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Molecular Phylogeny of Catfishes (Teleostei: Siluriformes) in the Philippines Using the Mitochondrial Genes COI, Cyt B, 16S Rrna, and the Nuclear Genes Rag1 and Rag2

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Molecular Phylogeny of Catfishes (Teleostei: Siluriformes) in the Philippines Using the Mitochondrial Genes COI, Cyt B, 16S Rrna, and the Nuclear Genes Rag1 and Rag2 Philippine Journal of Science 143 (2): 187-198, December 2014 ISSN 0031 - 7683 Date Received: 02 February 2014 Molecular Phylogeny of Catfishes (Teleostei: Siluriformes) in the Philippines Using the Mitochondrial Genes COI, Cyt b, 16S rRNA, and the Nuclear Genes Rag1 and Rag2 Shiny Cathlynne S. Yu and Jonas P. Quilang* Molecular Population Genetics Laboratory, Institute of Biology, College of Science, University of the Philippines, 1101Diliman, Quezon City, Philippines In this study, three mitochondrial genes, namely, cytochrome c oxidase subunit I (COI), cytochrome b (cyt b), and 16S rRNA, and two nuclear genes, namely, recombination activating gene 1 (rag1) and recombination activating gene 2 (rag2) were used to determine the phylogenetic relationships of seven native and four introduced catfishes in the Philippines belonging to five families. All genetic trees constructed using the methods Maximum-Likelihood (ML) and Bayesian inference (BI) of concatenated sequences of the five genes support the monophyly of catfishes in each of the five families. ML and BI generated a topology (Loricariidae + (Clariidae + (Ariidae + (Pangasiidae + Plotosidae)))). Loricariidae is separated from the monophyletic clade of Ariidae, Pangasiidae, Clariidae and Plotosidae. One specimen each of Arius manillensis and A. dispar (Ariidae) shared the same unique concatenated sequence, while two specimens of Pterygoplichthys pardalis shared a unique concatenated sequence with one specimen of P. disjunctivus (Loricariidae). It is possible that the two Arius species and the two Pterygoplichthys species are synonymous. Future studies may use cytogenomic markers to establish if the species of these latter genera are valid. Future studies may also use a combination of molecular and morphological data in inferring the phylogenetic relationships of catfishes. Key Words: catfishes, mitochondrial gene, nuclear gene, phylogeny, Siluriformes INTRODUCTION Pterygoplichthys disjunctivus and Pterygoplichthys pardalis are causing environmental problems. Catfishes (Order Siluriformes) are a diverse group of ray-finned fishes (Nelson 2006) that are distributed in Catfishes are primarily freshwater fishes with only all continents (Diogo 2004) and comprise more than two marine families: Plotosidae, which is distributed 3,088 valid species distributed among 477 genera and in the Indo-West Pacific and Ariidae, which is found 36 families (Ferraris 2007). Catfishes are valued as worldwide in tropical to warm temperate zones (Kailola popular sport fish, food items, and tropical aquarium fish 2004). In the Philippines, Froese & Pauly (2013) in (Nelson 2006). Two introduced species, namely, Clarias FishBase list 31 species of catfishes belonging to eight gariepinus and Pangasianodon hypophthalmus are used in families, namely, Ariidae, Clariidae, Callichthyidae, aquaculture, while two other introduced species, namely, Loricariidae, Ictaluridae, Pangasiidae, Plotosidae, and Siluridae. However, Corydoras aeneus, the single species *Corresponding author: [email protected] of Callichthyidae, is questionable as it was only reported 187 Philippine Journal of Science Yu and Quilang: Molecular Phylogeny of Vol. 143 No. 2, December 2014 Philippines Catfishes as a specimen in a fish living museum (Froese & Pauly (2006) used both rag1 and rag2 in showing the monophyly 2013). Likewise, the occurrence of Ictalurus punctatus, of Siluriformes. the single species of Ictaluridae, is questionable as this species was introduced in 1974 but it could not thrive in The combination of mitochondrial and nuclear genes the natural conditions of the Philippines (Juliano et al. tends to improve the accuracy of phylogenetic trees 1989). Only 15 catfish species do not have contradicting (Lake & Moore 1998). Information at different levels reports and are certain to occur in the Philippines. These of phylogeny can be obtained because the mtDNA and include Arius dispar, Arius manillensis, Plicofollis nuclear genes have different evolutionary rates and modes magatensis, Plicofollis nella, Clarias batrachus, Clarias of inheritance (Graybeal 1994). Mitochondrial genes can gariepinus, Clarias macrocephalus, Clarias nieuhofii, resolve terminal taxa because they evolve faster than Pterygoplichthys disjunctivus, Pterygoplichthys pardalis, nuclear genes (Avise 1994). Nuclear rag genes, on the Pangasianodon hypophthalmus, Paraplotosus albilabris, other hand, are highly conserved (Hoofer et al. 2003); Plotosus canius, Plotosus lineatus, and Pterocryptis thus, they can show deep phylogenetic relationships taytayensis. Eleven