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Molecular phylogenetic analysis of a taxonomically unstable ranid from Sumatra, Indonesia, reveals a new genus with gastromyzophorous tadpoles and two new species

Arifin U.a, Smart U.b, Hertwig S.T.c,d, Smith E.N.b, Iskandar D.T.e, Haas A.a

a Centrum für Naturkunde – Zoologisches Museum, Universität Hamburg, Hamburg, 20146, Germany
b Amphibian and Reptile Diversity Research Center, Department of Biology, University of Texas, Arlington, 76019-0498, United States
c Naturhistorisches Museum der Burgergemeinde Bern, Bern, CH-3005, Switzerland
d Institute of Ecology and Evolution, University of Bern, Bern, CH-3012, Switzerland
e School of Life Sciences and Technology, Institute of Technology Bandung, Tamansari, Bandung, 40132, Indonesia

[vc_row][vc_column][vc_row_inner][vc_column_inner][vc_separator css=”.vc_custom_1624529070653{padding-top: 30px !important;padding-bottom: 30px !important;}”][/vc_column_inner][/vc_row_inner][vc_row_inner layout=”boxed”][vc_column_inner width=”3/4″ css=”.vc_custom_1624695412187{border-right-width: 1px !important;border-right-color: #dddddd !important;border-right-style: solid !important;border-radius: 1px !important;}”][vc_empty_space][megatron_heading title=”Abstract” size=”size-sm” text_align=”text-left”][vc_column_text]© Umilaela Arifin et al.The presence of an adhesive abdominal sucker (gastromyzophory) allows tadpoles of certain species of anurans to live in fast-flowing streams. Gastromyzophorous tadpoles are rare among anurans, known only in certain American bufonids and Asian ranids. To date, Huia sumatrana, which inhabits cascading streams, has been the only Sumatran ranid known to possess gastromyzophorous tadpoles. In the absence of thorough sampling and molecular barcoding of adults and larvae, it has remained to be confirmed whether other Sumatran ranid species living in similar habitats, i.e., Chalcorana crassiovis, possesses this larval type. Moreover, the taxonomic status of this species has long been uncertain and its taxonomic position within the Ranidae, previously based exclusively on morphological characters, has remained unresolved. To study the diversity and relationships of these frogs and to establish the identity of newly collected gastromyzophorous tadpoles from Sumatra, we compared genetic sequences of C. crassiovis-like taxa from a wide range of sites on Sumatra. We conducted bayesian and maximum likelihood phylogenetic analyses on a concatenated dataset of mitochondrial (12S rRNA, 16S rRNA, and tRNAval) and nuclear (RAG1 and TYR) gene fragments. Our analyses recovered C. crassiovis to be related to Clinotarsus, Huia, and Meristogenys. The DNA barcodes of the gastromyzophorous tadpoles matched adults from the same sites. Herein, we provide a re-description of adult C. crassiovis and propose “C. kampeni” as a synonym of this species. The molecular evidence, morphological features, and distribution suggest the presence of two related new species. The two new species and C. crassiovis together represent a distinct phylogenetic clade possessing unique molecular and morphological synapomorphies, thus warranting a new genus.