Abstract
Simple SummaryMudskippers are amphibious fish that spend most of their lives on mudflats. The morphological and physiological adaptations of mudskippers resemble water-to-land transition of ancient tetrapod, yet comparative studies on the genetic backgrounds underlying the adaptation are still limited. The aim of this study is to compare genome-wide signatures of positive selection and gene family evolution between mudskipper and tetrapods. Here, we performed comparative genomics analysis between terrestrial tetrapods, coelacanth, mudskipper, and aquatic fish species. As a result, we discovered genes with selective signature in tetrapod and mudskipper lineages associated with immune responses, mitochondrial oxidative phosphorylation, kidney development, and DNA repair processes. In both tetrapod and mudskipper linages, we found convergent contraction of the gene family encoding βγ-crystallins that are found in the lens of vertebrate eye and involved in the refraction of the light. Our results present similar genetic adaptations in mudskipper and tetrapod lineages, which independently adapted to land environment.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 βγ-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.
Highlights
Water-to-land transition refers to the macro-evolution of aquatic organisms adapting to the terrestrial environment, supported by multiple pieces of evidence, including the emergence of our well-known ancestor-like species, Tiktaalik, in the Late DevonianEpoch [1]
We regarded a gene as candidates for terrestrial adaptation on the both lineages if the gene is detected in tetrapodand-mudskipper model or detected in both tetrapod and mudskipper model
We detected the amino acid substitutions in land-adapting lineages with the signature of positive selection in NOD1, Adenylate Cyclase 7 gene (ADCY7), NOA1, Laminin subunit beta-2 gene (LAMB2), and Kynurenine 3-mono-oxygenase (KMO) that are involved in immune responses, regulation of mitochondrial oxidative phosphorylation, and development of the kidney
Summary
Water-to-land transition refers to the macro-evolution of aquatic organisms adapting to the terrestrial environment, supported by multiple pieces of evidence, including the emergence of our well-known ancestor-like species, Tiktaalik, in the Late DevonianEpoch [1]. Even though land adaptation of ancient tetrapods, so called vertebrate land invasion, is one of the most famous and well-studied examples of water-to-land transition, it is thought that transition from aquatic to terrestrial environments has evolved in multiple lineages independently including turtles [2] and other invertebrates such as snails and arthopods [3]. Mudskippers including Periophthalmus magnuspinnatus are amphibious fishes that spend most of their time on mudflats Their unique traits well demonstrate physiological and morphological adaptations against ecological constraints of the terrestrial environment. They acquired eyes on the top of their head, which enable them to feed and recognize predators on land. Towards the stronger effect of gravity on land, mudskippers evolved their terrestrial locomotive behaviors (so called ‘crutching’)
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