Bone gain and loss: insights from genomes and fossils

Abstract

In the human body, bones are dynamic and highly tuned organs that allow efficient movement, protect vital organs and house the bone marrow [1]. Among the four skeletal tissue types (bone, dentine, enamel, cartilage) in vertebrates, bone is the most distinct and diversified mineralized tissue that is patterned to provide maximal strength withminimal mass [2]. Based on the bone formation or ossification types in the embryos and young of vertebrates, bones are classified into themembrane (achondral) and chondral bones, the latter comprising perichondral and endochondral bones (Fig. 1) [3]. In living vertebrates, in contrast to the widespread distribution of cartilage, bone is only present in osteichthyans or bony vertebrates (bony fishes and tetrapods including ourselves). This raises the question whether the absence of bone in living chondrichthyans (cartilaginous fishes) [4,5] is a primitive retention or a derived trait due to the bone loss from a bony ancestor. The past decade has witnessed a dramatic increase in our understanding of the molecular and genomic bases of mineralized tissues [6–8] as well as that of early vertebrate evolution [9–12]. New breakthroughs from these two independent lines of research have provided unparalleled insights into the molecular mechanism and pacing of bone gain and loss in vertebrates (Fig. 2) [5]. One aspect of the mineralized tissue biology that has received extensive attention from molecular geneticists is the correlation between the phenotypic complexity of hard tissues in vertebrates and the SCPP (secretory calcium-binding phosphoprotein) gene family [6–8]. SCPP genes have a common ancestor, sparcl1 (sparc-like 1). Recent research suggests that at around the same time that early jawless fishes first evolved a mineralized skeleton, sparcl1 arose from sparc (gene for secreted protein, acidic and cysteine-rich) as a by-product of a whole-genome