The neural crest is a vertebrate-specific migratory stem cell population that generates a remarkably diverse set of cell types and structures. Because many of the morphological, physiological and ...behavioural novelties of vertebrates are derived from neural crest cells, it is thought that the origin of this cell population was an important milestone in early vertebrate history. An outstanding question in the field of vertebrate evolutionary-developmental biology (evo-devo) is how this cell type evolved in ancestral vertebrates. In this review, we briefly summarize neural crest developmental genetics in vertebrates, focusing in particular on the gene regulatory interactions instructing their early formation within and migration from the dorsal neural tube. We then discuss how studies searching for homologues of neural crest cells in invertebrate chordates led to the discovery of neural crest-like cells in tunicates and the potential implications this has for tracing the pre-vertebrate origins of the neural crest population. Finally, we synthesize this information to propose a model to explain the origin of neural crest cells. We suggest that at least some of the regulatory components of early stages of neural crest development long pre-date vertebrate origins, perhaps dating back to the last common bilaterian ancestor. These components, originally directing neuroectodermal patterning and cell migration, served as a gene regulatory 'scaffold' upon which neural crest-like cells with limited migration and potency evolved in the last common ancestor of tunicates and vertebrates. Finally, the acquisition of regulatory programmes controlling multipotency and long-range, directed migration led to the transition from neural crest-like cells in invertebrate chordates to multipotent migratory neural crest in the first vertebrates.
Neural crest cells are central to vertebrate development and evolution, endowing vertebrates with a “new head” that resulted in morphological, physiological, and behavioral features that allowed ...vertebrates to become active predators. One remarkable feature of neural crest cells is their multi-germ layer potential that allows for the formation of both ectodermal (pigmentation, peripheral glia, sensory neurons) and mesenchymal (connective tissue, cartilage/bone, dermis) cell types. Understanding the cellular and evolutionary origins of this broad cellular potential in the neural crest has been a long-standing focus for developmental biologists. Here, we review recent work that has demonstrated that neural crest cells share key features with pluripotent blastula stem cells, including expression of the Yamanaka stem cell factors (Oct3/4, Klf4, Sox2, c-Myc). These shared features suggest that pluripotency is either retained in the neural crest from blastula stages or subsequently reactivated as the neural crest forms. We highlight the cellular and molecular parallels between blastula stem cells and neural crest cells and discuss the work that has led to current models for the cellular origins of broad potential in the crest. Finally, we explore how these themes can provide new insights into how and when neural crest cells and pluripotency evolved in vertebrates and the evolutionary relationship between these populations.
Glial cells in the nervous system regulate and support many functions related to neuronal activity. Understanding how the vertebrate nervous system has evolved demands a greater understanding of the ...mechanisms controlling evolution and development of glial cells in basal vertebrates. Among vertebrate glia, oligodendrocytes form an insulating myelin layer surrounding axons of the central nervous system (CNS) in jawed vertebrates. Jawless vertebrates lack myelinated axons but it is unclear when oligodendrocytes or the regulatory mechanisms controlling their development evolved. To begin to investigate the evolution of mechanisms controlling glial development, we identified key genes required for the differentiation of oligodendrocytes in gnathostomes, including Nkx2.2, SoxE genes, and PDGFR, analyzed their expression, and used CRISPR/Cas9 genome editing to perturb their functions in a primitively jawless vertebrate, the sea lamprey. We show in lamprey that orthologs required for oligodendrocyte development in jawed vertebrates are expressed in the lamprey ventral neural tube, in similar locations where gnathostome oligodendrocyte precursor cells (OPC) originate. In addition, they appear to be under the control of conserved mechanisms that regulate OPC development in jawed vertebrates and may also function in gliogenesis. Our results suggest that although oligodendrocytes first emerged in jawed vertebrates, regulatory mechanisms required for their development predate the divergence of jawless and jawed vertebrates.
•Oligodendrocyte markers are expressed in the lamprey ventral neural tube.•Regulation of oligodendrocyte markers controls glia outside the neural tube.•An Nkx2.2-PDGFR-SoxE axis was present in the vertebrate common ancestor.•Jawless and jawed vertebrates share common gliogenic regulatory mechanisms.
