The neural bases of vertebrate motor behaviour through the lens of evolution

The primary driver of the evolution of the vertebrate nervous system has been the necessity to move, along with the requirement of controlling the plethora of motor behavioural repertoires seen among the vast and diverse vertebrate species. Understanding the neural basis of motor control through the perspective of evolution, mandates thorough examinations of the nervous systems of species in critical phylogenetic positions. We present here, a broad review of studies on the neural motor infrastructure of the lamprey, a basal and ancient vertebrate, which enjoys a unique phylogenetic position as being an extant representative of the earliest group of vertebrates. From the central pattern generators in the spinal cord to the microcircuits of the pallial cortex, work on the lamprey brain over the years, has provided detailed insights into the basic organization (a bauplan ) of the ancestral vertebrate brain, and narrates a compelling account of common ancestry of fundamental aspects of the neural bases for motion control, maintained through half a billion years of vertebrate evolution. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.

Genomic Analysis of Hypoxia Inducible Factor Alpha Evolution in Ray-finned Fishes (Actinopterygii)

Two rounds of genome duplication (GD) in the ancestor of vertebrates, followed by additional GD during the evolution of ray-finned fishes (Actinopterygii), expanded certain gene families, including those encoding the hypoxia inducible transcription factor (HIF). The present study analyzed Actinopterygian genomes for duplicates of HIFα, the subunit that confers oxygen-dependent gene regulation. In contrast to tetrapod vertebrates that retain three HIFα genes from the ancestral vertebrate GD, four HIFα forms were found in the genomes of primitive Actinopterygians (spotted gar and Asian arowana). All four forms have been retained in zebrafish and related species (Otocephala) and salmonids and their sister taxa (northern pike) but one of them (HIF4α) was lost during the evolution of more derived fishes (Neoteleostei). In addition, the current analyses confirm that Otocephala retain duplicates of HIF1α and HIF2α from the teleost-specific GD, provide new evidence of salmonid-specific duplicates of HIF1α, HIF2α, and HIF3α, and reveal a broad distribution of a truncated form of HIF2α in salmonids and Neoteleostei. This study delivers a comprehensive view of HIFα evolution in the ray-finned fishes, highlights the need for a consistent nomenclature, and suggests avenues for future research on this critical transcription factor.

Tumor Necrosis Factor Superfamily: Ancestral Functions and Remodeling in Early Vertebrate Evolution

The evolution of the tumor necrosis factor superfamily (TNFSF) in early vertebrates is inferred by comparing the TNFSF genes found in humans and nine fishes: three agnathans, two chondrichthyans, three actinopterygians, and the sarcopterygian Latimeria chalumnae. By combining phylogenetic and synteny analyses, the TNFSF sequences detected are classified into five clusters of genes and 24 orthology groups. A model for their evolution since the origin of vertebrates is proposed. Fifteen TNFSF genes emerged from just three progenitors due to the whole-genome duplications (WGDs) that occurred before the agnathan/gnathostome split. Later, gnathostomes not only kept most of the genes emerged in the WGDs but soon added several tandem duplicates. More recently, complex, lineage-specific patterns of duplications and losses occurred in different gnathostome lineages. In agnathan species only seven to eight TNFSF genes are detected, because this lineage soon lost six of the genes emerged in the ancestral WGDs and additional losses in both hagfishes and lampreys later occurred. The orthologs of many of these lost genes are, in mammals, ligands of death-domain-containing TNFSF receptors, indicating that the extrinsic apoptotic pathway became simplified in the agnathan lineage. From the patterns of emergence of these genes, it is deduced that both the regulation of apoptosis and the control of the NF-κB pathway that depends in modern mammals on TNFSF members emerged before the ancestral vertebrate WGDs.

Fgf-driven Tbx protein activities directly induce myf5 and myod to initiate zebrafish myogenesis

Skeletal muscle derives from dorsal mesoderm that is formed during vertebrate gastrulation. Fibroblast growth factor (Fgf) signalling is known to cooperate with transcription factors of the Tbx family to promote dorsal mesoderm formation, but the role of these proteins in skeletal myogenesis has been unclear. Using the zebrafish, we show that dorsally-derived Fgf signals act through Tbx16 and Tbxta to induce two populations of slow and fast trunk muscle precursors at distinct dorsoventral positions. Tbx16 binds to and directly activates the myf5 and myod genes that are required for commitment to skeletal myogenesis. Tbx16 activity depends on Fgf signalling from the organiser. In contrast, Tbxta is not required for myf5 expression. However, Tbxta binds to a specific site upstream of myod not bound by Tbx16, driving myod expression in the adaxial slow precursors dependent upon Fgf signals, thereby initiating muscle differentiation in the trunk. After gastrulation, when similar muscle cell populations in the post-anal tail are generated from the tailbud, declining Fgf signalling is less effective at initiating adaxial myogenesis, which is instead initiated by Hedgehog signalling from the notochord. Our findings provide insight into the ancestral vertebrate trunk myogenic pattern and how it was co-opted during tail evolution to generate similar muscle by new mechanisms.

