Abstract

Jawed vertebrates (gnathostomes) have been the dominant lineage of deuterostomes for nearly three hundred fifty million years. Only a few lineages of jawless vertebrates remain in comparison. Composed of lampreys and hagfishes (cyclostomes), these jawless survivors are important systems for understanding the evolution of vertebrates. One focus of cyclostome research has been head skeleton development, as its evolution has been a driver of vertebrate morphological diversification. Recent work has identified hyaline-like cartilage in the oral cirri of the invertebrate chordate amphioxus, making cyclostomes critical for understanding the stepwise acquisition of vertebrate chondroid tissues. Our knowledge of cyclostome skeletogenesis, however, has lagged behind gnathostomes due to the difficulty of manipulating lamprey and hagfish embryos. In this review, we discuss and compare the regulation and histogenesis of cyclostome and gnathostome skeletal tissues. We also survey differences in skeletal morphology that we see amongst cyclostomes, as few elements can be confidently homologized between them. A recurring theme is the heterogeneity of skeletal morphology amongst living vertebrates, despite conserved genetic regulation. Based on these comparisons, we suggest a model through which these mesenchymal connective tissues acquired distinct histologies and that histological flexibility in cartilage existed in the last common ancestor of modern vertebrates.

Highlights

  • The evolution of vertebrates involved substantial elaboration of the ancestral chordate body plan

  • This suggests that the novel composition of vertebrate cartilage and its deployment may have been partly driven by the evolution of new vertebrate genes [16]

  • The few remaining jawless vertebrate taxa are known as cyclostomes, and they are an important lineage for understanding the evolution of vertebrate chondrogenesis

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Summary

Introduction

The evolution of vertebrates involved substantial elaboration of the ancestral chordate body plan. The few remaining jawless vertebrate taxa are known as cyclostomes, and they are an important lineage for understanding the evolution of vertebrate chondrogenesis This superclass consists of lampreys and hagfishes of approximately 110 species, and great progress has been made in recent decades to understand their development. In our understanding of the stepwise evolution of the vertebrate skeleton, we are presented with two challenges: (1) identifying core conserved features of vertebrate skeletal tissue; (2) identifying features that are likely evolutionary novelties in both jawed and extant jawless vertebrates. We see an intrinsic malleability of the vertebrate chondrocyte GRN, with varying features of non-skeletogenic connective tissues These comparisons indicate that skeletal heterogeneity was likely a feature in the last common ancestor of gnathostomes and cyclostomes, and these cell types have inherent similarities with tissues like the perichondrium and tendons

Overview of the Cartilaginous Skeleton of Lampreys and Hagfishes
History of Cyclostome Cartilage Research
The “Hard” and “Soft” Cartilages of Cyclostomes
Cyclostome Cartilage-Like Tissues
Looking Forward: A Synthesis of Classic Cyclostome Histology
Overview of Gnathostome Cartilage Development
All Gnathostome Cartilages Develop Using a Conserved Gene Regulatory Network
IX and type
Gnathostomes Have a Diversity of Cartilage Types
Common
Current Understanding of Cyclostome Cartilage Development
Identification of Unique Proteins in Cyclostome Skeletons
Aspects of the Skeletal GRN of Hagfish Appear Similar to That in Gnathostomes
The Core Skeletal GRN of Lamprey Is Similar to That in Gnathostomes
Larval Lampreys Have a Diversity of Cartilage Types
Future
Conclusions

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