Evolutionary origin of synovial joints

Abstract

Synovial joints, characterized by reciprocally congruent and lubricated articular surfaces separated by a cavity, are hypothesized to have evolved from continuous cartilaginous joints for increased mobility and improved load bearing. To test the evolutionary origins of synovial joints, we examine the morphology, genetic, and molecular mechanisms required for the development and function of the joints in elasmobranchs and cyclostomes. We find the presence of cavitated and articulated joints in elasmobranchs, such as the little skate (Leucoraja erinacea) and bamboo shark (Chiloscyllium plagiosum), and the expression of lubrication-related proteoglycans such as aggrecan and glycoproteins such as hyaluronic acid receptor (CD44) at the articular surfaces in little skates. Sea lampreys (Petromyozon marinus), a representative of cyclostomes, are devoid of articular cavities but express proteoglycan-linking proteins throughout their cartilaginous skeleton, suggesting that the expression of proteoglycans is primitively not limited to the articular cartilage. Analysis of the development of joints in the little skate reveals the expression of growth differentiation factor-5 (Gdf5) and {beta}-catenin at the joint interzone before the process of cavitation, indicating the involvement of BMP and Wnt-signaling pathway, and reliance on muscle contraction for the process of joint cavitation, similar to tetrapods. In conclusion, our results show that synovial joints are present in elasmobranchs but not cyclostomes, and therefore, synovial joints originated in the common ancestor of extant gnathostomes. A review of fossils from the extinct clades along the gnathostome stem further shows that synovial joints likely arose in the common ancestor of gnathostomes. Our results have implications for understanding how the evolution of synovial joints around 400 mya in our vertebrate ancestors unlocked motor behaviors such as feeding and locomotion. Author summaryWe owe our mobility and agility to synovial joints, characterized by a lubricated joint cavity between the bony elements. Due to the cavity, synovial joints function by bones sliding relative to each other, allowing an extensive range of motion and heightened stability compared to fused or cartilaginous joints that function by bending. Using histological and protein expression analysis, we show that reciprocally articulated, cavitated, and lubricated joints are present in elasmobranchs such as skates and sharks but not in cyclostomes such as the sea lamprey. Furthermore, the development of the little skate joints relies on genetic regulatory mechanisms such as BMP and Wnt-signalling, similar to tetrapods. Thus, our results show that synovial joints are present in elasmobranchs but not in cyclostomes. In conclusion, synovial joints originated in the common ancestor of jawed vertebrates. Furthermore, a review of fossil taxa along the gnathostome stem shows that cavitated joints that function by relative sliding of articulating surfaces originated at the common ancestor of all gnathostomes. Our results have consequences for understanding how the evolution of cavitated and lubricated joints in ancient vertebrates impacted behaviors like feeding and locomotion 400 million years ago.