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Revision of the Hillstream Lizard Loaches, Genus Balitoropsis (Cypriniformes: Balitoridae)

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Revision of the Hillstream Lizard Loaches, Genus Balitoropsis (Cypriniformes: Balitoridae) Zootaxa 3962 (1): 206–225 ISSN 1175-5326 (print edition) www.mapress.com/zootaxa/ Article ZOOTAXA Copyright © 2015 Magnolia Press ISSN 1175-5334 (online edition) http://dx.doi.org/10.11646/zootaxa.3962.1.13 http://zoobank.org/urn:lsid:zoobank.org:pub:FBCF7375-8ADD-4624-9DD8-1A5427B5FB9A Revision of the hillstream lizard loaches, genus Balitoropsis (Cypriniformes: Balitoridae) ZACHARY S. RANDALL & PATRICK A. RIGGS Florida Museum of Natural History, University of Florida, Dickinson Hall, Gainesville, FL 32611, USA. Email: [email protected] Abstract The genus Balitoropsis Smith 1945 consists of two species, B. zollingeri (Bleeker 1853) and B. ophiolepis (Bleeker 1853). Homaloptera maxinae Fowler 1937, Balitoropsis bartschi Smith 1945, and Homaloptera nigra Alfred 1969 are junior synonyms of B. zollingeri. Balitoropsis zollingeri has been reported from Thailand, Laos, Cambodia, Malay Peninsula, Sumatra, Java, and Borneo, and B. ophiolepis is known from Sumatra, Java, and Borneo. Keywords: Homaloptera zollingeri, Homaloptera ophiolepis, Balitoropsis bartschi, Homaloptera maxinae, Homaloptera nigra, Southeast Asia Introduction Randall and Page (2015) distinguished Balitoropsis from related genera, Homaloptera, Homalopteroides, Pseudohomaloptera, and Homalopterula, based on the nuclear recombination activating gene 1 (RAG1) and morphological characters, recognizing only two species in Balitoropsis: Homaloptera zollingeri Bleeker 1853 and H. ophiolepis Bleeker 1853. This classification includes fewer species in Balitoropsis than previously recognized (Kottelat 2012, 2013), and the objective of the present study was to use morphological and molecular data to assess the status of species synonymized with H. zollingeri: Homaloptera maxinae Fowler 1937, Balitoropsis bartschi Smith 1945, and Homaloptera nigra Alfred 1969. Materials and Methods Morphological. Measurements follow Hubbs and Lagler (2004) or Kottelat (1984); see Randall & Page (2012) for measurements from each source. Counts follow Randall and Page (2014). The terms “origin” and “insertion” refer, respectively, to the anterior and posterior ends of fin bases for both paired and unpaired fins. Lengths were measured to the nearest 0.1 mm using digital calipers and taken on the left side when possible. All measurements are given in millimeters (mm). Head length and measurements of the body are given as proportions of standard length (SL). Measurements of the head are presented as proportions of head length (HL), and eye length as a proportion of interorbital width (IO). Institutional abbreviations follow Sabaj Pérez (2012). When coordinates were unavailable, they were estimated using maps and GEOLocate. Maps were constructed using ArcMap10. Molecular. To test the monophyly of populations identified morphologically as Balitoropsis zollingeri, a molecular analysis of the mitochondrial cytochrome c oxidase subunit 1 gene (COI) was performed based on recently collected tissues (Table 1) and sequences available on Genbank (Balitora brucei [accession # KJ774109.1], Gastromyzon sp. [accession # JN646091.1], Metahomaloptera omeiensis [accession # JN177080.1]). Total genomic DNA was extracted from fin clips or muscle tissue preserved in 95% ethanol using a DNeasy Tissue Kit (Qiagen). COI was amplified and sequenced using the primers FISH-BCL: 5’–TCA ACY AAT CAY AAA GAT ATY GGC AC–3’ and FISH-BCH_R: 5’–ACT TCY GGG TGR CCR AAR AAT CA–3’ (Baldwin et al., 2009). 206 Accepted by R. L. Mayden: 29 Mar. 2015; published: 22 May 2015 Licensed under a Creative Commons Attribution License http://creativecommons.org/licenses/by/3.0 Revision of of Revision Balitoropsis TABLE 1. Samples produced from this study included in phylogenetic analysis. Genus Species Vial # Voucher Origin (region, province, river) Genbank accession # Balitoropsis ophiolepis 2006-0588 UF 166109 Sumatra, Lampung, Way Besai KR052868 zollingeri 2005-0948 UF 161715 Sumatra, Lampung, Way Rarem KR052865 2005-0962 UF 161715 Sumatra, Lampung, Way Rarem KR052864 KR052867 2006-0591 UF 166105 Sumatra, Lampung, Way Besai 2012-0167 UF 183727 Thailand, Nakhon Si Thammarat, Tha Di KR052871 KR052870 2012-0583 UF 235547 Malaysia, Kelantan, Kelantan Zootaxa KR052869 2012-0587 UF 235547 Malaysia, Kelantan, Kelantan 3962 (1) © 2015 Magnolia (1)©2015 Press 3962 2012-0598 UF 235547 Malaysia, Kelantan, Kelantan KR052866 Homaloptera ocellata 2005-0980 UF 161605 Sumatra. Lampung, Way Abung KR052873 Pseudohomaloptera leonardi 2012-0597 UF 235746 Malaysia, Kelantan, Kelantan KR052872 · 207 Reactions for the polymerase chain reaction (PCR) followed Randall and Page (2015). The PCR cycling parameters followed Parenti et