[/vc_column_text][vc_empty_space][vc_separator css=”.vc_custom_1624528584150{padding-top: 25px !important;padding-bottom: 25px !important;}”][vc_empty_space][megatron_heading title=”Author keywords” size=”size-sm” text_align=”text-left”][vc_column_text][/vc_column_text][vc_empty_space][vc_separator css=”.vc_custom_1624528584150{padding-top: 25px !important;padding-bottom: 25px !important;}”][vc_empty_space][megatron_heading title=”Indexed keywords” size=”size-sm” text_align=”text-left”][vc_column_text]Clinotarsus,Huia,Meristogenys,Molecular systematics,Morphology,Ranidae,Species diversity,Taxonomy[/vc_column_text][vc_empty_space][vc_separator css=”.vc_custom_1624528584150{padding-top: 25px !important;padding-bottom: 25px !important;}”][vc_empty_space][megatron_heading title=”Funding details” size=”size-sm” text_align=”text-left”][vc_column_text][{‘$’: ‘gemeinschaft (DFG Ha2323/12-1) and by a stipend for U. Arifin provided by the Deutscher Academischer Aus-tauschdienst–Indonesian German Scholarship Program (DAAD–IGSP, 91548731). Some parts of the study were funded by the National Science Foundation (NSF) DEB-1146324 to E. N. Smith and M. B. Harvey, Volkswagen Foundation (I/79 405) to A. Haas, and Rufford Small Grants (RSG) 15779-1 to U. Smart. The Synthesis of Systematic Resources Access program (SYNTHESYS; NL-TAF-4882 and GB-TAF-4412) supported U. Arifin during examination of type specimens and other materials. The authors thank the School of Life Sciences-Institute of Technology Bandung, Indonesian Science Institute, RISTEK, Director General KKH–PHKA as well as Balai Besar Taman Nasional Gunung Leuser (BBTNGL), Balai Besar Taman Nasional Kerinci-Seblat (BBTNKS), Balai Taman Nasional Batang Gadis (BTNBG) and all Balai Konservasi Sumber Daya Alam (BKSDA) in Sumatra which made this research possible. Permits for research and collecting (SIP) in Sumatra and Java were kindly provided by RISTEK to E. N. Smith and team during the years 2013 to 2016: 149–150/SIP/FRP/SM/V/2013, 152/ SIP/FRP/SM/V/2013, 149-A/SIP/FRP/SM/XII/2013, 151-A/SIP/FRP/SM/XII/2013, 153–154-A/SIP/FRP/SM/ XII/2013, 193–197/SIP/FRP/SM/Vl/2015, and 209–210/ SIP/FRP/SM/Vl/2015. For U. Arifin and team, research and collecting permit were kindly provided by Ministry of Forestry, Directorate General of Forest Protection and Nature Conservation: SI.10/Set-3/2014 and SI.298/Set-3/2014, S.49/KKH-2/2014, S.825/KKH-2/2014. We thank Ester Dondorp (Naturalis Biodiversity Center, Leiden) and Jeff Streicher (Natural History Museum, London) for their support during work of U. Arifin at both museums. We are grateful to Jamili Nais, Director of Research Sabah Parks, Economic Planning Unit, Prime Ministers department, Malaysia, for issuing collecting permit and providing essential help to A. Haas and team. We thank the Sarawak Forest Department and Sarawak Forestry Corporation, in particular Nur Afiza Binti Umar, Dayang Nuriza Binti Abang Abdillah, Mohamad bin Kohdi, En-gkamat Anak Lading Datu Haji Ali Yusop and Mohd. Shabudin Sabki, for providing advice and issuing permits to S.T. Hertwig and A. Haas: NCCD.907.4.4(Jld.VI)-107, Park Permit 56/2011, export permit 09813. We thank Jim- my McGuire, David Bickford, and Jens Vindum for tissue samples, and Andri Irawan for specimen materials. We are very grateful to Ganjar Cahyadi, Novari Fajria, Amir Ha-midy, Agus Yasin, Yoghi Budianto, Zainal, Kamarudin, Carmidi, Hajidin, Zamrin, Agusman, Aidil, Zainudin, Rikha, Sumarto, Darlizon, Muhardi, Samin, Hasbalah, Alfian, Adrinaldi, Abdullah, Mistar Kamsi, Dewi Roes-ma, Risky Dharma, Ari Arfama, David Gusman, Preddy Syahputra, Mantra Sanjaya, Dr. Nia Kurniawan and his group of herpetology students at Brawijaya University and many other people for all support during field work in Sumatra and Java. Annamarie Vogt, Dimitrij Trovin-ov, Katharina Gebauer, and Manuel Schweizer provided excellent support in the lab, and Lea Waser provided the illustration for morphological measurement. Ulrich Man-they kindly provided literature. David McLeod and two other anonymous reviewers for reviewing our manuscript.’