Phylogenetic Reclassification of Vertebrate Melatonin Receptors To Include Mel1d

The circadian and seasonal actions of melatonin are mediated by high affinity G-protein coupled receptors (melatonin receptors, MTRs), classified into phylogenetically distinct subtypes based on sequence divergence and pharmacological characteristics. Three vertebrate MTR subtypes are currently described: MT1 (MTNR1A), MT2 (MTNR1B), and Mel1c (MTNR1C / GPR50), which exhibit distinct affinities, tissue distributions and signaling properties. We present phylogenetic and comparative genomic analyses supporting a revised classification of the vertebrate MTR family. We demonstrate four ancestral vertebrate MTRs, including a novel molecule hereafter named Mel1d. We reconstructed the evolution of each vertebrate MTR, detailing genetic losses in addition to gains resulting from whole genome duplication events in teleost fishes. We show that Mel1d was lost separately in mammals and birds and has been previously mistaken for an MT1 paralogue. The genetic and functional diversity of vertebrate MTRs is more complex than appreciated, with implications for our understanding of melatonin actions in different taxa. The significance of our findings, including the existence of Mel1d, are discussed in an evolutionary and functional context accommodating a robust phylogenetic assignment of MTR gene family structure.

Phylogenetic reclassification of vertebrate melatonin receptors to include Mel1d

ABSTRACTThe circadian and seasonal actions of melatonin are mediated by high affinity G-protein coupled receptors (melatonin receptors, MTRs), classified into phylogenetically distinct subtypes based on sequence divergence and pharmacological characteristics. Three vertebrate MTR subtypes are currently described: MT1 (MTNR1A), MT2 (MTNR1B), and Mel1c (MTNR1C / GPR50), which exhibit distinct affinities, tissue distributions and signaling properties. We present phylogenetic and comparative genomic analyses supporting a revised classification of the vertebrate MTR family. We demonstrate four ancestral vertebrate MTRs, including a novel molecule hereafter named Mel1d. We reconstructed the evolution of each vertebrate MTR, detailing genetic losses in addition to gains resulting from whole genome duplication events in teleost fishes. We show that Mel1d was lost separately in mammals and birds and has been previously mistaken for an MT1 paralogue. The genetic and functional diversity of vertebrate MTRs is more complex than appreciated, with implications for our understanding of melatonin actions in different taxa. The significance of our findings, including the existence of Mel1d, are discussed in an evolutionary and functional context accommodating a robust phylogenetic assignment of MTR gene family structure.

An atlas of anteriorhoxgene expression in the embryonic sea lamprey head:hox-code evolution in vertebrates

In the hindbrain and the adjacent cranial neural crest (NC) cells of jawed vertebrates (gnathostomes), nested and segmentally-restricted domains ofHoxgene expression provide a combinatorialHox-code for specifying regional properties during head development. Extant jawless vertebrates, such as the sea lamprey(Petromyzon marinus),can provide insights into the evolution and diversification of thisHox-code in vertebrates. There is evidence for gnathostome-like spatial patterns ofHoxexpression in lamprey; however, the expression domains of the majority of lampreyhoxgenes from paralogy groups (PG) 1-4 are yet to be characterized, so it is unknown whether they are coupled to hindbrain segments (rhombomeres) and NC. In this study, we systematically describe the spatiotemporal expression of all 14 sea lampreyhoxgenes from PG1-PG4 in the developing hindbrain and pharynx to investigate the extent to which their expression conforms to the archetypal gnathostome hindbrain and pharyngealhox-codes. We find many similarities inHoxexpression between lamprey and gnathostome species, particularly in rhombomeric domains during hindbrain segmentation and in the cranial neural crest, enabling inference of aspects ofHoxexpression in the ancestral vertebrate embryonic head. These data are consistent with the idea that aHoxregulatory network underlying hindbrain segmentation is a pan vertebrate trait. We also reveal differences in hindbrain domains at later stages, as well as expression in the endostyle and in pharyngeal arch (PA) 1 mesoderm. Our analysis suggests that manyHoxexpression domains that are observed in extant gnathostomes were present in ancestral vertebrates but have been partitioned differently acrossHoxclusters in gnathostome and cyclostome lineages after duplication.

The nearshore cradle of early vertebrate diversification

Ancestral vertebrate habitats are subject to controversy and obscured by limited, often contradictory paleontological data. We assembled fossil vertebrate occurrence and habitat datasets spanning the middle Paleozoic (480 million to 360 million years ago) and found that early vertebrate clades, both jawed and jawless, originated in restricted, shallow intertidal-subtidal environments. Nearshore divergences gave rise to body plans with different dispersal abilities: Robust fishes shifted shoreward, whereas gracile groups moved seaward. Fresh waters were invaded repeatedly, but movement to deeper waters was contingent upon form and short-lived until the later Devonian. Our results contrast with the onshore-offshore trends, reef-centered diversification, and mid-shelf clustering observed for benthic invertebrates. Nearshore origins for vertebrates may be linked to the demands of their mobility and may have influenced the structure of their early fossil record and diversification.