Shedding Light on a Secretive Tertiary Urodelean Relict: Hynobiid Salamanders (<em>Paradactylodon persicus</em> s.l.) from Iran, Illuminated by Phylogeographic, Developmental, and Transcriptomic Data

The Hyrcanian Forests present a unique Tertiary relict ecosystem, covering the northern Elburz and Talysh Ranges (Iran, Azerbaijan), a poorly investigated, unique biodiversity hotspot with many cryptic species. Since the 1970s, two nominal species of Urodela, Hynobiidae, <i>Batrachuperus</i...

Full description

Bibliographic Details
Main Authors: Matthias Stöck, Fatemeh Fakharzadeh, Heiner Kuhl, Beata Rozenblut-Kościsty, Sophie Leinweber, Riddhi Patel, Mehregan Ebrahimi, Sebastian Voitel, Josef Friedrich Schmidtler, Haji Gholi Kami, Maria Ogielska, Daniel W. Förster
Format: Article
Language:English
Published: MDPI AG 2019-04-01
Series:Genes
Subjects:
Online Access:https://www.mdpi.com/2073-4425/10/4/306
id doaj-ab431bc6f041423b8859c26a2f6ada10
record_format Article
spelling doaj-ab431bc6f041423b8859c26a2f6ada102020-11-25T00:30:03ZengMDPI AGGenes2073-44252019-04-0110430610.3390/genes10040306genes10040306Shedding Light on a Secretive Tertiary Urodelean Relict: Hynobiid Salamanders (<em>Paradactylodon persicus</em> s.l.) from Iran, Illuminated by Phylogeographic, Developmental, and Transcriptomic DataMatthias Stöck0Fatemeh Fakharzadeh1Heiner Kuhl2Beata Rozenblut-Kościsty3Sophie Leinweber4Riddhi Patel5Mehregan Ebrahimi6Sebastian Voitel7Josef Friedrich Schmidtler8Haji Gholi Kami9Maria Ogielska10Daniel W. Förster11Leibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB), Müggelseedamm 301, D-12587 Berlin, GermanyDepartment of Biology, Faculty of Sciences, Shahid Chamran University of Ahvaz, Ahvaz 61357-43135, IranLeibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB), Müggelseedamm 301, D-12587 Berlin, GermanyDepartment of Evolutionary Biology and Conservation of Vertebrates, Wroclaw University, Sienkiewicza 21, 50-335 Wroclaw, PolandLeibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB), Müggelseedamm 301, D-12587 Berlin, GermanyEvolutionary Genetics Department, Leibniz-Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315 Berlin, GermanyDepartment of Biology, College of Sciences, Shiraz University, Shiraz 71467-13565, IranIndependent Researcher, Spangenbergstraße 81, D-06295 Eisleben, GermanyZoologische Staatssammlung, Münchhausenstraße 21, 81247 München, GermanyDepartment of Biology, Faculty of Sciences, Golestan University, Gorgan 49136-15759, IranDepartment of Evolutionary Biology and Conservation of Vertebrates, Wroclaw University, Sienkiewicza 21, 50-335 Wroclaw, PolandEvolutionary Genetics Department, Leibniz-Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315 Berlin, GermanyThe Hyrcanian Forests present a unique Tertiary relict ecosystem, covering the northern Elburz and Talysh Ranges (Iran, Azerbaijan), a poorly investigated, unique biodiversity hotspot with many cryptic species. Since the 1970s, two nominal species of Urodela, Hynobiidae, <i>Batrachuperus</i> (later: <i>Paradactylodon</i>) have been described: <i>Paradactylodon persicus</i> from northwestern and <i>P. gorganensis</i> from northeastern Iran. Although <i>P. gorganensis</i> has been involved in studies on phylogeny and development, there is little data on the phylogeography, systematics, and development of the genus throughout the Hyrcanian Forests; genome-wide resources have been entirely missing. Given the huge genome size of hynobiids, making whole genome sequencing hardly affordable, we aimed to publish the first transcriptomic resources for <i>Paradactylodon</i> from an embryo and a larva (9.17 Gb RNA sequences; assembled to 78,918 unigenes). We also listed 32 genes involved in vertebrate sexual development and sex determination. Photographic documentation of the development from egg sacs across several embryonal and larval