al. (2013). PCR cleaning with ExoSAP-IT and sequencing took place at the Interdisciplinary Center for Biotechnology Research, University of Florida, Gainesville, FL, USA. Geneious 7.1.4 (Kearse et al. 2012) was used to view chromatograms, assemble consensus sequences, and generate a final alignment using the Geneious global alignment tool. The final alignment was corrected manually. A Bayesian Inference (BI) analysis using MrBayes 3.2.2 (Ronquist et al. 2012) and a Maximum Likelihood (ML) analysis using RAxML 7.2 (Stamatakis 2014) were performed through the Cyberinfrastructure for Phylogenetic Research (CIPRES) (Miller et al. 2010). For the BI analysis, model selection was restricted to those available in MrBayes, where the HKY+I+G was the best fit substitution model of nucleotide evolution for COI using the Akaike Information Criterion with JModeltest version 2.1.5 (Darriba et al. 2012). Two Markov chain Monte Carlo (MCMC) analyses with four simultaneous chains were run for 5 million generations sampling every 1,000 generations resulting in 10,002 sampled trees. The standard deviation for split frequencies was 0.003512 and the average potential scale reduction factor for all parameters was 1.001, indicating convergence of the two runs; 25% of the first sampled trees were discarded as burn-in, leaving 7,502 trees. The best tree was viewed in Figtree v. 1.3.1 (http://tree.bio.ed.ac.uk/software/figtree/). The ML analysis procedure followed Randall and Page (2015). Gastromyzon a member of the gastromyzonins, sister group to balitorins (Randall & Page 2015), was used to root the gene trees for both BI and ML analyses. FIGURE 1. Balitorid phylogeny based on Bayesian analysis of CO1. Support values are indicated at the branch lengths (pp/ bs). Posterior probability values ≥ 0.95 and bootstrap support ≥ 90 are represented by an asterisk (*). Support values ≤ 50 are represented by a hyphen (-). M) peninsular Malaysia; S) Sumatra; T) Thailand. Phylogenetic Results The BI and ML analyses generated an identical topology which is represented in Figure 1 by the BI analysis (greater likelihood score of -2360.32). Balitoropsis was monophyletic and the sister group to other genera of balitorini included in the analysis (Balitora, Homaloptera, Metahomaloptera, Pseudohomaloptera). Balitoropsis 208 · Zootaxa 3962 (1) © 2015 Magnolia Press RANDALL & RIGGS zollingeri was monophyletic with shallow branch divergences among the three populations sampled (peninsular Malaysia, Sumatra, and Thailand). The Thailand population is sister group to the peninsular Malaysian population with weak support. The population from Sumatra is sister group to the other populations with strong support. Only the population from Sumatra is strongly supported as monophyletic in both analyses. The population from peninsular Malaysia is only strongly supported by the ML analysis. FIGURE 2. Dorsal, lateral, and ventral views of holotype of Homaloptera maxinae, ANSP 68004, 34.3 mm SL; Tachin (Samut Sakhon), Thailand. Balitoropsis Smith 1945 Lizard loaches Balitoropsis Smith, 1945:278. (type species: Balitoropsis bartschi Smith 1945:279, by original designation). Gender fem- inine. Systematic History. Balitoropsis was created for B. bartschi Smith (1945) based on having papillated lips and a deep preoral groove extending around the corners of the mouth. However, papillated lips (unculi) and a preoral groove are common characters in balitorid genera, and the genus was recognized as a junior synonym of Homaloptera van Hasselt 1823 by Kottelat & Chu (1988). Balitoropsis was recognized as a subgenus of Homaloptera by Tan & Ng (2005) and Randall & Page (2012) and as a genus consisting of 10 species by Kottelat (2012) and of 9 species by Kottelat (2013). Randall & Page (2015) recognized Balitoropsis as a genus consisting of 2 species based on molecular and morphological data. Revision of Balitoropsis Zootaxa 3962 (1) © 2015 Magnolia Press · 209 210 · Zootaxa 3962 (1) ©2015 (1) 3962 TABLE 2. Morphometrics and meristics for holotype of Homaloptera maxinae, ANSP 68004; holotype and paratypes of Homaloptera nigra, ZRC 2009, CAS-SU 66424 (2); and Balitoropsis zollingeri, BMNH 1866.5.2.53 (Bleeker specimen) (1), other material examined (31). All measurements in mm. Number of individuals with a value shown in parentheses. * denotes meristic counts for holotype. MORPHOMETRICS H. maxinae H. nigra B. zollingeri Range Mean±%SD BMNH Range Mean±%SD 1866.5.2.53 Standard Length 34.3 45.3-57.0 57.9 27.3-67.7 Magnolia Press Total Length 40.7 54.5-61.9 35.0-86.4 % of Standard Length Lateral head length 23.1 22.5-25.9 24.0±1.8 25.4 20.8-26.7 23.4±1.3 Body depth 15.0 14.8-16.0 15.3±0.6 13.6 13.7-17.6 15.1±0.8 Body width 14.5 13.2-16.0 14.6±1.9 15.5 12.3-18.5 14.9±1.5 Distance from pelvic fin to anal fin 30.9 30.7-31.6 31.1±0.4 33.5 27.0-32.2 30.5±1.3 Dorsal-fin base length 14.5 13.2-15.2 14.3±1.0 13.0
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