species of the catfishes reported (Sullivan et al. 2006).This study used the combination of in the Philippines have been DNA barcoded using the the aforementioned three mtDNA and two nuclear genes in cytochrome c oxidase subunit I (COI) gene (Quilang inferring the phylogeny of native and introduced catfishes & Yu 2013). These species include the endemic in the Philippines. Arius manillensis Valenciennes 1840 and Plicofollis The objective of this study was to determine the magatensis (Herre 1926), the native Arius dispar Herre phylogenetic relationships of 11 species of catfishes 1926, Clarias macrocephalus Gunther 1864, Clarias belonging to Ariidae (Arius manillensis, A. dispar, and batrachus (Linnaeus 1758), Paraplotosus albilabris Plicofollis magatensis), Pangasiidae (Pangasianodon (Valenciennes 1840), and Plotosus lineatus (Thunberg hypophthalmus), Clariidae (Clarias gariepinus, 1787), and the introduced Clarias gariepinus (Burchell C. macrocephalus, and C. batrachus), Plotosidae 1822), Pangasianodon hypophthalmus (Sauvage 1878), (Paraplotosus albilabris and Plotosus lineatus), and Pterygoplichthys disjunctivus (Weber 1991), and Loricariidae (Pterygoplichthys disjunctivus and P. Pterygoplichthys pardalis (Castelnau 1855). The DNA pardalis) using the mitochondrial genes COI, cyt b, 16S barcoding successfully discriminated seven of the eleven rRNA, and the nuclear genes rag1 and rag2. species; however, the COI was not able to differentiate Arius dispar from A. manillensis, and Pterygoplichthys disjunctivus from P. pardalis. Several studies have been undertaken to determine MATERIALS AND METHODS the phylogenetic relationships of catfishes based on morphology (de Pinna 1998; Teugels 2003; Diogo 2004; Sample collection and identification Rodiles-Hernandez et al. 2005) as well as molecular Eleven species of native and introduced catfishes data (Hardman 2005; Sullivan et al. 2006). Some issues were collected from around the Philippines (Table and questions, however, remain on the classification 1). These included the native Arius dispar, endemic of catfishes (Nelson 2006). For example, there is no Arius manillensis and Plicofollis magatensis (Ariidae), consensus yet on the phylogenetic relationships of some native Clarias batrachus and Clarias macrocephalus, catfish subfamilies, such as of that of Galeichthyinae and introduced Clarias gariepinus (Clariidae), native Ariinae (Kailola 2004; Betancur-R et al. 2007). Paraplotosus albilabris and Plotosus lineatus (Plotosidae), introduced Pangasianodon hypophthalmus (Pangasiidae), The mitochondrial gene regions COI, cytochrome b Pterygoplichthys disjunctivus and Pterygoplichthys (cyt b), and 16S rRNA have been used to determine pardalis (Loricariidae).The specimens were initially the phylogenetic relationships of catfishes. Wong et al. identified based on morphology. Arius dispar, Arius (2011) showed the phylogenetic relationships of nine manillensis, and Plicofollis magatensis were identified catfish species of families Clariidae and Pangasiidae following Herre (1926), Kailola (1999), and Marceniuk using COI. Guo et al. (2004) used both mitochondrial cyt & Menezes (2007). Pangasianodon hypophthalmus b and 16S rRNA genes in elucidating the phylogeny and was identified according to Roberts & Vidthayanon phylogeography of Chinese sisorid catfishes. Kartavtsev (1991). The Clarias species were identified using the et al. (2007) also used cyt b and 16S rRNA regions taxonomic keys of Conlu (1986), Teugels et al. (1999), in inferring the phylogeny of bullhead torrent catfish, Sudarto & Pouyaud (2005), and Ng & Kottelat (2008). Liobagrus obesus. The nuclear recombination activating The two janitor fishes (Pterygoplichthys pardalis and P. gene (rag) is also used to infer deep phylogenetic disjunctivus) were identified according to Armbruster relationships in fishes (Hardman 2004). Sullivan et al. (2002) and Wu et al. (2011). Paraplotosus albilabris and 188 Philippine Journal of Science Yu and Quilang: Molecular Phylogeny of Vol. 143 No. 2, December 2014 Philippines Catfishes 189 Table 1. Taxonomy, collection site, GenBank accession numbers and voucher ID of specimens used in this study. No. of Species Family Status Collection Site GenBank accession number Voucher ID specimens COI cyt b 16S rRNA rag1 rag2 Plicofollis Ariidae Endemic Camalaniugan, 2 KF604678; KJ533246; KJ533228; KJ533268; KJ533286; CgA2; magatensis Cagayan KF604677 KJ533247 KJ533229 KJ533269 KJ533287 CgA3 Clarias Aparri, KF604663; KJ533248; KJ533230; KJ533270; KJ533288; CgCm2; Clariidae Native 2 macrocephalus Cagayan KF604666 KJ533249 KJ533231 KJ533271 KJ533289 CgCm3 Clarias Aparri, KF604645; KJ533250; KJ533232; KJ533272; KJ533290; CCBR1; Clariidae Native 2 batrachus Cagayan KF604646 KJ533251 KJ533233 KJ533273 KJ533291 CCBR2 Clarias Bustos, KF604660; KJ533252; KJ533234; KJ533274; KJ533292; BCG1; Clariidae Introduced 2 gariepinus Bulacan KF604661 KJ533253 KJ533235 KJ533275 KJ533293 BCG2 Pangasianodon
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