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Three New Species of the 'Geophagus' Brasiliensis Species

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Three New Species of the 'Geophagus' Brasiliensis Species Zoosyst. Evol. 94 (2) 2018, 325–337 | DOI 10.3897/zse.94.22685 Three new species of the ‘Geophagus’ brasiliensis species group from the northeast Brazil (Cichlidae, Geophagini) José L. O. Mattos1, Wilson J. E. M. Costa1 1 Laboratory of Systematics and Evolution of Teleost Fishes, Institute of Biology, Federal University of Rio de Janeiro, Rio de Janeiro, Caixa Postal 68049, CEP 21944-970, Rio de Janeiro, Brazil http://zoobank.org/E446D128-9ACA-4CFB-944F-B15492ABFDC2 Corresponding author: José L. O. Mattos ([email protected]); Wilson J. E. M. Costa ([email protected]) Abstract Received 1 December 2017 Morphological characters and phylogenetic trees generated by analyses of segments of Accepted 21 June 2018 two mitochondrial genes cytochrome b and cytochrome c oxidase I support recognition Published 6 July 2018 of three new species of the ‘Geophagus’ brasiliensis species group from coastal basins of northeast Brazil. All new species were diagnosed by exclusive morphological characters Academic editor: and exclusive nucleotide transformations. Geophagus rufomarginatus sp. n., from the Rio Johannes Penner Buranhém Basin, is distinguished from all other species of the group by dorsal-fin lappets with red edges, the presence of longitudinal series of small light blue spots between the Key Words anal-fin spines and rays, and non-denticulated gill-rakers; it is closely related to G. brasil- iensis and G. iporangensis. Geophagus multiocellus sp. n., from the Rio de Contas Basin, Atlantic Forest is distinguished from all other species of the group by having small pale blue spots with Biodiversity hotspot minute bright blue dots at their centres, that are often vertically coalesced to form short bars Molecular phylogeny on the caudal fin. Geophagus santosi sp. n., from the Rio Mariana Basin, is distinguished Neotropical from all other species of the group by having blue stripes parallel to the dorsal and anal fin Systematics rays on their longest portions. Geophagus multiocellus and G. santosi belong to the same Integrative taxonomy clade of G. itapicuruensis. The clade composed by the Rio Paraguaçu Basin species was recovered as the sister group of the other species of the ‘G.’ brasiliensis species group. Introduction occupy a wide range of ecological niches and exhibit remarkable morphological and behavioural adaptations The Atlantic Forest is a biodiversity hotspot biome which (López-Fernández et al. 2013, Arbour and López-Fernán- has suffered degradation and drastic reduction throughout dez 2014). The type genus Geophagus Haeckel, 1940 has the history of human occupation and development of eco- been diagnosed by the morphology of vertebrae, compris- nomic activities (Myers et al. 2000). Consequently, many ing the presence of epipleural ribs on caudal vertebrae, components of its endemic biodiversity are currently which are associated with expansions of the swim blad- under threat of extinction. This South American natural der, and caudal vertebrae more numerous than abdominal province (Morrone 2006) shows a high rate of endemism (Kullander 1986). However, these morphological features in its remaining fragments (Myers et al. 2000), harbor- are not shared by all species of the genus. Presently, the ing some endemic species of freshwater fishes, including genus has been divided into three species groups (Kul- cichlids (Kullander 2003, Lucena and Kullander 2006, lander 1998; López-Fernández and Taphorn 2004). Spe- Ottoni 2013, Ottoni and Costa 2008). cies that fit Kullander’s (1986) generic diagnosis were as- The cichlid tribe Geophagini is broadly distribut- sembled into the Geophagus sensu stricto species group, ed in South America and presents the greatest diversi- which includes the type species of the genus Geophagus ty among tribes of Neotropical cichlids, comprising 15 altifrons Haeckel, 1840 and other species distributed in genera (López-Fernández et al. 2010). Included species northern South America, including the Amazonas, Orino- Copyright José L. O. Mattos, Wilson J. E. M. Costa. