Mudskippers and Their Genetic Adaptations to an Amphibious Lifestyle

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Mudskippers and Their Genetic Adaptations to an Amphibious Lifestyle animals Review Mudskippers and Their Genetic Adaptations to an Amphibious Lifestyle Xinxin You 1,2,†, Min Sun 1,†, Jia Li 1, Chao Bian 1,2, Jieming Chen 1,3, Yunhai Yi 1,2 ID , Hui Yu 1 and Qiong Shi 1,2,4,* 1 Shenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI Marine, BGI, Shenzhen 518083, China; [email protected] (X.Y.); [email protected] (M.S.); [email protected] (J.L.); [email protected] (C.B.); [email protected] (J.C.); [email protected] (Y.Y.);[email protected] (H.Y.) 2 BGI Education Center, University of Chinese Academy of Sciences, Shenzhen 518063, China 3 BGI-Zhenjiang Institute of Hydrobiology, BGI Marine, BGI, Zhenjiang 212000, China 4 Laboratory of Aquatic Genomics, College of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, China * Correspondence: [email protected]; Tel.: +86-185-6627-9826, Fax: +86-755-3635-2508 † These authors contributed equally to this work. Received: 18 December 2017; Accepted: 3 February 2018; Published: 7 February 2018 Simple Summary: Mudskippers are an interesting group of goggle-eyed amphibious fish that can live both in water and on land. They are a useful model for obtaining insights into the genetic mechanisms underlying the terrestrial adaptations of amphibious fish. This review summarizes the morphological and physiological modifications of representative mudskippers, and focuses on the recent advancement of genomic studies on their genetic adaptations to the amphibious lifestyle. Abstract: Mudskippers are the largest group of amphibious teleost fish that are uniquely adapted to live on mudflats. During their successful transition from aqueous life to terrestrial living, these fish have evolved morphological and physiological modifications of aerial vision and olfaction, higher ammonia tolerance, aerial respiration, improved immunological defense against terrestrial pathogens, and terrestrial locomotion using protruded pectoral fins. Comparative genomic and transcriptomic data have been accumulated and analyzed for understanding molecular mechanisms of the terrestrial adaptations. Our current review provides a general introduction to mudskippers and recent research advances of their genetic adaptations to the amphibious lifestyle, which will be helpful for understanding the evolutionary transition of vertebrates from water to land. Our insights into the genomes and transcriptomes will also support molecular breeding, functional identification, and natural compound screening. Keywords: mudskipper; amphibious lifestyle; genome; transcriptome; terrestrial adaptation 1. Introduction Amphibious fish spend periods of time out of water, in or above the ground surface, as normal parts of their life histories [1]. Mudskippers (Figure1) are a major group of amphibious fish with an enormous potential for theoretical research into critical adaptations to facilitate the evolution from an aqueous to a terrestrial lifestyle. They are divided into four main genera, including Boleophthalmus, Periophthalmodon, Periophthalmus, and Scartelaos [2]. Mudskippers have developed morphological and physiological terrestrial adaptations to match their unique lifestyle, such as modification of aerial vision, higher ammonia tolerance, and terrestrial locomotion using protruded pectoral fins [3–5]. Animals 2018, 8, 24; doi:10.3390/ani8020024 www.mdpi.com/journal/animals Animals 2018, 8, x 2 of 12 modificationAnimals 2018, 8, of 24 aerial vision, higher ammonia tolerance, and terrestrial locomotion using protruded2 of 12 pectoral fins [3–5]. Figure 1. Representative mudskippers and their habitats [5]. Scartelaos histophorus (SH) and Figure 1. Representative mudskippers and their habitats [5]. Scartelaos histophorus (SH) and Boleophthalmus pectinirostris (BP) are predominantly water-dwelling, whereas Periophthalmodon Boleophthalmus pectinirostris (BP) are predominantly water-dwelling, whereas Periophthalmodon schlosseri schlosseri (PS) and Periophthalmus magnuspinnatus (PM) spend extended periods of time on land. (PS) and Periophthalmus magnuspinnatus (PM) spend extended periods of time on land. By presenting the first genome sequences of amphibious fish [5], we provide a new model for understandingBy presenting the theadaptive first genome evolution sequences of animals of amphibious from water fish to land. [5], we In provide the genome a new report, model we for sequencedunderstanding four the representative adaptive evolution species of of animals mudskippers from water (Figure to land. 1), Inincluding the genome Boleophthalmus report, we pectinirostrissequenced four (BP representative or blue-spotted species mudskipper), of mudskippers Scartelaos (Figure 