The acquisition of neural crest cells was a key step in the origin of the vertebrate body plan. An outstanding question is how neural crest cells acquired their ability to undergo an ...epithelial-mesenchymal transition (EMT) and migrate extensively throughout the vertebrate embryo. We tested if differential regulation of classical cadherins—a highly conserved feature of neural crest EMT and migration in jawed vertebrates—mediates these cellular behaviors in lamprey, a basal jawless vertebrate. Lamprey has single copies of the type I and type II classical cadherins (CadIA and CadIIA). CadIIA is expressed in premigratory neural crest, and requires the transcription factor Snail for proper expression, yet CadIA is never expressed in the neural tube during neural crest development, suggesting that differential regulation of classical cadherin expression is not required to initiate neural crest migration in basal vertebrates. We hypothesize that neural crest cells evolved by retention of regulatory programs linking distinct mesenchymal and multipotency properties, and emigrated from the neural tube without differentially regulating type I/type II cadherins. Our results point to the coupling of mesenchymal state and multipotency as a key event facilitating the origin of migratory neural crest cells.
•Lampreys contain a single epithelial and a single mesenchymal cadherin.•A mesenchymal, but not epithelial, cadherin is expressed in lamprey neural crest.•Snail regulates mesenchymal cadherin expression in lamprey migratory neural crest.•Modulation of cadherin expression is a gnathostome novelty for neural crest migration.•Cadherin expansion in gnathostomes is likely related to evolution of a GRN migratory module.
Neural crest and placodes are key innovations of the vertebrate clade. These cells arise within the dorsal ectoderm of all vertebrate embryos and have the developmental potential to form many of the ...morphological novelties within the vertebrate head. Each cell population has its own distinct developmental features and generates unique cell types. However, it is essential that neural crest and placodes associate together throughout embryonic development to coordinate the emergence of several features in the head, including almost all of the cranial peripheral sensory nervous system and organs of special sense. Despite the significance of this developmental feat, its evolutionary origins have remained unclear, owing largely to the fact that there has been little comparative (evolutionary) work done on this topic between the jawed vertebrates and cyclostomes—the jawless lampreys and hagfishes. In this review, we briefly summarize the developmental mechanisms and genetics of neural crest and placodes in both jawed and jawless vertebrates. We then discuss recent studies on the role of neural crest and placodes—and their developmental association—in the head of lamprey embryos, and how comparisons with jawed vertebrates can provide insights into the causes and consequences of this event in early vertebrate evolution.
Lampreys are one of the few survivors of an ancient lineage of jawless vertebrates and have become an important study organism in numerous disciplines in the biological sciences, including ...evolutionary biology, embryology, ecology, physiology and biomedicine. At the same time, however, lampreys have created economic and ecological problems due, primarily, to the invasion of parasitic sea lamprey (Petromyzon marinus) into the North American Great Lakes and consequent negative impacts on local fish populations. Barriers, trapping and lampricide treatments have reduced these impacts, but concern for habitat restoration, non-target effects and possible evolution of resistance to lampricides suggests the need to develop additional strategies that supplement current control measures. The advent of functional genomics, and in particular CRISPR/Cas9 genome editing, offers a molecular approach to this on-going problem. Here, we review the successful application of functional genetic, transcriptomic, and CRISPR/Cas9 genome editing technologies in lampreys to address basic research questions in the fields of evolutionary and developmental biology. We then describe how these tools may be repurposed for use by fishery and conservation biologists to approach the problem of invasive sea lamprey from a molecular-genetic perspective.
