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Abstract Noncoding microRNAs tend to evolve within introns of coding genes that provide them with transcriptional opportunity. As an outcome of natural selection, the intragenic position of microRNAs is crucial for their expression, evolution, and functional cooperation with the host gene. Therefore, understanding the evolution of intragenic microRNA structures may bring novel insights into genetic and phenotypic evolution. However, it remains largely unexplored. Here, by analyzing microRNA genomics in 34 metazoan species, we found that the majority (630/1,154) of microRNA families originated from introns of coding genes that provided them with initial transcriptional capacity. The most rapid expansion of intragenic microRNAs happened at the advent of vertebrates when 21 microRNA families emerged from introns of neural genes and reorganized the gene regulatory network, leading to the rise of vertebrate-specific neural crest cells, which transformed the invertebrate head and enabled the ecological shift from filter feeding to active predation. Intragenic microRNAs gradually gain independence from their host genes, which is accelerated by whole-genome duplications. After a whole-genome duplication, the purging of redundant host genes often set an orphaned microRNA “free” to diversify with the transcriptional elements inherited from the host. Whole-genome duplications facilitated a dramatic microRNA diversification during the initial divergence of vertebrates, as the intragenic status of 12 neural crest-regulating microRNAs was retained in jawed vertebrates but was lost in jawless cyclostomes, which diverged their neural crest development. We propose that coding genes not only facilitate the origination of new microRNAs, but also “sacrifice” themselves to help microRNA diversification. Graphical abstract Graphical Abstract

The assembly of the gnathostome bodyplan constitutes a formative episode in vertebrate evolutionary history, an interval in which the mineralized skeleton and its canonical suite of cell and tissue types originated. Fossil jawless fishes, assigned to the gnathostome stem-lineage, provide an unparalleled insight into the origin and evolution of the skeleton, hindered only by uncertainty over the phylogenetic position and evolutionary significance of key clades. Chief among these are the jawless anaspids, whose skeletal composition, a rich source of phylogenetic information, is poorly characterized. Here we survey the histology of representatives spanning anaspid diversity and infer their generalized skeletal architecture. The anaspid dermal skeleton is composed of odontodes comprising spheritic dentine and enameloid, overlying a basal layer of acellular parallel fibre bone containing an extensive shallow canal network. A recoded and revised phylogenetic analysis using equal and implied weights parsimony resolves anaspids as monophyletic, nested among stem-gnathostomes. Our results suggest the anaspid dermal skeleton is a degenerate derivative of a histologically more complex ancestral vertebrate skeleton, rather than reflecting primitive simplicity. Hypotheses that anaspids are ancestral skeletonizing lampreys, or a derived lineage of jawless vertebrates with paired fins, are rejected.

Anatomical knowledge of early chondrichthyans and estimates of their phylogeny are improving, but many taxa are still known only from microremains. The nearly cosmopolitan and regionally abundant Devonian genus Phoebodus has long been known solely from isolated teeth and fin spines. Here, we report the first skeletal remains of Phoebodus from the Famennian (Late Devonian) of the Maïder region of Morocco, revealing an anguilliform body, specialized braincase, hyoid arch, elongate jaws and rostrum, complementing its characteristic dentition and ctenacanth fin spines preceding both dorsal fins. Several of these features corroborate a likely close relationship with the Carboniferous species Thrinacodus gracia, and phylogenetic analysis places both taxa securely as members of the elasmobranch stem lineage. Identified as such, phoebodont teeth provide a plausible marker for range extension of the elasmobranchs into the Middle Devonian, thus providing a new minimum date for the origin of the chondrichthyan crown-group. Among pre-Carboniferous jawed vertebrates, the anguilliform body shape of Phoebodus is unprecedented, and its specialized anatomy is, in several respects, most easily compared with the modern frilled shark Chlamydoselachus. These results add greatly to the morphological, and by implication ecological, disparity of the earliest elasmobranchs.

