Click here to close
Hello! We notice that you are using Internet Explorer, which is not supported by Xenbase and may cause the site to display incorrectly.
We suggest using a current version of Chrome,
FireFox, or Safari.
BMC Genomics
2019 May 09;201:354. doi: 10.1186/s12864-019-5694-1.
Show Gene links
Show Anatomy links
What lies beneath? Molecular evolution during the radiation of caecilian amphibians.
Torres-Sánchez M
,
Gower DJ
,
Alvarez-Ponce D
,
Creevey CJ
,
Wilkinson M
,
San Mauro D
.
???displayArticle.abstract???
BACKGROUND: Evolution leaves an imprint in species through genetic change. At the molecular level, evolutionary changes can be explored by studying ratios of nucleotide substitutions. The interplay among molecular evolution, derived phenotypes, and ecological ranges can provide insights into adaptive radiations. Caecilians (order Gymnophiona), probably the least known of the major lineages of vertebrates, are limbless tropical amphibians, with adults of most species burrowing in soils (fossoriality). This enigmatic order of amphibians are very distinct phenotypically from other extant amphibians and likely from the ancestor of Lissamphibia, but little to nothing is known about the molecular changes underpinning their radiation. We hypothesised that colonization of various depths of tropical soils and of freshwater habitats presented new ecological opportunities to caecilians.
RESULTS: A total of 8540 candidate groups of orthologous genes from transcriptomic data of five species of caecilian amphibians and the genome of the frog Xenopus tropicalis were analysed in order to investigate the genetic machinery behind caecilian diversification. We found a total of 168 protein-coding genes with signatures of positive selection at different evolutionary times during the radiation of caecilians. The majority of these genes were related to functional elements of the cell membrane and extracellular matrix with expression in several different tissues. The first colonization of the tropical soils was connected to the largest number of protein-coding genes under positive selection in our analysis. From the results of our study, we highlighted molecular changes in genes involved in perception, reduction-oxidation processes, and aging that likely were involved in the adaptation to different soil strata.
CONCLUSIONS: The genes inferred to have been under positive selection provide valuable insights into caecilian evolution, potentially underpin adaptations of caecilians to their extreme environments, and contribute to a better understanding of fossorial adaptations and molecular evolution in vertebrates.
MCB 1818288 National Science Foundation, EEBB-I-17-12039 Ministerio de Economía y Competitividad, RYC-2011-09321 Ministerio de Economía y Competitividad, EEBB-I-16-11395 Ministerio de Economía y Competitividad, MCB 1818288 National Foundation for Science Foundation, P20 GM103440 NIGMS NIH HHS , CGL2012-40082 Ministerio de Economía y Competitividad, 5P30GM110767-04 Foundation for the National Institutes of Health, P30 GM110767 NIGMS NIH HHS , BES-2013-062723 Ministerio de Economía y Competitividad, P20GM103440 Foundation for the National Institutes of Health
Fig. 1. Phylogenetic tree used in the tests of positive selection. Branches used as foreground branches in the different tests are indicated with numbers as follows: 1: Gymnophiona branch, 2: Teresomata branch, 3: R. bivittatum branch, 4: Microcaecilia branch, 5: Caecilia + Typhlonectes branch, 6: M. dermatophaga branch, 7: M. unicolor branch, 8: T. compressicauda branch and 9: C. tentaculata branch. Hyphothesied ecological opportunities are marked with asterisks. Phylogeny based on [40] and [69]. Note that the sampling includes species from both sides of the basal divergence within Gymnophiona, so that branch 1 terminates in the last common ancestor of all extant caecilians. (Pictures credit: MW)
Fig. 2. General categories of biological processes from gene ontologies (GO) related to the genes under positive selection. For each of the sampled branches, the relative number of different annotated GO terms (a proxy of the number of identified genes under positive selection) under a general biological processes is symbolized by the different circle sizes (see legend)
Fig. 3. Protein-protein interaction (PPi) network predicted from the positive selected genes of the Gymnophiona branch (branch 1) that are involved in the ECM-receptor interaction pathway with a binding interaction (blue line) between lamc1 and itga3, and a reaction interaction (black line) between vwf and qsox1 (the latter protein-coding gene is part of a second shell of interactions)
Altschul,
Basic local alignment search tool.
1990, Pubmed
Altschul,
Basic local alignment search tool.
1990,
Pubmed
Anisimova,
Multiple hypothesis testing to detect lineages under positive selection that affects only a few sites.
2007,
Pubmed
Apweiler,
UniProt: the Universal Protein knowledgebase.
2004,
Pubmed
Ashburner,
Gene ontology: tool for the unification of biology. The Gene Ontology Consortium.
2000,
Pubmed
Bergthorsson,
Ohno's dilemma: evolution of new genes under continuous selection.
