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Myoglobin primary structure reveals multiple convergent transitions to semi-aquatic life in the world's smallest mammalian divers.

Kai He | Triston G Eastman | Hannah Czolacz | Shuhao Li | Akio Shinohara | Shin-Ichiro Kawada | Mark S Springer | Michael Berenbrink | Kevin L Campbell
eLife | 2021

The speciose mammalian order Eulipotyphla (moles, shrews, hedgehogs, solenodons) combines an unusual diversity of semi-aquatic, semi-fossorial, and fossorial forms that arose from terrestrial forbearers. However, our understanding of the ecomorphological pathways leading to these lifestyles has been confounded by a fragmentary fossil record, unresolved phylogenetic relationships, and potential morphological convergence, calling for novel approaches. The net surface charge of the oxygen-storing muscle protein myoglobin (ZMb), which can be readily determined from its primary structure, provides an objective target to address this question due to mechanistic linkages with myoglobin concentration. Here, we generate a comprehensive 71 species molecular phylogeny that resolves previously intractable intra-family relationships and then ancestrally reconstruct ZMb evolution to identify ancient lifestyle transitions based on protein sequence alone. Our phylogenetically informed analyses confidently resolve fossorial habits having evolved twice in talpid moles and reveal five independent secondary aquatic transitions in the order housing the world's smallest endothermic divers.

Pubmed ID: 33949308

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This is a list of tools and resources that we have found mentioned in this publication.


R Project for Statistical Computing (tool)

RRID:SCR_001905

Software environment and programming language for statistical computing and graphics. R is integrated suite of software facilities for data manipulation, calculation and graphical display. Can be extended via packages. Some packages are supplied with the R distribution and more are available through CRAN family.It compiles and runs on wide variety of UNIX platforms, Windows and MacOS.

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Torrent Variant Caller Standalone (tool)

RRID:SCR_015694

A variant vcf file analysis tool.

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BEAST2 (tool)

RRID:SCR_017307

Software package for advanced Bayesian evolutionary analysis by sampling trees. Used for phylogenetics, population genetics and phylodynamics. Program for Bayesian phylogenetic analysis of molecular sequences. Estimates rooted, time measured phylogenies using strict or relaxed molecular clock models. Framework can be extended by third parties. Comprised of standalone programs including BEAUti, BEAST, MASTER, RBS, SNAPP, MultiTypeTree, BDSKY, LogAnalyser, LogCombiner, TreeAnnotator, DensiTree and package manager.

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Trinity (tool)

RRID:SCR_013048

Software for the efficient and robust de novo reconstruction of transcriptomes from RNA-seq data.

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New England Biolabs (tool)

RRID:SCR_013517

An Antibody supplier

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Fastml (tool)

RRID:SCR_016092

Web application for the reconstruction of ancestral sequences. It computes maximum likelihood ancestral sequence reconstruction based on the phylogenetic relations between homologous sequences.

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FastTree (software resource)

RRID:SCR_015501

Source code that infers approximately-maximum-likelihood phylogenetic trees from alignments of nucleotide or protein sequences. It uses the Jukes-Cantor or generalized time-reversible (GTR) models of nucleotide evolution and the JTT, WAG, or LG models of amino acid evolution.

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SPAdes (software resource)

RRID:SCR_000131

Software package for assembling single cell genomes and mini metagenomes. Uses short read sets as input. Used for genomes of uncultivatable bacteria that vastly exceeds what may be obtained via traditional metagenomics studies. Works with Illumina or IonTorrent reads and can provide hybrid assemblies using PacBio, Oxford Nanopore and Sanger reads. Intended for small genomes like bacterial or fungal.

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MEGA Software (software resource)

RRID:SCR_000667

Software integrated tool for conducting automatic and manual sequence alignment, inferring phylogenetic trees, mining web based databases, estimating rates of molecular evolution, and testing evolutionary hypotheses. Used for comparative analysis of DNA and protein sequences to infer molecular evolutionary patterns of genes, genomes, and species over time. MEGA version 4 expands on existing facilities for editing DNA sequence data from autosequencers, mining Web-databases, performing automatic and manual sequence alignment, analyzing sequence alignments to estimate evolutionary distances, inferring phylogenetic trees, and testing evolutionary hypotheses. MEGA version 6 enables inference of timetrees, as it implements RelTime method for estimating divergence times for all branching points in phylogeny.

