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Giant lungfish genome elucidates the conquest of land by vertebrates.

ABSTRACT: Lungfishes belong to lobe-fined fish (Sarcopterygii) that, in the Devonian period, 'conquered' the land and ultimately gave rise to all land vertebrates, including humans^1-3. Here we determine the chromosome-quality genome of the Australian lungfish (Neoceratodus forsteri), which is known to have the largest genome of any animal. The vast size of this genome, which is about 14× larger than that of humans, is attributable mostly to huge intergenic regions and introns with high repeat content (around 90%), the components of which resemble those of tetrapods (comprising mainly long interspersed nuclear elements) more than they do those of ray-finned fish. The lungfish genome continues to expand independently (its transposable elements are still active), through mechanisms different to those of the enormous genomes of salamanders. The 17 fully assembled lungfish macrochromosomes maintain synteny to other vertebrate chromosomes, and all microchromosomes maintain conserved ancient homology with the ancestral vertebrate karyotype. Our phylogenomic analyses confirm previous reports that lungfish occupy a key evolutionary position as the closest living relatives to tetrapods^4,5, underscoring the importance of lungfish for understanding innovations associated with terrestrialization. Lungfish preadaptations to living on land include the gain of limb-like expression in developmental genes such as hoxc13 and sall1 in their lobed fins. Increased rates of evolution and the duplication of genes associated with obligate air-breathing, such as lung surfactants and the expansion of odorant receptor gene families (which encode proteins involved in detecting airborne odours), contribute to the tetrapod-like biology of lungfishes. These findings advance our understanding of this major transition during vertebrate evolution.

SUBMITTER: Meyer A

PROVIDER: S-EPMC7875771 | biostudies-literature | 2021 Feb

REPOSITORIES: biostudies-literature

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Giant lungfish genome elucidates the conquest of land by vertebrates.

Meyer Axel A Schloissnig Siegfried S Franchini Paolo P Du Kang K Woltering Joost M JM Irisarri Iker I Wong Wai Yee WY Nowoshilow Sergej S Kneitz Susanne S Kawaguchi Akane A Fabrizius Andrej A Xiong Peiwen P Dechaud Corentin C Spaink Herman P HP Volff Jean-Nicolas JN Simakov Oleg O Burmester Thorsten T Tanaka Elly M EM Schartl Manfred M

Nature 20210118 7845

Lungfishes belong to lobe-fined fish (Sarcopterygii) that, in the Devonian period, 'conquered' the land and ultimately gave rise to all land vertebrates, including humans<sup>1-3</sup>. Here we determine the chromosome-quality genome of the Australian lungfish (Neoceratodus forsteri), which is known to have the largest genome of any animal. The vast size of this genome, which is about 14× larger than that of humans, is attributable mostly to huge intergenic regions and introns with high repeat c ...[more]

PMID: 33461212

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Project description:A crucial evolutionary change in vertebrate history was the Palaeozoic (Devonian 419–359 million years ago) water-to-land transition, allowed by key morphological and physiological modifications including the acquisition of lungs. Nonetheless, the origin and early evolution of vertebrate lungs remain highly controversial, particularly whether the ancestral state was paired or unpaired. Due to the rarity of fossil soft tissue preservation, lung evolution can only be traced based on the extant phylogenetic bracket. Here we investigate, for the first time, lung morphology in extensive developmental series of key living lunged osteichthyans using synchrotron x-ray microtomography and histology. Our results shed light on the primitive state of vertebrate lungs as unpaired, evolving to be truly paired in the lineage towards the tetrapods. The water-to-land transition confronted profound physiological challenges and paired lungs were decisive for increasing the surface area and the pulmonary compliance and volume, especially during the air-breathing on land. eLife digest All life on Earth started out under water. However, around 400 million years ago some vertebrates, such as fish, started developing limbs and other characteristics that allowed them to explore life on land. One of the most pivotal features to evolve was the lungs, which gave vertebrates the ability to breathe above water. Most land-living vertebrates, including humans, have two lungs which sit on either side of their chest. The lungs extract oxygen from the atmosphere and transfer it to the bloodstream in exchange for carbon dioxide which then gets exhaled out in to the atmosphere. How this important organ first evolved is a hotly debated topic. This is largely because lung tissue does not preserve well in fossils, making it difficult to trace how the lungs of vertebrates changed over the course of evolution. To overcome this barrier, Cupello et al. compared the lungs of living species which are crucial to understand the early stages of the water-to-land transition. This included four species of lunged bony fish which breathe air at the water surface, and a four-legged salamander that lives on land. Cupello et al. used a range of techniques to examine how the lungs of the bony fish and salamander changed shape during development. The results suggested that the lungs of vertebrates started out as a single organ, which became truly paired later in evolution once vertebrates started developing limbs. This anatomical shift increased the surface area available for exchanging oxygen and carbon dioxide so that vertebrates could breathe more easily on land. These findings provide new insights in to how the lung evolved into the paired structure found in most vertebrates alive today. It likely that this transition allowed vertebrates to fully adapt to breathing above water, which may explain why this event only happened once over the course of evolution.

Project description:Like other diapsids, Tyrannosaurus rex has two openings in the temporal skull region. In addition, like in other dinosaurs, its snout and lower jaw show large cranial fenestrae. In T. rex, they are thought to decrease skull weight, because, unlike most other amniotes, the skull proportion is immense compared to the body. Understanding morphofunctional complexity of this impressive skull architecture requires a broad scale phylogenetic comparison with skull types different to that of dinosaurs with fundamentally diverging cranial regionalization. Extant fully terrestrial vertebrates (amniotes) provide the best opportunities in that regard, as their skull performance is known from life. We apply for the first time anatomical network analysis to study skull bone integration and modular constructions in tyrannosaur and compare it with five representatives of the major amniote groups in order to get an understanding of the general patterns of amniote skull modularity. Our results reveal that the tyrannosaur has the most modular skull organization among the amniotes included in our study, with an unexpected separation of the snout in upper and lower sub-modules and the presence of a lower adductor chamber module. Independent pathways of bone reduction in opossum and chicken resulted in different degrees of cranial complexity with chicken having a typical sauropsidian pattern. The akinetic skull of opossum, alligator, and leatherback turtle evolved in independent ways mirrored in different patterns of skull modularity. Kinetic forms also show great diversity in modularity. The complex tyrannosaur skull modularity likely represents a refined mosaic of phylogenetic and ecological factors with food processing being probably most important for shaping its skull architecture. Mode of food processing primarily shaped skull integration among amniotes, however, phylogenetic patterns of skull integration are low in our sampling. Our general conclusions on amniote skull integrity are obviously preliminary and should be tested in subsequent studies. As such, this study provides a framework for future research focusing on the evolution of modularity on lower taxonomic levels.

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Giant lungfish genome elucidates the conquest of land by vertebrates.

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Giant lungfish genome elucidates the conquest of land by vertebrates.

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