The Devonian marks a critical stage in the early evolution of vertebrates: It opens with an unprecedented diversity of fishes and closes with the earliest evidence of limbed tetrapods. However, the latter part of the Devonian has also been characterized as a period of global biotic crisis marked by two large extinction pulses: a \"Big Five\" mass extinction event at the Frasnian-Famennian stage boundary (374 Ma) and the less well-documented Hangenberg event some 15 million years later at the Devonian-Carboniferous boundary (359 Ma). Here, we report the results of a wide-ranging analysis of the impact of these events on early vertebrate evolution, which was obtained from a database of vertebrate occurrences sampling over 1,250 taxa from 66 localities spanning Givetian to Serpukhovian stages (391 to 318 Ma). We show that major vertebrate clades suffered acute and systematic effects centered on the Hangenberg extinction involving long-term losses of over 50% of diversity and the restructuring of vertebrate ecosystems worldwide. Marine and nonmarine faunas were equally affected, precluding the existence of environmental refugia. The subsequent recovery of previously diverse groups (including placoderms, sarcopterygian fish, and acanthodians) was minimal. Tetrapods, actinopterygians, and chondrichthyans, all scarce within the Devonian, undergo large diversification events in the aftermath of the extinction, dominating all subsequent faunas. The Hangenberg event represents a previously unrecognized bottleneck in the evolutionary history of vertebrates as a whole and a historical contingency that shaped the roots of modern biodiversity.

Chondrichthyes (cartilaginous fishes) are fundamental for understanding vertebrate evolution, yet their genomes are understudied. We report long-read sequencing of the whale shark genome to generate the best gapless chondrichthyan genome assembly yet with higher contig contiguity than all other cartilaginous fish genomes, and studied vertebrate genomic evolution of ancestral gene families, immunity, and gigantism. We found a major increase in gene families at the origin of gnathostomes (jawed vertebrates) independent of their genome duplication. We studied vertebrate pathogen recognition receptors (PRRs), which are key in initiating innate immune defense, and found diverse patterns of gene family evolution, demonstrating that adaptive immunity in gnathostomes did not fully displace germline-encoded PRR innovation. We also discovered a new toll-like receptor (TLR29) and three NOD1 copies in the whale shark. We found chondrichthyan and giant vertebrate genomes had decreased substitution rates compared to other vertebrates, but gene family expansion rates varied among vertebrate giants, suggesting substitution and expansion rates of gene families are decoupled in vertebrate genomes. Finally, we found gene families that shifted in expansion rate in vertebrate giants were enriched for human cancer-related genes, consistent with gigantism requiring adaptations to suppress cancer.

This study establishes the origin and evolutionary history of the synuclein genes. A combination of phylogenetic analyses of the synucleins from twenty-two model species, characterization of local synteny similarities among humans, sharks and lampreys, and statistical comparisons among lamprey and human chromosomes, provides conclusive evidence for the current diversity of synuclein genes arising from the whole-genome duplications (WGDs) that occurred in vertebrates. An ancestral synuclein gene was duplicated in a first WGD, predating the diversification of all living vertebrates. The two resulting genes are still present in agnathan vertebrates. The second WGD, specific to the gnathostome lineage, led to the emergence of the three classical synuclein genes, SNCA, SNCB and SNCG, which are present in all jawed vertebrate lineages. Additional WGDs have added new genes in both agnathans and gnathostomes, while some gene losses have occurred in particular species. The emergence of synucleins through WGDs prevented these genes from experiencing dosage effects, thus avoiding the potential detrimental effects associated with individual duplications of genes that encode proteins prone to aggregation. Additional insights into the structural and functional features of synucleins are gained through the analysis of the highly divergent synuclein proteins present in chondrichthyans and agnathans.