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SWISS-MODEL (software resource)

RRID:SCR_018123

Software tool as fully automated protein structure homology modeling server, accessible via ExPASy web server, or from program DeepView Swiss Pdb-Viewer. Structural bioinformatics web-server dedicated to homology modeling of 3D protein structures. Used to make protein modelling accessible to all biochemists and molecular biologists.

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Recombination Detection Program (software resource)

RRID:SCR_018537

Software package to analyse nucleotide sequence data and identify evidence of genetic recombination. RDP3 is version of RDP program for characterizing recombination events in DNA-sequence alignments. RDP4 is version of RDP program for detection and analysis of recombination patterns in virus genomes.

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ABySS (software resource)

RRID:SCR_010709

Software providing de novo, parallel, paired-end sequence assembler that is designed for short reads. ABySS 1.0 originally showed that assembling human genome using short 50 bp sequencing reads was possible by aggregating half terabyte of compute memory needed over several computers using standardized message passing system. ABySS 2.0 is Resource Efficient Assembly of Large Genomes using Bloom Filter. ABySS 2.0 departs from MPI and instead implements algorithms that employ Bloom filter, probabilistic data structure, to represent de Bruijn graph and reduce memory requirements.

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Geneious (software resource)

RRID:SCR_010519

Software package for sequence alignment, assembly and analysis. Integrated and extendable desktop software platform for organization and analysis of sequence data. Bioinformatics software platform packed with molecular biology and sequence analysis tools.

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SolexaQA (software resource)

RRID:SCR_005421

Software package to calculate sequence quality statistics and create visual representations of data quality for Illumina's second-generation sequencing technology.

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phytools (software resource)

RRID:SCR_015502

Software R package for phylogenetic comparative biology. The package contains various functions for phylogenetic analysis of comparative data from species.

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PAML (software resource)

RRID:SCR_014932

Package of programs for phylogenetic analyses of DNA or protein sequences using maximum likelihood. PAML estimates parameters and tests hypotheses to study the evolutionary process from a phylogenetic tree.

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AlienTrimmer (software resource)

RRID:SCR_011835

Allows detecting and removing multiple alien sequences in both ends of sequence reads.

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Trimmomatic (data processing software)

RRID:SCR_011848

Software Java pipeline for trimming tasks for Illumina paired end and single ended data. Flexible Trimmer for Illumina Sequence Data. Pair aware preprocessing tool optimized for Illumina next generation sequencing data. Includes several processing steps for read trimming and filtering. Operating systems Unix/Linux, Mac OS, Windows.

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MAFFT (software resource)

RRID:SCR_011811

Software package as multiple alignment program for amino acid or nucleotide sequences. Can align up to 500 sequences or maximum file size of 1 MB. First version of MAFFT used algorithm based on progressive alignment, in which sequences were clustered with help of Fast Fourier Transform. Subsequent versions have added other algorithms and modes of operation, including options for faster alignment of large numbers of sequences, higher accuracy alignments, alignment of non-coding RNA sequences, and addition of new sequences to existing alignments.

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RAxML (software resource)

RRID:SCR_006086

Software program for phylogenetic analyses of large datasets under maximum likelihood.

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PyMOL (software resource)

RRID:SCR_000305

A user-sponsored molecular visualization software system on an open-source foundation. The software has the capabilities to view, render, animate, export, present and develop three dimensional molecular structures.

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FastQC (software resource)

RRID:SCR_014583

Quality control software that perform checks on raw sequence data coming from high throughput sequencing pipelines. This software also provides a modular set of analyses which can give a quick impression of the quality of the data prior to further analysis.

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ggtree (data processing software)

RRID:SCR_018560

Software R package for visualization and annotation of phylogenetic trees with their covariates and other tree like structures with their annotation data. Can import evolutionary data from different tree file formats and analysis programs as well as other associated data from experiments so that various sources and types of data can be displayed on tree for comparison and further analyses.

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BEAST (software resource)

RRID:SCR_010228

A cross-platform software program for Bayesian MCMC analysis of molecular sequences. It is entirely orientated towards rooted, time-measured phylogenies inferred using strict or relaxed molecular clock models. It can be used as a method of reconstructing phylogenies but is also a framework for testing evolutionary hypotheses without conditioning on a single tree topology. BEAST uses MCMC to average over tree space, so that each tree is weighted proportional to its posterior probability. We include a simple to use user-interface program for setting up standard analyses and a suit of programs for analysing the results.

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MIRA (software resource)

RRID:SCR_010731

Sequence assembler and mapper for whole genome shotgun and EST/RNASeq sequencing data.

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