stages until metamorphosis enabled, for the first time, comparison of the ontogeny with that of other hynobiids and new histological and transcriptomic insights into early gonads and timing of their differentiation. Transcriptomes from central Elburz, next-generation sequencing (NGS) libraries of archival DNA of topotypic <i>P. persicus</i>, and GenBank-sequences of eastern <i>P. gorganensis</i> allowed phylogenetic analysis with three mitochondrial genomes, supplemented by PCR-amplified mtDNA-fragments from 17 museum specimens, documenting &lt;2% uncorrected intraspecific genetic distance. Our data suggest that these rare salamanders belong to a single species <i>P. persicus</i> s.l. Humankind has a great responsibility to protect this species and the unique biodiversity of the Hyrcanian Forest ecosystems.https://www.mdpi.com/2073-4425/10/4/306UrodelaHynobiidaephylogeographyRNAseqgenomicsgene expressiongonadal developmenthistologysystematics
collection DOAJ
language English
format Article
sources DOAJ
author Matthias Stöck
Fatemeh Fakharzadeh
Heiner Kuhl
Beata Rozenblut-Kościsty
Sophie Leinweber
Riddhi Patel
Mehregan Ebrahimi
Sebastian Voitel
Josef Friedrich Schmidtler
Haji Gholi Kami
Maria Ogielska
Daniel W. Förster
spellingShingle Matthias Stöck
Fatemeh Fakharzadeh
Heiner Kuhl
Beata Rozenblut-Kościsty
Sophie Leinweber
Riddhi Patel
Mehregan Ebrahimi
Sebastian Voitel
Josef Friedrich Schmidtler
Haji Gholi Kami
Maria Ogielska
Daniel W. Förster
Shedding Light on a Secretive Tertiary Urodelean Relict: Hynobiid Salamanders (<em>Paradactylodon persicus</em> s.l.) from Iran, Illuminated by Phylogeographic, Developmental, and Transcriptomic Data
Genes
Urodela
Hynobiidae
phylogeography
RNAseq
genomics
gene expression
gonadal development
histology
systematics
author_facet Matthias Stöck
Fatemeh Fakharzadeh
Heiner Kuhl
Beata Rozenblut-Kościsty
Sophie Leinweber
Riddhi Patel
Mehregan Ebrahimi
Sebastian Voitel
Josef Friedrich Schmidtler
Haji Gholi Kami
Maria Ogielska
Daniel W. Förster
author_sort Matthias Stöck
title Shedding Light on a Secretive Tertiary Urodelean Relict: Hynobiid Salamanders (<em>Paradactylodon persicus</em> s.l.) from Iran, Illuminated by Phylogeographic, Developmental, and Transcriptomic Data
title_short Shedding Light on a Secretive Tertiary Urodelean Relict: Hynobiid Salamanders (<em>Paradactylodon persicus</em> s.l.) from Iran, Illuminated by Phylogeographic, Developmental, and Transcriptomic Data
title_full Shedding Light on a Secretive Tertiary Urodelean Relict: Hynobiid Salamanders (<em>Paradactylodon persicus</em> s.l.) from Iran, Illuminated by Phylogeographic, Developmental, and Transcriptomic Data
title_fullStr Shedding Light on a Secretive Tertiary Urodelean Relict: Hynobiid Salamanders (<em>Paradactylodon persicus</em> s.l.) from Iran, Illuminated by Phylogeographic, Developmental, and Transcriptomic Data
title_full_unstemmed Shedding Light on a Secretive Tertiary Urodelean Relict: Hynobiid Salamanders (<em>Paradactylodon persicus</em> s.l.) from Iran, Illuminated by Phylogeographic, Developmental, and Transcriptomic Data
title_sort shedding light on a secretive tertiary urodelean relict: hynobiid salamanders (<em>paradactylodon persicus</em> s.l.) from iran, illuminated by phylogeographic, developmental, and transcriptomic data
publisher MDPI AG
series Genes
issn 2073-4425
publishDate 2019-04-01