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 2 Mattos, J.L.O. & Costa, W.J.E.M.: Three new species of the ‘Geophagus’ brasiliensis species group co and Parnaíba river basins. Nevertheless, two species map was generated using QGIS Geographic Information groups do not have those morphological characteristics: System, Open Source Geospatial Foundation Project, and the ‘Geophagus’ steindachneri species group, with a the information of this map was based on our examined trans-Andean distribution between southern Panama and material and data provided by Mattos et al. 2015. Speci- Maracaibo lake region in Venezuela, and the ‘Geophagus’ mens were euthanized by immersion in a buffered solution brasiliensis species group, geographically widespread of tricaine methane sulphonate (MS-222) at a concentra- in eastern South America, mostly in the Atlantic Forest tion of 250 mg/L, for a period of 10 minutes, following (Kullander 2003, Mattos et al. 2015). Recent phylogenet- the guidelines of the Journal of the American Veterinary ic studies (López-Fernández et al. 2010, Ilves et al. 2017) Medical Association (AVMA Guidelines) (Leary et al. indicate that these three species groups together do not 2013) and European Commission DGXI consensus for form a monophyletic lineage, and consequently, authors fish euthanasia (Close et al. 1996, 1997). Tissue speci- when describing new species of the last two groups have mens for molecular analysis (DNA) were fixed and pre- tentatively assigned them to ‘Geophagus’, thus using the served in absolute ethanol just after collection. genus name between apostrophes to designate their un- certain position (Kullander 1998, López-Fernández et al. Species delimitation 2010, Ilves et al. 2017). The species delimitation methodology followed in this Currently, the ‘G.’ brasiliensis species group com- study aims to fulfil goals of integrative taxonomy. The prises five valid species (Kullander 2003; Mattos et al. character-based methodology for species delimitation 2015): G. iporangensis Haseman, 1911, from the Rio was the Population Aggregation Analysis. It employs a Ribeira do Iguape Basin; G. itapicuruensis Haseman, unique combination of morphological character states 1911, from the Rio Itapicuru Basin; G. obscurus (Castel- to diagnose species. This method of species delimitation nau, 1855), from the coastal section of the Rio Paraguaçu was formally described by Davis and Nixon (1992). Basin (Lucena and Kullander 2006); G. diamantinensis The PAA applied for molecular data in this study Mattos, Costa & Santos, 2015 from the upper section of aimed the unique substitution nucleotide for each gene the Rio Paraguaçu Basin; and ‘G.’ brasiliensis, occurring analysed (Costa and Amorim 2014, Costa et. al. 2014, in a broad area along the coastal basins between Bahia Costa et. al. 2017). The character-state optimization state, northeast Brazil, and the La Plata province, north- among the ‘G.’ brasiliensis species group and another in- east Argentina (Kullander 2003, Mattos et al. 2015). The cluded genus were performed using PAUP4 by most par- distribution of this species group covers a broad area of simonious reconstruction method (Swofford 1993). The the Atlantic Forest and a small area of the Caatinga, a relative numeric position was determined for each trans- semiarid northeast Brazilian biome (Mattos et al. 2015). formation through sequence alignment with the complete This study is the first analysis in which all valid species mitochondrial genome of Astronotus ocellatus (Agassiz, of the ‘G.’ brasiliensis species group were sampled and 1831) (Mabuchi et al. 2007). Plesiomorphic state for each analysed in a molecular phylogenetic framework, besides species was presented before arrow and apomorphic state including populations of three unidentified species from after the arrow. the Atlantic Forest of northeast Brazil exhibiting unique The tree-based approach used for molecular data was morphological features, which are herein recognised and proposed by Wiens and Penkrot (2002), in which species described as new. are delimited through well supported clades of haplo- types with concordant geographic distribution. The sig- nificance of the branches for species delimitation was Material and methods evaluated by the support values, bootstrap values equal or higher than 70% as significant (Hillis and Bull 1993) Material and posterior probability of the branches values equal or Measurements and counts follow Kullander (1986, 1990) higher than 0.95 as significant (Alfaro and Holder 2006). and Kullander & Nijssen (1989). Measurements are pre- DNA extraction, amplification and sequencing sented as percentages of standard length (SL), except sub- units of head, which are presented as percentages of head Total genomic DNA was extracted from muscular tissue length (HL). Osteological preparations (C&S) were made of the right side of the caudal peduncle using the DNeasy according to Taylor and Van Dyke (1985). Osteological Blood & Tissue Kit (Qiagen). Sequence fragments of nomenclature follows Costa (2006). Material examined cytochrome b (CYTB) with 1,100 bp and cytochrome c is deposited in the following ichthyological collections: oxidase I (COI) with 680 bp were obtained. To amplify Ichthyology collection of the Center for Agrarian and these DNA fragments,
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