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Molecular Phylogeny of the Highly Diversified Catfish Subfamily

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Molecular Phylogeny of the Highly Diversified Catfish Subfamily Molecular Phylogenetics and Evolution 94 (2016) 492–517 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Molecular phylogeny of the highly diversified catfish subfamily Loricariinae (Siluriformes, Loricariidae) reveals incongruences with morphological classification q ⇑ Raphaël Covain a, , Sonia Fisch-Muller a, Claudio Oliveira b, Jan H. Mol c, Juan I. Montoya-Burgos d, Stéphane Dray e,f a Muséum d’histoire naturelle, Département d’herpétologie et d’ichtyologie, route de Malagnou 1, case postale 6434, CH-1211 Genève 6, Switzerland b Departamento de Morfologia, Universidade Estadual Paulista Júlio de Mesquita Filho, Instituto de Biociências, Laboratório de Biologia e Genética de Peixes, Rubião Junior 18618-970, Botucatu, SP, Brazil c University of Suriname, Center for Agricultural Research in Suriname, CELOS and Department of Biology, POB 9212, Paramaribo, Suriname d Université de Genève, Département de Génétique et Evolution, Sciences III, quai E. Ansermet 30, CH-1211 Genève 4, Switzerland e Université de Lyon, F-69000 Lyon, France f Université Lyon 1, CNRS, UMR5558, Laboratoire de Biométrie et Biologie Evolutive, F-69622 Villeurbanne, France article info abstract Article history: The Loricariinae belong to the Neotropical mailed catfish family Loricariidae, the most species-rich catfish Received 24 February 2015 family. Among loricariids, members of the Loricariinae are united by a long and flattened caudal peduncle Revised 15 September 2015 and the absence of an adipose fin. Despite numerous studies of the Loricariidae, there is no comprehen- Accepted 19 October 2015 sive phylogeny of this morphologically highly diversified subfamily. To fill this gap, we present a molec- Available online 26 October 2015 ular phylogeny of this group, including 350 representatives, based on the analysis of mitochondrial and nuclear genes (8426 positions). The resulting phylogeny indicates that Loricariinae are distributed into Keywords: two sister tribes: Harttiini and Loricariini. The Harttiini tribe, as classically defined, constitutes a Systematics paraphyletic assemblage and is here restricted to the three genera Harttia, Cteniloricaria, and Harttiella. Neotropics Mitochondrial genes Two subtribes are distinguished within Loricariini: Farlowellina and Loricariina. Within Farlowellina, Nuclear genes the nominal genus formed a paraphyletic group, as did Sturisoma and Sturisomatichthys. Within Freshwaters Loricariina, Loricaria, Crossoloricaria, and Apistoloricaria are also paraphyletic. To solve these issues, and Amazon basin given the lack of clear morphological diagnostic features, we propose here to synonymize several genera (Quiritixys with Harttia; East Andean members of Crossoloricaria, and Apistoloricaria with Rhadinoloricaria; Ixinandria, Hemiloricaria, Fonchiiichthys, and Leliella with Rineloricaria), to restrict others (Crossoloricaria, and Sturisomatichthys to the West Andean members, and Sturisoma to the East Andean species), and to revalidate the genus Proloricaria. Ó 2015 Elsevier Inc. All rights reserved. 1. Introduction Rift Valley in Africa (Schaefer and Stewart, 1993). The species core flock Loricariidae (sensu Lecointre et al., 2013), represents the most The Loricariinae represent a highly diversified subfamily among species rich family of the Siluriformes with 898 valid species and the large Neotropical catfish family Loricariidae, or suckermouth an estimated 300 undescribed species distributed in more than armored catfish. Loricariids have undergone an evolutionary radia- 100 genera (Reis et al., 2003; Ferraris, 2007; Eschmeyer and tion at a subcontinental scale, from Costa Rica to Argentina, which Fong, 2015). Extremely variable color patterns and body shapes has been compared to that of the Cichlidae of the Great Lakes of the among loricariid taxa reflect their high degree of ecological special- ization, and because of their highly specialized morphology lori- cariids were recognized as a monophyletic assemblage in the q This paper was edited by the Associate Editor G. Orti. earliest classifications of the Siluriformes (de Pinna, 1998). The ⇑ Corresponding author. Loricariidae are characterized by a depressed body covered by E-mail addresses: [email protected] (R. Covain), sonia.fisch-muller@ bony plates, and above all, by the modification of the mouth into ville-ge.ch (S. Fisch-Muller), [email protected] (C. Oliveira), fi[email protected] a sucker disk. Within the Loricariidae, members of the subfamily (J.H. Mol), [email protected] (J.I. Montoya-Burgos), stephane.dray@ Loricariinae are diagnosed by a long and depressed caudal univ-lyon1.fr (S. Dray). http://dx.doi.org/10.1016/j.ympev.2015.10.018 