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Description of a New Species of Moenkhausia (Characiformes: Characidae) from the Upper Paraguay Basin, Central Brazil, with Comments on Its Phylogenetic Relationships

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Description of a New Species of Moenkhausia (Characiformes: Characidae) from the Upper Paraguay Basin, Central Brazil, with Comments on Its Phylogenetic Relationships Neotropical Ichthyology, 16(2): e170086, 2018 Journal homepage: www.scielo.br/ni DOI: 10.1590/1982-0224-20170086 Published online: 16 July 2018 (ISSN 1982-0224) Copyright © 2018 Sociedade Brasileira de Ictiologia Printed: 30 June 2018 (ISSN 1679-6225) Original article Description of a new species of Moenkhausia (Characiformes: Characidae) from the upper Paraguay basin, Central Brazil, with comments on its phylogenetic relationships Ricardo Britzke1, 2, Waldo P. Troy3, Claudio Oliveira1 and Ricardo C. Benine4 A new species of Moenkhausia is described from tributaries of the upper rio Sepotuba, Paraguay basin, Brazil. The new species is distinguished from its congeners by a combination of characters, including an inconspicuous oval-shaped vertically elongated humeral blotch, extending horizontally from third through five lateral-line scales, and vertically from third row above lateral line to first row below it, followed by a diffuse field of dark chromatophores in the flank, combined with a well- defined dark line at the base of the anal fin. Furthermore, the phylogenetic position of the new species is presented based on molecular data, showing a close relationship among species of Moenkhausia and Hemigrammus that have a well-defined dark line at the base of the anal fin. Until this moment, this species is only known from in the upper rio Sepotuba basin. Keywords: Hemigrammus, Molecular phylogeny, Neotropical tetras, Taxonomy. Uma nova espécie de Moenkhausia é descrita nos afluentes do rio Sepotuba, bacia do Paraguai, no Brasil. A nova espécie se distingue dos seus congêneres por uma combinação de caracteres, incluindo uma mancha umeral discreta de forma oval, alongada verticalmente, que se estende horizontalmente da terceira a quinta escamas da linha lateral e, verticalmente, da terceira fila de escamas acima da linha lateral até a primeira fila abaixo da linha lateral; seguida por escassos cromatóforos no flanco, combinado com uma linha escura bem definida na base da nadadeira anal. Além disso, a posição filogenética da nova espécie é apresentada com base em dados moleculares, mostrando um relacionamento próximo entre as espécies de Moenkhausia e Hemigrammus que possuem uma linha escura bem definida na base da nadadeira anal. Até o momento, essa espécie é conhecida apenas da bacia do Alto Sepotuba. Palavras-chave: Filogenia Molecular, Hemigrammus, Taxonomia, Tetras Neotropical. Introduction Géry, 1977; Fink, 1979; Costa, 1994; Weitzman, Palmer, 1997; Lucena, Lucena, 1999; Lima, Toledo-Piza, 2001; The genus Moenkhausia Eigenmann basically differs Benine, 2002; 2004; Benine et al., 2009; Lima, Sousa, 2009; from Hemigrammus Gill by possessing a completely pored Lima et al., 2007; Ota et al., 2014) even though not based on lateral line (vs. an incompletely pored lateral line in the tested hypothesis of phylogenetic relationships. In an attempt latter) (Eigenmann, Myers, 1917; Géry, 1977). However, to test the monophyly of the Characidae, Mirande (2010) several species have been described on Moenkhausia despite and Oliveira et al. (2011) found Moenkhausia xinguensis the fact of possessing incomplete or interrupted lateral lines (Steindachner, 1882) and Hemigrammus unilineatus (e.g. M. pyrophthalma Costa, 1994; M. diktyota Lima & Toledo- (Gill, 1858), the type species of both genera, to be more Piza, 2001; M. forestii Benine, Mariguela & Oliveira, 2009). closely related to species of Hasemania, Hyphessobrycon, The non-monophyletic condition of these genera has long Paracheirodon, Pristella, and Thayeria, evidencing their been discussed by several authors since their proposition (e.g. non-monophyletic condition. 1Departamento de Morfologia, Instituto de Biociências, Universidade Estadual Paulista (IBB-UNESP), R. Prof. Dr. Antonio C. W. Zanin, s/n, Rubião Jr, 18618-689 Botucatu, São Paulo, Brazil. (RB) [email protected], https://orcid.org/0000-0002-1042-2544 (corresponding autor), (CO) [email protected] 2Universidad Técnica de Machala, Unidad Académica de Ciencias Agropecuarias, Km. 41/2 Vía Machala-Pasaje. 070150. Machala, El Oro, Ecuador. 