description The Hyrcanian Forests present a unique Tertiary relict ecosystem, covering the northern Elburz and Talysh Ranges (Iran, Azerbaijan), a poorly investigated, unique biodiversity hotspot with many cryptic species. Since the 1970s, two nominal species of Urodela, Hynobiidae, <i>Batrachuperus</i> (later: <i>Paradactylodon</i>) have been described: <i>Paradactylodon persicus</i> from northwestern and <i>P. gorganensis</i> from northeastern Iran. Although <i>P. gorganensis</i> has been involved in studies on phylogeny and development, there is little data on the phylogeography, systematics, and development of the genus throughout the Hyrcanian Forests; genome-wide resources have been entirely missing. Given the huge genome size of hynobiids, making whole genome sequencing hardly affordable, we aimed to publish the first transcriptomic resources for <i>Paradactylodon</i> from an embryo and a larva (9.17 Gb RNA sequences; assembled to 78,918 unigenes). We also listed 32 genes involved in vertebrate sexual development and sex determination. Photographic documentation of the development from egg sacs across several embryonal and larval stages until metamorphosis enabled, for the first time, comparison of the ontogeny with that of other hynobiids and new histological and transcriptomic insights into early gonads and timing of their differentiation. Transcriptomes from central Elburz, next-generation sequencing (NGS) libraries of archival DNA of topotypic <i>P. persicus</i>, and GenBank-sequences of eastern <i>P. gorganensis</i> allowed phylogenetic analysis with three mitochondrial genomes, supplemented by PCR-amplified mtDNA-fragments from 17 museum specimens, documenting &lt;2% uncorrected intraspecific genetic distance. Our data suggest that these rare salamanders belong to a single species <i>P. persicus</i> s.l. Humankind has a great responsibility to protect this species and the unique biodiversity of the Hyrcanian Forest ecosystems.
topic Urodela
Hynobiidae
phylogeography
RNAseq
genomics
gene expression
gonadal development
histology
systematics
url https://www.mdpi.com/2073-4425/10/4/306
work_keys_str_mv AT matthiasstock sheddinglightonasecretivetertiaryurodeleanrelicthynobiidsalamandersemparadactylodonpersicusemslfromiranilluminatedbyphylogeographicdevelopmentalandtranscriptomicdata
AT fatemehfakharzadeh sheddinglightonasecretivetertiaryurodeleanrelicthynobiidsalamandersemparadactylodonpersicusemslfromiranilluminatedbyphylogeographicdevelopmentalandtranscriptomicdata
AT heinerkuhl sheddinglightonasecretivetertiaryurodeleanrelicthynobiidsalamandersemparadactylodonpersicusemslfromiranilluminatedbyphylogeographicdevelopmentalandtranscriptomicdata
AT beatarozenblutkoscisty sheddinglightonasecretivetertiaryurodeleanrelicthynobiidsalamandersemparadactylodonpersicusemslfromiranilluminatedbyphylogeographicdevelopmentalandtranscriptomicdata
AT sophieleinweber sheddinglightonasecretivetertiaryurodeleanrelicthynobiidsalamandersemparadactylodonpersicusemslfromiranilluminatedbyphylogeographicdevelopmentalandtranscriptomicdata
AT riddhipatel sheddinglightonasecretivetertiaryurodeleanrelicthynobiidsalamandersemparadactylodonpersicusemslfromiranilluminatedbyphylogeographicdevelopmentalandtranscriptomicdata
AT mehreganebrahimi sheddinglightonasecretivetertiaryurodeleanrelicthynobiidsalamandersemparadactylodonpersicusemslfromiranilluminatedbyphylogeographicdevelopmentalandtranscriptomicdata
AT sebastianvoitel sheddinglightonasecretivetertiaryurodeleanrelicthynobiidsalamandersemparadactylodonpersicusemslfromiranilluminatedbyphylogeographicdevelopmentalandtranscriptomicdata
AT joseffriedrichschmidtler sheddinglightonasecretivetertiaryurodeleanrelicthynobiidsalamandersemparadactylodonpersicusemslfromiranilluminatedbyphylogeographicdevelopmentalandtranscriptomicdata
AT hajigholikami sheddinglightonasecretivetertiaryurodeleanrelicthynobiidsalamandersemparadactylodonpersicusemslfromiranilluminatedbyphylogeographicdevelopmentalandtranscriptomicdata
AT mariaogielska sheddinglightonasecretivetertiaryurodeleanrelicthynobiidsalamandersemparadactylodonpersicusemslfromiranilluminatedbyphylogeographicdevelopmentalandtranscriptomicdata
AT danielwforster sheddinglightonasecretivetertiaryurodeleanrelicthynobiidsalamandersemparadactylodonpersicusemslfromiranilluminatedbyphylogeographicdevelopmentalandtranscriptomicdata
_version_ 1725328197718900736