2007,
Pubmed
Bhosale,
Calcium signaling as a mediator of cell energy demand and a trigger to cell death.
2015,
Pubmed
Carey,
Amphibian declines: an immunological perspective.
1999,
Pubmed
,
Xenbase
Chakraborty,
Positive Selection and Centrality in the Yeast and Fly Protein-Protein Interaction Networks.
2016,
Pubmed
Cho,
Variants in FAM13A are associated with chronic obstructive pulmonary disease.
2010,
Pubmed
Conant,
Turning a hobby into a job: how duplicated genes find new functions.
2008,
Pubmed
Davalli,
ROS, Cell Senescence, and Novel Molecular Mechanisms in Aging and Age-Related Diseases.
2016,
Pubmed
Davies,
Family Wide Molecular Adaptations to Underground Life in African Mole-Rats Revealed by Phylogenomic Analysis.
2015,
Pubmed
Diekmann,
Gene Tree Affects Inference of Sites Under Selection by the Branch-Site Test of Positive Selection.
2015,
Pubmed
Dobó,
Multiple roles of complement MASP-1 at the interface of innate immune response and coagulation.
2014,
Pubmed
Fang,
Genome-wide adaptive complexes to underground stresses in blind mole rats Spalax.
2014,
Pubmed
Fraher,
Zebrafish Embryonic Lipidomic Analysis Reveals that the Yolk Cell Is Metabolically Active in Processing Lipid.
2016,
Pubmed
Gharib,
The branch-site test of positive selection is surprisingly robust but lacks power under synonymous substitution saturation and variation in GC.
2013,
Pubmed
Gillespie,
Community assembly through adaptive radiation in Hawaiian spiders.
2004,
Pubmed
Givnish,
Origin, adaptive radiation and diversification of the Hawaiian lobeliads (Asterales: Campanulaceae).
2009,
Pubmed
Grant,
Darwin's finches: Population variation and sympatric speciation.
1979,
Pubmed
Hemler,
Tetraspanin functions and associated microdomains.
2005,
Pubmed
Hull,
Life in the Aftermath of Mass Extinctions.
2015,
Pubmed
Inoue,
Tetraspanin 3c requirement for pigment cell interactions and boundary formation in zebrafish adult pigment stripes.
2014,
Pubmed
Irisarri,
Phylotranscriptomic consolidation of the jawed vertebrate timetree.
2017,
Pubmed
Kamei,
Discovery of a new family of amphibians from northeast India with ancient links to Africa.
2012,
Pubmed
Kim,
Positive selection at the protein network periphery: evaluation in terms of structural constraints and cellular context.
2007,
Pubmed
Kim,
Genome sequencing reveals insights into physiology and longevity of the naked mole rat.
2011,
Pubmed
Kosiol,
Patterns of positive selection in six Mammalian genomes.
2008,
Pubmed
Kupfer,
Parental investment by skin feeding in a caecilian amphibian.
2006,
Pubmed
LeGates,
Light as a central modulator of circadian rhythms, sleep and affect.
2014,
Pubmed
Lemmink,
Mutations in the type IV collagen alpha 3 (COL4A3) gene in autosomal recessive Alport syndrome.
1994,
Pubmed
Li,
RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome.
2011,
Pubmed
Lowe,
Three periods of regulatory innovation during vertebrate evolution.
2011,
Pubmed
Luisi,
Recent positive selection has acted on genes encoding proteins with more interactions within the whole human interactome.
2015,
Pubmed
Löytynoja,
Phylogeny-aware alignment with PRANK.
2014,
Pubmed
Maddin,
Influence of fossoriality on inner ear morphology: insights from caecilian amphibians.
2014,
Pubmed
Matern,
Transcriptomic Profiling of Zebrafish Hair Cells Using RiboTag.
2018,
Pubmed
Meyer,
Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions.
1999,
Pubmed
Mkaddem,
Lyn and Fyn function as molecular switches that control immunoreceptors to direct homeostasis or inflammation.
2017,
Pubmed
Mohun,
Identification and characterization of visual pigments in caecilians (Amphibia: Gymnophiona), an order of limbless vertebrates with rudimentary eyes.
2010,
Pubmed
Montoya-Burgos,
Patterns of positive selection and neutral evolution in the protein-coding genes of Tetraodon and Takifugu.
2011,
Pubmed
Murray,
Regulation of programmed cell death by basement membranes in embryonic development.
2000,
Pubmed
Naylor,
The trunk musculature of caecilians (Amphibia: Gymnophiona).
1980,
Pubmed
Park,
Transcript profiling and lipidomic analysis of ceramide subspecies in mouse embryonic stem cells and embryoid bodies.