Jaws are a key vertebrate feature that arose early in our evolution. Placoderms are among the first jawed vertebrates; their fossils yield essential knowledge about the early diversification of gnathostome feeding strategies, diets and modularity. Modularity can be expressed through disproportional lengths of lower and upper jaws as in swordfish or halfbeaks. Alienacanthus malkowskii is an arthrodire from the Famennian of Morocco and Poland, whose most remarkable feature is its lower jaw, which is twice as long as the skull. This is the oldest record of such extreme jaw elongation and modularity in vertebrates. The gnathal plates of Alienacanthus possess sharp, posteriorly recurved teeth that continue anterior of the occlusion in the inferognathals. The dentition suggests a catching and trapping live prey function, and the jaw occlusion is unique among placoderms. This armoured ‘fish’ expands the morphological and ecological diversity during one of the first radiations of jawed vertebrates with a combination of features so far unrecorded for arthrodires.

Although relationships among the major groups of living gnathostomes are well established, the relatedness of early jawed vertebrates to modern clades is intensely debated. Here, we provide a new description of Gladbachus, a Middle Devonian (Givetian approx. 385-million-year-old) stem chondrichthyan from Germany, and one of the very few early chondrichthyans in which substantial portions of the endoskeleton are preserved. Tomographic and histological techniques reveal new details of the gill skeleton, hyoid arch and jaws, neurocranium, cartilage, scales and teeth. Despite many features resembling placoderm or osteichthyan conditions, phylogenetic analysis confirms Gladbachus as a stem chondrichthyan and corroborates hypotheses that all acanthodians are stem chondrichthyans. The unfamiliar character combination displayed by Gladbachus, alongside conditions observed in acanthodians, implies that pre-Devonian stem chondrichthyans are severely under-sampled and strongly supports indications from isolated scales that the gnathostome crown group originated at the latest by the early Silurian (approx. 440 Ma). Moreover, phylogenetic results highlight the likely convergent evolution of conventional chondrichthyan conditions among earliest members of this primary gnathostome division, while skeletal morphology points towards the likely suspension feeding habits of Gladbachus, suggesting a functional origin of the gill slit condition characteristic of the vast majority of living and fossil chondrichthyans.

Solving the evolutionary relationships of the acanthodians is one of the key problems in reconstructing ancestral anatomical conditions for the jawed vertebrates (gnathostomes). Current debate concerns whether acanthodians are an assemblage of stem chondrichthyans, or a more generalized grade encompassing some early stem osteichthyans. The skull anatomy of Acanthodes bronni has been pivotal in these debates, owing to tension between chondrichthyan- and osteichthyan-like models of reconstruction. We use computed tomography scanning and traditional palaeontological techniques to resolve the long-standing debate about the anatomy of the jaw suspension. We establish the correct length of the hyomandibula and show that it attaches to a process on the ventrolateral angle of the braincase below the jugular vein groove. This condition corresponds precisely to that in chondrichthyans. This character represents an unambiguously optimized synapomorphy with chondrichthyans given current gnathostome phylogenies, corroborating the growing consensus of the chondrichthyan affinity of acanthodians.

Osteostraci and Galeaspida are stem-gnathostomes, occupying a key phylogenetic position for resolving the nature of the jawless ancestor from which jawed vertebrates evolved more than 400 million years ago. Both groups are characterized by the presence of rigid headshields that share a number of common morphological traits, in some cases hindering the resolution of their interrelationships and the exact nature of their affinities with jawed vertebrates. Here, we explore the morphological and functional diversity of osteostracan and galeaspid headshields using geometric morphometrics and computational fluid dynamics to constrain the factors that promoted the evolution of their similar morphologies and informing on the ecological scenario under which jawed vertebrates emerged. Phylomorphospace, Mantel analysis and Stayton metrics demonstrate a high degree of homoplasy. Computational fluid dynamics reveals similar hydrodynamic performance among morphologically convergent species, indicating the independent acquisition of the same morphofunctional traits and, potentially, equivalent lifestyles. These results confirm that a number of the characters typically used to infer the evolutionary relationships among galeaspids, osteostracans and jawed vertebrates are convergent in nature, potentially obscuring understanding of the assembly of the gnathostome bodyplan. Ultimately, our results reveal that while the jawless relatives of the earliest jawed vertebrates were ecologically diverse, widespread convergence on the same hydrodynamic adaptations suggests they had reached the limits of their potential ecological diversity—overcome by jawed vertebrates and their later innovations.