The bowfin genome illuminates the developmental evolution of ray-finned fishes

The bowfin (Amia calva) is a ray-finned fish that possesses a unique suite of ancestral and derived phenotypes, which are key to understanding vertebrate evolution. The phylogenetic position of bowfin as a representative of neopterygian fishes, its archetypical body plan and its unduplicated and slowly evolving genome make bowfin a central species for the genomic exploration of ray-finned fishes. Here we present a chromosome-level genome assembly for bowfin that enables gene-order analyses, settling long-debated neopterygian phylogenetic relationships. We examine chromatin accessibility and gene expression through bowfin development to investigate the evolution of immune, scale, respiratory and fin skeletal systems and identify hundreds of gene-regulatory loci conserved across vertebrates. These resources connect developmental evolution among bony fishes, further highlighting the bowfin’s importance for illuminating vertebrate biology and diversity in the genomic era.

The genome of the bowfin (Amia calva) illuminates the developmental evolution of ray-finned fishes

The bowfin fish (Amia calva) diverged before the genome duplication in teleost fishes, and its archetypical body plan and slow rate of molecular evolution make it a key species for genomic exploration as a basal representative of the neopterygian fishes. To investigate the evolution and development of ray-finned fishes, we generated a chromosome-level genome assembly for bowfin that enables gene-order analyses which settle its long-debated, phylogenetic relationship with gars. We analyze the genomic underpinnings of the bowfin’s unique combination of derived and ancestral phenotypes involving the immune system as well as scale, respiratory organ, and skeletal development. By detailing chromatin accessibility and gene expression through bowfin development, we connect developmental gene regulatory loci across vertebrates. We illustrate the utility of these genomic resources to connect developmental evolution across bony fishes, showing the importance of bowfin in understanding vertebrate biology and diversity.

Comparative Analysis of the Organization of the Catecholaminergic Systems in the Brain of Holostean Fishes (Actinopterygii/Neopterygii)

Living holosteans, comprising 8 species of bowfins and gars, form a small monophyletic group of actinopterygian fishes, which are currently considered as the sister group to the enormously numerous teleosts and have largely been neglected in neuroanatomical studies. We have studied the catecholaminergic (CAergic) systems by means of antibodies against tyrosine hydroxylase (TH) and dopamine (DA) in the brain of representative species of the 3 genera included in the 2 orders of holostean fishes: Amia calva (Amiiformes) and Lepisosteus platyrhincus, Lepisosteus oculatus, and Atractosteus spatula (Lepisosteiformes). Different groups of TH/DA-immunoreactive (ir) cells were observed in the olfactory bulb, subpallium, and preoptic area of the telencephalon. Hypothalamic groups were labeled in the suprachiasmatic nucleus, tuberal (only in A. calva), retrotuberal, and retromamillary areas; specifically, the paraventricular organ showed only DA immunoreactivity. In the diencephalon, TH/DA-ir groups were detected in the prethalamus, posterior tubercle, and pretectum. In the caudal hindbrain, the solitary tract nucleus and area postrema presented TH/DA-ir cell groups, and also the spinal cord and the retina. Only in A. calva, particular CAergic cell groups were observed in the habenula, the mesencephalic tegmentum, and in the locus coeruleus. Following a neuromeric analysis, the comparison of these results with those obtained in other classes of fishes and tetrapods shows many common traits of CAergic systems shared by most vertebrates and in addition highlights unique features of actinopterygian fishes.

Organization of the Orexin/Hypocretin System in the Brain of Holostean Fishes: Assessment of Possible Relationships with Monoamines and Neuropeptide Y

Holosteans form a small group of actinopterygian fishes considered the sister group of teleosts. Despite this proximity to the biggest group of vertebrates, relatively few studies have been conducted to investigate the organization of the central nervous system of this group of fishes. In this study, the neuroanatomical distribution of orexin/hypocretin-like immunoreactive (OX-ir) cell bodies and fibers was analyzed in the brain of 3 representative species of the 2 orders of extant holosteans, the spotted gar Lepisosteus oculatus, the Florida gar Lepisosteus platyrhincus, and the bowfin Amia calva. Antibodies against orexin-A (OXA) and orexin-B (OXB) were used, which labeled the same cells and fibers throughout the brain. In addition, double immunohistofluorescence was performed for the simultaneous detection of OXA and OXB with tyrosine hydroxylase, serotonin, and neuropeptide Y (NPY), in an attempt to localize the orexinergic structures precisely and study the possible interactions between these neuroactive substances. The pattern of distribution of OX-ir cells in the 3 species was largely similar, showing labeled cells in the preoptic area (POA), and the tuberal and retrotuberal hypothalamic regions, with only subtle differences between species in the density of labeled cells. OX-ir fibers were found in all main brain subdivisions of the 3 species, mostly in the ventral subpallial areas, POA, hypothalamus, posterior tubercle, thalamus, and mesencephalic tectum. Different densities of orexinergic fibers were observed in relation to catecholaminergic and serotoninergic cell groups, as well as an absence of colocalization between orexins and NPY in the same hypothalamic neurons. The comparison of these results with those obtained in other vertebrates highlights a constant pattern of distribution of this system of neurotransmission among different groups of actinopterygian fishes, especially in teleosts. Conserved features shared by all vertebrates studied were also observed, such as the presence of OX-ir cells in the basal hypothalamus, reflecting the preserved functions of these neuropeptides over the course of evolution.

The oldest ionoscopiform from China sheds new light on the early evolution of halecomorph fishes

The Halecomorphi are a major subdivision of the ray-finned fishes. Although living halecomorphs are represented solely by the freshwater bowfin, Amia calva , this clade has a rich fossil history, and the resolution of interrelationships among extinct members is central to the problem of understanding the origin of the Teleostei, the largest clade of extant vertebrates. The Ionoscopiformes are extinct marine halecomorphs that were inferred to have originated in the Late Jurassic of Europe, and subsequently dispersed to the Early Cretaceous of the New World. Here, we report the discovery of a new ionoscopiform, Robustichthys luopingensis gen. et sp. nov., based on eight well-preserved specimens from the Anisian (242–247 Ma), Middle Triassic marine deposits of Luoping, eastern Yunnan Province, China. The new species documents the oldest known ionoscopiform, extending the stratigraphic range of this group by approximately 90 Ma, and the geographical distribution of this group into the Middle Triassic of South China, a part of eastern Palaeotethys Ocean. These new data provide a minimum estimate for the split of Ionoscopiformes from its sister clade Amiiformes and shed new light on the origin of ionoscopiform fishes.