2010,
Pubmed
Parker,
Genome-wide signatures of convergent evolution in echolocating mammals.
2013,
Pubmed
Peterson,
Blunted neuronal calcium response to hypoxia in naked mole-rat hippocampus.
2012,
Pubmed
Rayagiri,
Basal lamina remodeling at the skeletal muscle stem cell niche mediates stem cell self-renewal.
2018,
Pubmed
Renous,
[Cranial morphology of an American siphonopid, Microcaecilia unicolor (Amphibia, Gymnophiona) and its functional interpretation].
1990,
Pubmed
Roscito,
Comparative cranial osteology of fossorial lizards from the tribe Gymnophthalmini (Squamata, Gymnophthalmidae).
2010,
Pubmed
Roux,
Patterns of positive selection in seven ant genomes.
2014,
Pubmed
San Mauro,
Life-history evolution and mitogenomic phylogeny of caecilian amphibians.
2014,
Pubmed
Seehausen,
African cichlid fish: a model system in adaptive radiation research.
2006,
Pubmed
Sela,
GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters.
2015,
Pubmed
Shim,
Differential expression of laminin chain-specific mRNA transcripts during mouse preimplantation embryo development.
1996,
Pubmed
Smyth,
Absence of basement membranes after targeting the LAMC1 gene results in embryonic lethality due to failure of endoderm differentiation.
1999,
Pubmed
Supek,
REVIGO summarizes and visualizes long lists of gene ontology terms.
2011,
Pubmed
Szklarczyk,
STRING v10: protein-protein interaction networks, integrated over the tree of life.
2015,
Pubmed
Sánchez Alvarado,
To solve old problems, study new research organisms.
2018,
Pubmed
Talavera,
Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments.
2007,
Pubmed
Taylor,
Duplication and divergence: the evolution of new genes and old ideas.
2004,
Pubmed
Toews,
Blood respiratory properties of a viviparous amphibian.
1977,
Pubmed
Torres-Sánchez,
Multi-tissue transcriptomes of caecilian amphibians highlight incomplete knowledge of vertebrate gene families.
2019,
Pubmed
Tsai,
The ectoenzyme E-NPP3 negatively regulates ATP-dependent chronic allergic responses by basophils and mast cells.
2015,
Pubmed
Wagner,
The molecular origins of evolutionary innovations.
2011,
Pubmed
Wellborn,
Ecological opportunity and the adaptive diversification of lineages.
2015,
Pubmed
Wilkinson,
One hundred million years of skin feeding? Extended parental care in a Neotropical caecilian (Amphibia: Gymnophiona).
2008,
Pubmed
Wilkinson,
Caecilians.
2012,
Pubmed
Wilkinson,
A new species of skin-feeding caecilian and the first report of reproductive mode in Microcaecilia (amphibia: Gymnophiona: Siphonopidae).
2013,
Pubmed
Wollenberg,
Why colour in subterranean vertebrates? Exploring the evolution of colour patterns in caecilian amphibians.
2009,
Pubmed
Wu,
Molecular study of worldwide distribution and diversity of soil animals.
2011,
Pubmed
Yang,
Inference of selection from multiple species alignments.
2002,
Pubmed
Yang,
PAML 4: phylogenetic analysis by maximum likelihood.
2007,
Pubmed
Yang,
Statistical properties of the branch-site test of positive selection.
2011,
Pubmed
Yang,
Bayes empirical bayes inference of amino acid sites under positive selection.
2005,
Pubmed
Yates,
Ensembl 2016.
2016,
Pubmed
Yoder,
Ecological opportunity and the origin of adaptive radiations.
2010,
Pubmed
Zhang,
Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level.
2005,
Pubmed
Zhang,
Hypoxia serves a key function in the upregulated expression of vascular adhesion protein‑1 in vitro and in a rat model of hemorrhagic shock.
2017,
Pubmed
Zhang,
Higher-level salamander relationships and divergence dates inferred from complete mitochondrial genomes.
2009,
Pubmed
Zhong,
Tet2: breaking down barriers to T cell cytokine expression.
2015,
Pubmed
Zhou,
The Pin2/TRF1-interacting protein PinX1 is a potent telomerase inhibitor.
2001,
Pubmed
Ziółkowska-Suchanek,
Susceptibility loci in lung cancer and COPD: association of IREB2 and FAM13A with pulmonary diseases.
2015,
Pubmed
Ziółkowska-Suchanek,
FAM13A as a Novel Hypoxia-Induced Gene in Non-Small Cell Lung Cancer.
2017,
Pubmed
Zylberberg,
Structure of the dermal scales in gymnophiona (Amphibia).
1980,
Pubmed
de Magalhães,
A database of vertebrate longevity records and their relation to other life-history traits.
2009,
Pubmed