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Systematic Revision of Microhyla (Microhylidae) Frogs of South Asia: a Molecular, Morphological, and Acoustic Assessment

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Systematic Revision of Microhyla (Microhylidae) Frogs of South Asia: a Molecular, Morphological, and Acoustic Assessment 69 (1): 1 – 71 © Senckenberg Gesellschaft für Naturforschung, 2019. 27.2.2019 Systematic revision of Microhyla (Microhylidae) frogs of South Asia: a molecular, morphological, and acoustic assessment Sonali Garg 1 , Robin Suyesh 1, 2, Abhijit Das 3 , Jianping Jiang 4 , Nayana Wijayathilaka 5, 6, A. A. Thasun Amarasinghe 7 , Farits Alhadi 1 , Kumar K. Vineeth 8 , N. A. Aravind 9 , Gayani Senevirathne 10, 6, Madhava Meegaskumbura 11, 6 & S. D. Biju 1, * 1 Systematics Lab, Department of Environmental Studies, University of Delhi, Delhi, India — 2 Sri Venkateswara College, University of Delhi, Delhi, India — 3 Wildlife Institute of India (WII), Dehradun, India — 4 Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China — 5 Department of Zoology, Faculty of Applied Sciences, University of Sri Jayewardenepura, Sri Lanka — 6 Department of Molecular Biology and Biotechnology, Faculty of Science & Postgraduate Institute of Science, University of Peradeniya, Sri Lanka — 7 Research Centre for Climate Change, University of Indonesia, Depok, Indonesia — 8 Department of Applied Zoology, Mangalore University, Mangaluru, India — 9 Ashoka Trust for Research in Ecology and the Environment (ATREE), Bengaluru, India — 10 Department of Organismal Biology & Anatomy, University of Chicago, IL, USA — 11 Guangxi Key Laboratory of Forest Ecology and Conservation, College of Forestry, Guangxi University, Nanning, China — * Corresponding author: [email protected] Submitted May 28, 2018. Accepted November 23, 2018. Published online at www.senckenberg.de/vertebrate-zoology on December 18, 2018. Published in print on February 27, 2019. Editor in charge: Raffael Ernst Abstract This study presents a systematic revision of South Asian members of the taxonomically challenging genus Microhyla Tschudi, 1838. Species relationships and diagnostic characters are determined by integrating molecular, morphological, and acoustic approaches, through which we also recognize six groups of closely related species. In addition, a new species from the southern Western Ghats of India is formally described as Microhyla darreli sp. nov. Species accounts of all the 16 recognized members from South Asia include current taxonomic status, metric and meristic characters, divergence in mitochondrial DNA, phylogenetic relationships, acoustic characters, re- vised geographical distributions, and natural history notes. Molecular and morphological relationships of three poorly known members — M. chakrapanii, M. karunaratnei, and M. zeylanica²DUHFODUL¿HGIRUWKH¿UVWWLPHVLQFHWKHLURULJLQDOGHVFULSWLRQV7KHSUHVHQFHRI M. berdmorei and another potential new species close to M. heymonsi in India LVJHQHWLFDOO\FRQ¿UPHGDQGVHYHUDOPLVLGHQWL¿FDWLRQVDUH corrected. For comparative purposes, molecular, morphological, and acoustic relationships are also discussed for eight closely related East and Southeast Asian species. Consequently, insights from this study will facilitate a much-needed comprehensive revision of the Pan-Asian frog genus Microhyla. Key words Amphibians; bioacoustics; cryptic species; diagnostic characters; integrative taxonomy; Microhylidae; molecular phylogeny; morphology; species groups; new species. Introduction The genus Microhyla Tschudi, 1838 (family Microhyli- ing frogs that are widely distributed in South, Southeast, dae) currently comprises of 42 small to medium-sized and East Asia. It is also the most speciose (AMPHIBIAWEB, (SVL 10 – 46 mm), narrow-mouthed, and ground-dwell- 2018; FROST, 2018) and wide-ranging genus of the Asian ISSN 1864-5755 | eISSN 2625-8498 | DOI: 10.26049/VZ69-1-2019-01 1 Garg, S. et al.: Systematic revision of Microhyla (Microhylidae) frogs of South Asia subfamily Microhylinae (MATSUI et al., 2011). Species accommodating all South Asian members. Additionally, in this genus usually occupy habitats ranging from nat- relationships with close congeners from Southeast and ural forests to human-altered landscapes. Despite com- East Asia are discussed based on comparative material mon occurrence, genus Microhyla has remained one of from outside the range to facilitate systematic conclu- the most challenging taxonomical group of microhylid sions. frogs, mainly because of the small size, conserved mor- phology, and wide distribution of its members across Asia (e.g., MATSUI et al., 2005, 2011). In recent years, WKHXVHRIPROHFXODUGDWDKDVVLJQL¿FDQWO\DLGHGGHOLQHD- Materials and methods tion of known taxa (e.g., MATSUI et al., 2005, 2011; MAT- SUI, 2011; HASAN et al., 2012; YUAN et al., 2016; GARG et al., 2018A DQGLGHQWL¿FDWLRQRIQHZFU\SWLFVSHFLHV Field surveys and data collection (MATSUI, 2011; MATSUI