}, {‘$’: ‘This study was funded by the Deutsche Forschungs-‘}, {‘$’: ‘This study was funded by the Deutsche Forschungsgemeinschaft (DFG Ha2323/12-1) and by a stipend for U. Arifin provided by the Deutscher Academischer Austauschdienst-Indonesian German Scholarship Program (DAAD-IGSP, 91548731). Some parts of the study were funded by the National Science Foundation (NSF) DEB-1146324 to E. N. Smith and M. B. Harvey, Volkswagen Foundation (I/79 405) to A. Haas, and Rufford Small Grants (RSG) 15779-1 to U. Smart. The Synthesis of Systematic Resources Access program (SYNTHESYS; NLTAF-4882 and GB-TAF-4412) supported U. Arifin during examination of type specimens and other materials. The authors thank the School of Life Sciences-Institute of Technology Bandung, Indonesian Science Institute, RISTEK, Director General KKH-PHKA as well as Balai Besar Taman Nasional Gunung Leuser (BBTNGL), Balai Besar Taman Nasional Kerinci-Seblat (BBTNKS), Balai Taman Nasional Batang Gadis (BTNBG) and all Balai Konservasi Sumber Daya Alam (BKSDA) in Sumatra which made this research possible. Permits for research and collecting (SIP) in Sumatra and Java were kindly provided by RISTEK to E. N. Smith and team during the years 2013 to 2016: 149-150/SIP/FRP/SM/V/2013, 152/SIP/FRP/SM/V/2013, 149-A/SIP/FRP/SM/XII/2013, 151-A/SIP/FRP/SM/XII/2013, 153-154-A/SIP/FRP/SM/XII/2013, 193-197/SIP/FRP/SM/Vl/2015, and 209-210/SIP/FRP/SM/Vl/2015. For U. Arifin and team, research and collecting permit were kindly provided by Ministry of Forestry, Directorate General of Forest Protection and Nature Conservation: SI.10/Set-3/2014 and SI.298/Set-3/2014, S.49/KKH-2/2014, S.825/KKH-2/2014. We thank Ester Dondorp (Naturalis Biodiversity Center, Leiden) and JeffStreicher (Natural History Museum, London) for their support during work of U. Arifin at both museums. We are grateful to Jamili Nais, Director of Research Sabah Parks, Economic Planning Unit, Prime Ministers department, Malaysia, for issuing collecting permit and providing essential help to A. Haas and team. We thank the Sarawak Forest Department and Sarawak Forestry Corporation, in particular Nur Afiza Binti Umar, Dayang Nuriza Binti Abang Abdillah, Mohamad bin Kohdi, Engkamat Anak Lading Datu Haji Ali Yusop and Mohd. Shabudin Sabki, for providing advice and issuing permits to S.T. Hertwig and A. Haas: NCCD.907.4.4(Jld. VI)-107, Park Permit 56/2011, export permit 09813. We thank Jimmy McGuire, David Bickford, and Jens Vindum for tissue samples, and Andri Irawan for specimen materials. We are very grateful to Ganjar Cahyadi, Novari Fajria, Amir Hamidy, Agus Yasin, Yoghi Budianto, Zainal, Kamarudin, Carmidi, Hajidin, Zamrin, Agusman, Aidil, Zainudin, Rikha, Sumarto, Darlizon, Muhardi, Samin, Hasbalah, Alfian, Adrinaldi, Abdullah, Mistar Kamsi, Dewi Roesma, Risky Dharma, Ari Arfama, David Gusman, Preddy Syahputra, Mantra Sanjaya, Dr. Nia Kurniawan and his group of herpetology students at Brawijaya University and many other people for all support during field work in Sumatra and Java. Annamarie Vogt, Dimitrij Trovinov, Katharina Gebauer, and Manuel Schweizer provided excellent support in the lab, and Lea Waser provided the illustration for morphological measurement. Ulrich Manthey kindly provided literature. David McLeod and two other anonymous reviewers for reviewing our manuscript.’}][/vc_column_text][vc_empty_space][vc_separator css=”.vc_custom_1624528584150{padding-top: 25px !important;padding-bottom: 25px !important;}”][vc_empty_space][megatron_heading title=”DOI” size=”size-sm” text_align=”text-left”][vc_column_text]https://doi.org/10.3897/zse.94.22120[/vc_column_text][/vc_column_inner][vc_column_inner width=”1/4″][vc_column_text]Widget Plumx[/vc_column_text][/vc_column_inner][/vc_row_inner][/vc_column][/vc_row][vc_row][vc_column][vc_separator css=”.vc_custom_1624528584150{padding-top: 25px !important;padding-bottom: 25px !important;}”][/vc_column][/vc_row]