Abstract
Vertebrates are the only animals that produce bone, but the molecular genetic basis for this evolutionary novelty remains obscure. Here, we synthesize information from traditional evolutionary and modern molecular genetic studies in order to generate a working hypothesis on the evolution of the gene regulatory network (GRN) underlying bone formation. Since transcription factors are often core components of GRNs (i.e., kernels), we focus our analyses on Sox9 and Runx2. Our argument centers on three skeletal tissues that comprise the majority of the vertebrate skeleton: immature cartilage, mature cartilage, and bone. Immature cartilage is produced during early stages of cartilage differentiation and can persist into adulthood, whereas mature cartilage undergoes additional stages of differentiation, including hypertrophy and mineralization. Functionally, histologically, and embryologically, these three skeletal tissues are very similar, yet unique, suggesting that one might have evolved from another. Traditional studies of the fossil record, comparative anatomy and embryology demonstrate clearly that immature cartilage evolved before mature cartilage or bone. Modern molecular approaches show that the GRNs regulating differentiation of these three skeletal cell fates are similar, yet unique, just like the functional and histological features of the tissues themselves. Intriguingly, the Sox9 GRN driving cartilage formation appears to be dominant to the Runx2 GRN of bone. Emphasizing an embryological and evolutionary transcriptomic view, we hypothesize that the Runx2 GRN underlying bone formation was co-opted from mature cartilage. We discuss how modern molecular genetic experiments, such as comparative transcriptomics, can test this hypothesis directly, meanwhile permitting levels of constraint and adaptation to be evaluated quantitatively. Therefore, comparative transcriptomics may revolutionize understanding of not only the clade-specific evolution of skeletal cells, but also the generation of evolutionary novelties, providing a modern paradigm for the evolutionary process.
Highlights
Cartilage and Bone might Share an Evolutionary HistoryMost of evolutionary theory has focussed on studies of morphological change among taxa, but the formation of tissue types can evolve in clade-specific manners
Two related, fascinating questions remain for future research: how did the gene regulatory network (GRN) directing skeletal cell differentiation appear, and how did they evolve afterward? In this review, we argue that gradual establishment of the Runx2 GRN during evolution of the mature chondrocyte is more parsimonious than the de novo appearance of the Runx2 GRN in osteoblasts (Figure 4)
We focus on the three main skeletal tissues present in vertebrates, and use findings from both traditional and modern studies to argue that bone evolved from mature cartilage
Summary
Vertebrates are the only animals that produce bone, but the molecular genetic basis for this evolutionary novelty remains obscure. We synthesize information from traditional evolutionary and modern molecular genetic studies in order to generate a working hypothesis on the evolution of the gene regulatory network (GRN) underlying bone formation. Histologically, and embryologically, these three skeletal tissues are very similar, yet unique, suggesting that one might have evolved from another. Traditional studies of the fossil record, comparative anatomy and embryology demonstrate clearly that immature cartilage evolved before mature cartilage or bone. Modern molecular approaches show that the GRNs regulating differentiation of these three skeletal cell fates are similar, yet unique, just like the functional and histological features of the tissues themselves. Emphasizing an embryological and evolutionary transcriptomic view, we hypothesize that the Runx GRN underlying bone formation was co-opted from mature cartilage.
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have