A major challenge in vertebrate evolution is to identify the gene regulatory mechanisms that facilitated the origin of neural crest cells and placodes from ancestral precursors in invertebrates. ...Here, we show in lamprey, a primitively jawless vertebrate, that the transcription factor Snail is expressed simultaneously throughout the neural plate, neural plate border, and pre-placodal ectoderm in the early embryo and is then upregulated in the CNS throughout neurogenesis. Using CRISPR/Cas9-mediated genome editing, we demonstrate that Snail plays functional roles in all of these embryonic domains or their derivatives. We first show that Snail patterns the neural plate border by repressing lateral expansion of Pax3/7 and activating nMyc and ZicA. We also present evidence that Snail is essential for DlxB-mediated establishment of the pre-placodal ectoderm but is not required for SoxB1a expression during formation of the neural plate proper. At later stages, Snail regulates formation of neural crest-derived and placode-derived PNS neurons and controls CNS neural differentiation in part by promoting cell survival. Taken together with established functions of invertebrate Snail genes, we identify a pan-bilaterian mechanism that extends to jawless vertebrates for regulating neurogenesis that is dependent on Snail transcription factors. We propose that ancestral vertebrates deployed an evolutionarily conserved Snail expression domain in the CNS and PNS for neurogenesis and then acquired derived functions in neural crest and placode development by recruitment of regulatory genes downstream of neuroectodermal Snail activity. Our results suggest that Snail regulatory mechanisms in vertebrate novelties such as the neural crest and placodes may have emerged from neurogenic roles that originated early in bilaterian evolution.
•Snail is expressed in vertebrate neural crest and invertebrate nervous systems.•Lamprey embryos use Snail for neural crest, placode and neural development.•Snail genes regulate neurogenesis across bilaterians.•Snail neural crest and placode regulation evolved from an ancient neurogenic role.
Summary
Vertebrates possess paired cranial sensory ganglia derived from two embryonic cell populations, neural crest and placodes. Cranial sensory ganglia arose prior to the divergence of jawed and ...jawless vertebrates, but the developmental mechanisms that facilitated their evolution are unknown. Using gene expression and cell lineage tracing experiments in embryos of the sea lamprey, Petromyzon marinus, we find that in the cranial ganglia we targeted, development consists of placode‐derived neuron clusters in the core of ganglia, with neural crest cells mostly surrounding these neuronal clusters. To dissect functional roles of neural crest and placode cell associations in these developing cranial ganglia, we used CRISPR/Cas9 gene editing experiments to target genes critical for the development of each population. Genetic ablation of SoxE2 and FoxD‐A in neural crest cells resulted in differentiated cranial sensory neurons with abnormal morphologies, whereas deletion of DlxB in cranial placodes resulted in near‐total loss of cranial sensory neurons. Taken together, our cell‐lineage, gene expression, and gene editing results suggest that cranial neural crest cells may not be required for cranial ganglia specification but are essential for shaping the morphology of these sensory structures. We propose that the association of neural crest and placodes in the head of early vertebrates was a key step in the organization of neurons and glia into paired sensory ganglia.
Incorporating microsatellite techniques to determine parentage is a powerful addition to behavioral mating system studies in wild animals. Nonetheless, in some tetrapod taxa such as lizards, there ...are relatively few direct comparisons of individual reproductive success measured genetically versus estimates based on behavioral interactions, especially in species where males and females do not maintain prolonged social contact. We combined observations of behavior with microsatellite analysis of parentage over ten seasons in male Collared Lizards, (
Crotaphytus collaris
), to test the extent to which the proportion of each female’s total courtship interactions with different males predicted the proportion of total offspring sired by those males (proportion of paternity). Territorial males (T-males) court females frequently. Non-territorial (NT) males on the other hand behave stealthily. This allows them to court females, albeit less frequently, while limiting attacks by T-males. Both T- and NT-males occupied habitats that varied in structural complexity which might influence which males court and sire offspring with individual females, therefore we included habitat type (simple vs. complex) and male social tactic as possible predictors in our test. Proportion of courtship by NT-males did not predict their proportion of paternity in either habitat type. Courtship by T-males was a strong predictor of paternity in simple habitats but not complex habitats. Our findings support the hypothesis that courtship is a more accurate predictor of T-male mating success in simple habitats, which is consistent with previous findings suggesting that reduced area and topographical heterogeneity, especially the absence of subsurface crevices in simpler habitats, makes it more economical for T-males to prevent surreptitious mating by NT-males. Our study, therefore, highlights the importance of considering possible effects of alternative social tactics and variation in environmental conditions when testing the accuracy of behaviorally based estimates of breeding relationships, especially in polygamous species with multiple paternity.
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