1055-7903/Ó 2015 Elsevier Inc. All rights reserved. R. Covain et al. / Molecular Phylogenetics and Evolution 94 (2016) 492–517 493 peduncle and by the absence of an adipose fin. They live stuck to Farlowellini, and the Acestridiini. The latter were subsequently the substrate and show marked variations in body shape according placed in the subfamily Hypoptopomatinae by Schaefer (1991). to the various habitats colonized, from lotic to lentic systems, on In her PhD thesis, Rapp Py-Daniel (1997) proposed a phylogeny mineral or organic substrates. For example, members of Farlowella of the Loricariinae based on a phylogenetic analysis of morpholog- resemble a thin stick and blend remarkably among submerged ical characters. She confirmed the monophyly of the subfamily, and wood and leafs, whereas members of Pseudohemiodon are large split the Loricariinae into two tribes: Loricariini and Harttiini, the and flattened and bury themselves in sandy substrates like latter comprising Farlowellini (sensu Isbrücker, 1979). In a flatfishes. Some groups have numerous teeth, pedunculated, and morphological phylogenetic analysis of the family Loricariidae, organized in a comblike manner, while other groups have few Armbruster (2004) also obtained a similar splitting based on a teeth or even no teeth on the premaxillae. Teeth are often strongly restricted sampling of the Loricariinae, with Harttiini (sensu Rapp differentiated, and can be bicuspid straight and thick, spoon- Py-Daniel, 1997, comprising Harttia, Lamontichthys, Sturisoma, shaped, reduced in size or very long. An important diversity in and Sturisomatichthys), forming the sister group of Loricariini lip characteristics, which can be strongly papillose, filamentous (sensu Rapp Py-Daniel, 1997, comprising Crossoloricaria, Loricaria, or smooth, also characterizes this subfamily (Isbrücker, 1979; Loricariichthys, Ixinandria, and Rineloricaria). Covain and Fisch- Covain and Fisch-Muller, 2007). Muller (2007), based on multivariate analyses of generic diagnostic Different hypotheses have been proposed to classify the Lori- characters, also split the subfamily into two tribes, the Harttiini cariinae (summarized in Table 1). The first attempt was performed and the Loricariini, and proposed four morphological groups within by Isbrücker (1979) who distributed them into four tribes and the Loricariini: (1) the Pseudohemiodon group, (2) the Loricaria eight subtribes on the basis of external morphology, but without group, (3) the Rineloricaria group, and (4) the Loricariichthys phylogenetic inferences. These included the Loricariini, comprising group. Montoya-Burgos et al. (1998) proposed a first molecular six subtribes (Loricariina, Planiloricariina, Reganellina, Rinelori- phylogeny of the family Loricariidae using mitochondrial genes. cariina, Loricariichthyina, and Hemiodontichthyina), the Harttiini, Although, their analysis included only nine representatives of the including two subtribes (Harttiina and Metaloricariina), the Loricariinae, they partially confirmed their subdivision into two Table 1 Alternative classifications of the Loricariinae according to different authors. The different colors provide limits of the different recognised tribes. These tribes can include different taxa according to the different authors. Salmon: Loricariini; blue: Harttiini; green: Farlowellini; red: Acestridiini. 494 R. Covain et al. / Molecular Phylogenetics and Evolution 94 (2016) 492–517 main groups, but with Harttia (nominal genus of Harttiini) forming Montgomery (AUM); and Museu de Ciências e Tecnologia of the the sister genus of all other Loricariinae (comprising Farlowellini, Pontifícia Universidade Católica do Rio Grande do Sul (MCP), Porto part of Harttiini, and Loricariini). Covain et al. (2008) using mito- Alegre. The sequences were deposited in GenBank. chondrial genes, and Rodriguez et al. (2011) using mitochondrial and nuclear markers performed a molecular phylogeny on a small 2.2. DNA extraction, choice of markers, amplification, and sequencing sampling of the Loricariinae. Both studies restricted Harttiini to Harttia, and included Farlowelliini as a subtribe of Loricariini. Tissue samples were preserved in 80% ethanol and stored at Within the latter, the Loricariichthys and Loricaria–Pseudohemiodon À20 °C. Total genomic DNA was extracted with the DNeasy Tissue morphological groups (sensu Covain and Fisch-Muller, 2007) were Kit (Qiagen) following the instructions of the manufacturer. The confirmed as natural groupings, whereas monophyly of the choice of markers was governed by their ability to resolve inter Rineloricaria group was rejected. Similar results were also obtained generic relationships at subfamilial ranks. We thus selected the using different markers by Cramer et al. (2011) in a molecular mitonchondrial genes
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