1histophorus), including (SHBoleophthalmus or blue mudskipper), pectinirostris (BPPeriophthalmodon or blue-spotted schlosseri mudskipper), (PS or Scartelaosgiant mudskipper), histophorus and(SH Periophthalmus or blue mudskipper), magnuspinnatusPeriophthalmodon (PM or giant-finschlosseri (PSmudskipper). or giant mudskipper), The four mudskippers and Periophthalmus form a magnuspinnatusmonophyletic clade(PM or that giant-fin diverged mudskipper). from the Theother four teleosts mudskippers ~140 million form years a monophyletic ago [5]. BP cladeand SH that form diverged one sister from group, the other and teleosts are predominantly ~140 million aqueousyears ago and [5]. spend BP and less SH time form out one of sister water, group, whereas and PS are and predominantly PM constitute aqueous another and sister spend group, less timeand areout primarily of water, whereasterrestrial PS and and spend PM constituteextended periods another of sister time group,on land. and Interestingly, are primarily the terrestrial genome sizes and decreasespend extended in the following periods oforder: time BP on land.> SH > Interestingly, PM > PS, which the genomemay be associated sizes decrease with in their the followingterrestrial affinityorder: BP but > SHunrelated > PM > to PS, their which body may size be (PS associated > BP > withSH > theirPM). terrestrial Comparative affinity genomic but unrelated analyses to were their carriedbody size out (PS to > BPgain > SHinsights > PM). into Comparative the fundamen genomictalanalyses genetic werebasis carried of terrestrial out to gain adaptation insights into in mudskippers.the fundamental Since genetic then, basis more of an terrestriald more knowledge adaptation about in mudskippers. genetic adaptations Since then, to the more amphibious and more lifestyleknowledge has aboutbeen accumulated genetic adaptations (Figure to 2). the amphibious lifestyle has been accumulated (Figure2). Mudskippers spendspend part part of of their their lives lives out ofout water of water to feed, to mate,feed, andmate, avoid and capture avoid bycapture terrestrial by predators.terrestrial predators. Therefore, theyTherefore, have developed they have behavioral developed and behavioral physiological and physiological specializations specializations for adaptation forto the adaptation amphibious to life.the Theamphibious most significant life. The morphological most significant and functional morphological modifications and functional (Figure1) modificationsare the trend to (Figure possess 1) close-set are the trend and moveableto possess protuberant close-set and eyes moveable set high protuberant on the head eyes for escape set high from on predatorsthe head for on escape land, andfrom the predators eyes are on structural land, and adapted the eyes for are accurate structural vision adapted in both for accurate air andwater vision [ 6in]; + bothhigher air ammonia and water tolerance [6]; higher allow ammonia the fish tolerance to live in al thelow high the concentrationfish to live in ofthe NH high3/NH concentration4 within the of NHintertidal3/NH4+ zone within [7 –the9]; intertidal stronger pectoralzone [7–9]; fins stronger help mudskippers pectoral fins crawl help andmudskippers jump in the crawl mudflat and jump [10]; inhigher the diseasemudflat resistance [10]; higher enables disease mudskippers resistance to enables inhabit bothmudskippers aqueous and to terrestrialinhabit both environments aqueous and [5]; terrestrialand specialized environments skin retains [5]; moreand sp waterecialized for them skin to retains stay on more land water for a longerfor them period to stay [6]. on land for a longerThe period main [6]. objective of this review is to summarize the current knowledge of genetic adaptations to theThe amphibious main objective lifestyle of ofthis mudskippers, review is to suchsummari as aerialze the vision current and knowledge olfaction modifications, of genetic adaptations ammonia totolerance the amphibious mechanisms, lifestyle terrestrial of mudskippers, locomotion, immunological such as aerial difference, vision and and olfaction air exposure modifications, response. ammonia tolerance mechanisms, terrestrial locomotion, immunological difference, and air exposure response. Animals 2018, 8, 24 3 of 12 Animals 2018, 8, x 3 of 12 Figure 2.2. SummarySummary ofof important important genes genes related related to theto th amphibiouse amphibious lifestyle lifestyle of mudskippers. of mudskippers. The blue-The blue-spottedspotted mudskipper mudskipper (B. pectinirostris (B. pectinirostris, BP) is jumping, BP) is onjumping the mudflat. on the Abbreviations: mudflat. Abbreviations:aanat, aralkylamine aanat, aralkylamineN-acetyltransferase; N-acetyltransferase;And2, actinodin And2 2; Arg, actinodin, arginase; 2; Rhcg1Arg,
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