et al., 2013; HASAN et al., 2014A; HOWLADER et al., 2015; WIJAYATHILAKA et al., 2016; SE- )URJVZHUHVDPSOHGGXULQJ¿HOGVXUYH\VFRQGXFWHGEH- SHADRI et al., 2016A; KHATIWADA et al., 2017), leading to a tween 2002 – 2017 at over 90 localities across India and continuous increase in the number of recognized Micro- Sri Lanka in South Asia, and Indonesia in Southeast hyla species. However, lack of molecular information for Asia. Detailed list of species and localities surveyed in several known species (at least 13 species), continues to the present study along with taxa incorporated from pre- deter a thorough taxonomic revision of this group. The vious studies are provided in Table S1. Adult specimens latest available systematic study addressing species from and larvae were mostly sampled during the breeding WKHHQWLUHNQRZQUDQJHRIWKHJHQXVSURYLGHGVLJQL¿FDQW season, from May to September; random opportunistic insights on phylogenetic relationships among Microhyla searches were also conducted outside this period. Adult frogs (MATSUI et al., 2011); however, the South Asian males were often located by their advertisement calls. members remained poorly represented, i.e., only two out Calls were recorded using a Marantz PMD620 or Fostex of six formerly known regional endemics (from the coun- FR2LE solid-state digital recorder (44.1 kHz sampling tries of Bangladesh, Bhutan, India, Nepal, Pakistan, and rate, 16-bit resolution) with Sennheiser ME66 or MKH Sri Lanka). Furthermore, subsequent research has dou- 416 unidirectional microphone. One specimen from each bled the number of Microhyla species occurring in South of the recorded populations was collected for morpholog- Asia (HASAN et al., 2014A; HOWLADER et al., 2015; WIJA- LFDODQGJHQHWLFLGHQWL¿FDWLRQ6DPSOHGLQGLYLGXDOVZHUH YA THILAKA et al., 2016; SESHADRI et al., 2016A; KHATIWADA photographed, followed by euthanisation in Tricaine et al., 2017; VINEETH et al., 2018), consequently elevating PHWKDQHVXOSKRQDWH 06 VROXWLRQ ¿[DWLRQ LQ the prominence of this region for Microhyla diversity. IRUPDOLQDQGSUHVHUYDWLRQLQHWKDQRO7LVVXHVDP- The taxonomy of South Asian Microhyla has also ples for molecular studies were obtained from the thigh EHHQLQDVWDWHRIÀX[8QWLOUHFHQWO\ORQJVWDQGLQJFRQ- (adult) or tail (tadpole) muscle and preserved in absolute IXVLRQV FRQFHUQLQJ LGHQWL¿FDWLRQ DQG UDQJH GHOLQHDWLRQ ethanol. Geographical coordinates were recorded using existed for many species, including some of the oldest a Garmin 76CSx GPS with the WGS84 datum system. known members such as Microhyla ornata (Duméril Distribution maps were prepared in QGIS version 2.6.1 & Bibron, 1841), M. rubra (Jerdon, 1854 “1853”), and (http://www.qgis.org). Type specimens from the present M. sholigari Dutta & Ray, 2000 (MATSUI et al., 2005; study are deposited in the Zoological Survey of India – WIJAYATHILAKA et al., 2016; SESHADRI et al., 2016B; GARG Western Ghats Regional Centre (ZSI-WGRC), Calicut, et al., 2018A). The systematic relationships of three other India. species — M. chakrapanii Pillai, 1977, M. karunaratnei Fernando & Siriwardhane, 1996, and M. zeylanica Park- er & Osman-Hill, 1949 — are still unknown. Moreover, Molecular study recent species descriptions largely include literature- based comparisons with closely related congeners (e.g., Extraction of genomic DNA from 48 tissue samples was HASAN et al., 2014A; SESHADRI et al., 2016A; VINEETH et carried out using DNeasy blood and tissue kit (Qiagen, al., 2018), lacking attempts to study available types, mu- 9DOHQFLD&$86$ IROORZLQJWKHPDQXIDFWXUHU¶VSUR- seum specimens, or new collections from original type tocol. For all the samples, a fragment of ca. 540 bp of the localities. Hence altogether, the South Asian Microhyla mitochondrial (mt) 16S ribosomal RNA gene (16S) was frogs remain poorly understood. 3&5DPSOL¿HG XVLQJ VWDQGDUG SURWRFROV DQG WKH SULP- In this work, we study all the known Microhyla spe- er set 16Sar and 16Sbr previously published by SIMON cies of South Asia based on an integrated molecular, et al. (1994). Additionally, a fragment of ca. 700 bp of morphological, and acoustic assessment; this utilized the nuclear (nu) brain derived neurotrophic factor gene QHZO\REWDLQHGSULPDU\GDWDIURP¿HOGZRUNDQGVWXG\ %'1) ZDVDPSOL¿HGXVLQJWKHSULPHUVHW%'1)$PS of available types and additional museum specimens. F1 and BDNF.Amp.R1 (VAN DER MEIJDEN et al., 2007) Our study also uncovers a new Microhyla species from for selected taxa representing all known and newly rec- India, provides insights on poorly known taxa, presents ognized South Asian Microhyla species (Table S1). Se- new distribution records, and recognizes species groups quencing was performed on both strands using BigDye 2 VERTEBRATE ZOOLOGY — 69 (1) 2019 Terminator v3.1 Cycle Sequencing Kit on ABI 3730 Morphological study automated DNA sequencer (Applied Biosystems). Se- quences were assembled and checked in ChromasPro Adult specimens were
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