3Departamento de Ciências Biológicas, Universidade do Estado de Mato Grosso - Campus de Tangará da Serra, 78300-000 Tangará da Serra, MT, Brazil. [email protected] 4Departamento de Zoologia, Instituto de Biociências, Universidade Estadual Paulista (IBB-UNESP), R. Prof. Dr. Antonio C. W. Zanin, s/n, Rubião Jr, 18618-689 Botucatu, São Paulo, Brazil. [email protected] e170086[1] Neotropical Ichthyology, 16(2): e170086, 2018 2 New species of Moenkhausia from the upper Paraguay Mariguela et al. (2013) presented a phylogenetic Molecular data. The present study included 30 species analysis including 29 species out of the 91 current valid currently allocated in Moenkhausia, including the new species of Moenkhausia (Eschmeyer et al., 2017). Their species. As a framework for the selection of species to be results showed that representatives of this genus appeared included in our analysis we follow the results presented in distributed in five different clades related to genera such Oliveira et al. (2011), selecting representatives of their node as Bario, Hemigrammus, Hasemania, Nematocharax, 31, which includes the Acestrorhynchidae, Bryconidae, Aphyodite, Parecbasis, and also with members of the Chalceidae, Characidae, Gasteropelecidae, Iguanodectidae, subfamily Stethaprioninae. and Triportheidae. Despite of these recent efforts in trying to identify the sister species of Moenkhausia xinguensis and Molecular methods. Total DNA was extracted from Hemigrammus unilineatus, and propose a phylogenetic ethanol preserved muscle samples using DNeasy Tissue definition for both genera, the low number of taxa included Extraction Kit (Qiagen), following manufacturer’s in those analyses, along with the lack of understanding of instructions. Partial sequences of the genes 16SrRNA, closely related, species-rich genera such as Astyanax and Cytochrome b (Cytb), recombination activating gene Hyphessobrycon, has precluded a more consistent and 1 (Rag1), recombination activating gene 2 (Rag2), and useful definition for these and other characid genera. Myosin, heavy chain 6, cardiac muscle, alpha (Myh6) were Collecting efforts in headwater streams of the upper amplified by polymerase chain reaction (PCR) with the same rio Sepotuba, rio Paraguay basin, revealed an undescribed primers utilized by Oliveira et al. (2011). Amplifications species of small characin that, despite of its similarity were performed in a total volume of 25 ml with 2.5 ml of to species of Hemigrammus, such as H. lunatus, would 10X buffer (10mM Tris-HCL + 15mM MgCl2 buffer), 0.5 better fit to the artificial and traditional definition of ml MgCl2, 0.5 ml each primer (5 mM); 0.4 ml dNTPs (200 Moenkhausia, since it has a completely pored lateral nM of each), 0.2 ml Taq Platinum polymerase (Invitrogen), line. Herein, we present a phylogenetic analysis based 1 ml template DNA (10-50ng) and 19.4 ml ddH2O. The on molecular data to infer and discuss its phylogenetic thermo-cycler profile used for the fragments 16SrRNA relationships within Characidae and formally describe and Cyt b was with 35 cycles and annealing temperature this new species. of 50-55oC. Nested-PCR was used to amplify the nuclear genes rag1, rag2, and Myh6. Conditions for amplification Material and Methods of these genes for both rounds of PCR used 15 cycles with annealing temperature at 56oC followed by 15 cycles Morphological data. Counts and measurements followed with annealing temperature at 54oC. PCR products were Fink, Weitzman (1974), except for counts of scale rows, purified using ExoSap-IT® (USB Corporation), sequenced which follow Lima et al. (2007) and with the addition of using the “Big DyeTM Terminator v 3.1 Cycle Sequencing pelvic-fin origin to anal-fin origin measured at origin of Ready Reaction Kit” (Applied Biosystems), purified pelvic-fin through the anal-fin origin. again by ethanol precipitation and loaded on an automatic Measurements were taken point to point with a digital sequencer 3130-Genetic Analyzer (Applied Biosystems) at caliper on the left side of specimens whenever possible Instituto de Biociências, Universidade Estadual Paulista, (precision of 0.1 mm). All measurements are expressed as Botucatu, São Paulo, Brazil. percentage of standard length (SL) or head length (HL). Values in the parentheses indicate the number of specimens Alignment and phylogenetic analyses. Contigs were with a particular count and an asterisk indicates values of assembled and edited in Geneious v 5.4 software (Kearse the holotype. Vertebrae of the Weberian apparatus were et al., 2012). Sequences were independently aligned counted as four elements and the fused PU1+U1 as a using the muscle algorithm under default parameters single element. Vertebrae, supraneural counts and gill- (Edgar, 2004), and alignments were inspected for any rakers of first arch were taken from seven cleared and problems. The first alignments were initially analyzed by stained (cs) specimens prepared following the method of neighbour-joining (NJ) using MEGA 7.0 software (Kumar Taylor, Van Dyke (1985). et al., 2016) to control potential sequencing errors. The Institutional abbreviations used are as follows: sequences were translated using Geneious v 5.4 (Kearse Laboratório de Biologia e Genética de Peixes (LBP), et al., 2012) to check for the unexpected occurrence Universidade Estadual Paulista, Botucatu, Brazil; of stop codons. PartitionFinder v1.1.1 (Lanfear et al., Museo de Ciencias Naturales de Guanare (MCNG),
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