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Genetic Adaptations in Mudskipper and Tetrapod Give Insights into Their Convergent Water-to-Land Transition.

ABSTRACT: Water-to-land transition has been independently evolved in multiple vertebrate lineages including the most recent common ancestor of tetrapod and multiple fish clades, and among them, mudskippers uniquely adapted to the mudflat. Even though physiological and morphological adaptation of mudskippers is thought to resemble that of the ancestral tetrapod, it is unclear if they share genome-wide evolutionary signatures. To detect potential signatures of positive selection in mudskipper and tetrapods, we analyzed 4118 singleton orthologues of terrestrial tetrapods, coelacanth, mudskipper, and fully aquatic fishes. Among positively selected genes identified in mudskipper and tetrapod lineages, genes involved in immune responses, mitochondrial oxidative phosphorylation, and kidney development were detected. On the other hand, tetrapod-specific and mudskipper-specific positively selected genes were functionally enriched for DNA repair processes, which could be associated with higher exposure to UV light. We also performed gene family analysis and discovered convergent contraction of eight gene families, including ??-crystallin coding genes in both tetrapod and mudskipper lineages. Findings of this study suggest the similar genetic adaptation against environmental constraints between the ancient tetrapod and mudskippers for their land adaptation.

SUBMITTER: Kim J

PROVIDER: S-EPMC7926366 | biostudies-literature | 2021 Feb

REPOSITORIES: biostudies-literature

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Genetic Adaptations in Mudskipper and Tetrapod Give Insights into Their Convergent Water-to-Land Transition.

Kim Juwan J Lee Chul C Yoo DongAhn D Kim Heebal H

Animals : an open access journal from MDPI 20210223 2

Water-to-land transition has been independently evolved in multiple vertebrate lineages including the most recent common ancestor of tetrapod and multiple fish clades, and among them, mudskippers uniquely adapted to the mudflat. Even though physiological and morphological adaptation of mudskippers is thought to resemble that of the ancestral tetrapod, it is unclear if they share genome-wide evolutionary signatures. To detect potential signatures of positive selection in mudskipper and tetrapods, ...[more]

PMID: 33672418

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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.

Dataset Information

Genetic Adaptations in Mudskipper and Tetrapod Give Insights into Their Convergent Water-to-Land Transition.

Publications

Genetic Adaptations in Mudskipper and Tetrapod Give Insights into Their Convergent Water-to-Land Transition.

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