Molecular Phylogeny of Philippine Tigerperches (Perciformes: Terapontidae) Based on Mitochondrial Genes
Reynand Jay C. Canoy1,2,3, Ian Kendrich C. Fontanilla1,2, and Jonas P. Quilang1,2*
1Natural Sciences Research Institute, University of the Philippines
Diliman, Quezon City 1101 Philippines
2Institute of Biology, College of Science, University of the Philippines
Diliman, Quezon City 1101 Philippines
3Institute of Human Genetics, National Institutes of Health
University of the Philippines Manila, 625 Pedro Gil St., Ermita, Manila 1000 Philippines
The molecular phylogeny of the Philippine tigerperches is first described in this study. Eight species were analyzed: these include one endemic species (Leiopotherapon plumbeus); one introduced species (Bidyanus bidyanus); and six native species (Terapon jarbua, Terapon puta, Terapon theraps, Pelates quadrilineatus, Helotes sexlineatus, and Mesopristes cancellatus). Primers were designed to amplify and sequence the 12S rRNA (12S), cytochrome c oxidase subunit I (COI), and cytochrome b (CytB) genes. The concatenated 12S, COI, and CytB sequences (3529 bp) were used to construct the phylogeny of the tigerperches using Maximum Parsimony (MP), Neighbor Joining (NJ), Maximum Likelihood (ML), and Bayesian Inference (BI) analyses. All four analyses supported the monophyly of tigerperches. Except for the MP tree, all phylogenetic trees showed that Terapon jarbua was the first to have diverged from the rest of the tigerperch species examined. The congeneric T. jarbua, T. puta and T. theraps did not group together, suggesting their non-monophyly. However, SH test on the unconstrained (actual observation) and constrained (the three congeneric species were forced to group together) NJ trees showed no significant difference (p = 0.55). This demonstrated that the monophyly of the genus Terapon remains unclear. Helotes sexlineatus and Pelates quadrilineatus were found to group together based on the three markers, which lends support to assertions in other studies that these taxa are congeneric and should be placed in the same genus Pelates. The immediate sister taxa of B. bidyanus, L. plumbeus, M. cancellatus, and Rhynchopelates oxyrhynchus were not confirmed by the MP, NJ, ML, and BI phylogenetic trees. The inclusion of additional unsampled Philippine species, as well as those from neighboring countries, is recommended to further refine the phylogeny of tigerperches.
Tigerperches or grunters (family Terapontidae) are ray-finned fishes (order Perciformes, class Actinopterygii, phylum Chordata) composed of 61 species from 15 genera (Fricke et al. 2019) that thrive in marine, coastal, brackish, or freshwater parts of the Indo-West Pacific region (Nelson 2006). They have oblong to oblong-ovate body shape, two spines on the opercle, dorsal fin with 11–14 spines and 8–14 soft rays, anal fin with three spines and 7–15 soft rays, and body length that can reach up to 80 cm (Nelson 2006). They are characterized by having an upper jaw that does not extend beyond the center of orbit (Vari 1999).
In the Philippines, historical records show that there are eight tigerperch species (Herre 1953) present, but Froese and Pauly (2019) reported that there are 10 tigerperch species that thrive in lakes, brackish and sea waters. They are locally traded as food fishes and are thus economically and commercially important. In particular, the Philippine endemic Leiopotherapon plumbeus – locally known as “ayungin” – is traded around the major lakes of Luzon Island. The native Mesopristes cancellatus or “pigek” is highly-priced in Mindanao. It can also be found in Lake Naujan, Lake Mainit, and Kalinwan River. It is an exquisite delicacy and is served at very high prices in restaurants and hotels. A recent study has shown that the “bulidao” fish in Abra River is the same as the “pigek” fish found in Mindanao (Maralit et al. 2012). Other tigerperch species such as Terapon jarbua and Pelates quadrilineatus are commonly caught in coastal areas. . . . read more
Acquah HdG. 2010. Comparison of Akaike information criterion (AIC) and Bayesian information criterion (BIC) in selection of an asymmetric price relationship. J Dev Agric Econ 2(1): 1–6.
Akaike H. 1973. Information theory and an extension of the maximum likelihood principle. In: Second International Symposium on Information Theory. Petrov BN, Csaki F eds. Budapest (Hungary): Akademiai Kiado. p. 267–281.
Akihito, Iwata A, Kobayashi T, Ikeo K, Imanishi T, Ono H, Umehara Y, Hamamatsu C, Sugiyama K, Ikeda Y, Sakamoto K, Fumihito A, Ohno S, Gojobori T. 2000. Evolutionary aspects of gobioid fishes based upon a phylogenetic analysis of mitochondrial cytochrome b genes. Gene 259: 5–15.
Azhagar S, Anbalangan T, Veerapan N. 2009. Distribution and abundance of finfish larvae along the Bay of Bengal (South East Coast of India). Curr Res J Biol Sci 1(1): 14–17.
BOSTOCK BM, ADAMS M, LAURENSON LJB, AUSTIN CM. 2006. The molecular systematics of Leiopotherapon unicolor (Günther, 1859): Testing for cryptic speciation in Australia’s most widespread freshwater fish. Biol J Linn Soc 87: 537–552.
Chen SF, Huang BQ, Chien YY. 1998. Histochemical characteristics of sonic muscle fibers in tigerperch, Terapon jarbua. Zool Stud 37(1): 56–62.
Chen D, Guo X, Nie P. 2010. Phylogenetic studies of sinipercid fish (Perciformes: Sinipercidae) based on multiple genes, with first application of an immune-related gene, the virus-induced protein (viperin) gene. Mol Phylogenet Evol 55: 1167–1176.
Darriba D, Taboada GL, Doallo R, Posada D. 2012. jModelTest 2: More models, new heuristics and parallel computing. Nat Methods 9(8): 772.
Davis AM, Unmack PJ, Pusey BJ, Johnson JB, Pearson RG. 2012. Marine-freshwater transitions are associated with the evolution of dietary diversification in terapontid grunters (Teleostei: Terapontidae). J Evol Biol 25: 1163–1179.
Doiuchi R, Nakabo T. 2006. Molecular phylogeny of the stromateoid fishes (Teleostei: Perciformes) inferred from mitochondrial DNA sequences and compared with morphology-based hypotheses. Mol Phylogenet Evol 39: 111–123.
Evans J, Sullivan J. 2011. Approximating model probabilities in Bayesian information criterion and decision-theoretic approaches to model selection in phylogenetics. Mol Biol Evol 28(1): 343–349.
Farris JS, