mammals and birds, the patella in certain lizards and Sphenodon appears to be a polymorphic trait. We have also explored the evolution of the patella through ancestral state reconstruction, finding that the patella is ancestral for lizards and possibly Lepidosauria as a whole. Clear evidence of the patella in rhynchocephalian or stem lepidosaurian fossil taxa would clarify the evolutionary origin(s) of the patella, but due to the small size of this bone and the opportunity for degradation or loss we could not definitively conclude presence or absence in the fossils examined. The pattern of evolution in lepidosaurs is unclear but our data suggest that the emergence of this sesamoid may be related to the evolution of secondary ossification centres and/or changes in knee joint conformation, where enhancement of extensor muscle leverage would be more beneficial.

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.…”

“…This raises questions about the patellar sesamoids of other tetrapod vertebrates. Do these structures, which have evolved independently in birds, mammals and lizards (Dye, 1987;Sarin et al, 1999;Regnault, Pitsillides & Hutchinson, 2014;Regnault et al, 2016) share a similar gearing function? If so, why do some taxa have sesamoids in their knee extensor tendons, whereas others (even if similar in form and behaviour) do not?…”

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.…”

Evolution of the patellar sesamoid bone in mammals

“…In contrast, an ossified patella is present in many or most Squamata (lizards and kin) with limbs (Camp, 1923; Carrano, 2000; De Vriese, 1909; Dye, 1987, 2003; Gauthier et al, 2012; Haines, 1940, 1942; Hutchinson, 2002, 2004; Jerez & Tarazona, 2009; Maisano, 2002a; Regnault et al, 2016; Vickaryous & Olson, 2007). Patellar status (used throughout our study to refer to presence/absence of ossification in adults) is unknown for the (mostly extinct) Rhynchocephalia (sister group to Squamata), although a patella is at least sometimes present in the tuatara Sphenodon —the only extant rhynchocephalian (Regnault et al, 2016). An apparent sesamoid bone was noted in the knee joint region of a specimen of Macrocnemus , a mid-Triassic (∼235 Mya) reptile, which may be the earliest identified occurrence of a patella in any animal group (Rieppel, 1989), although this structure may have been a different sesamoid bone or ossicle.…”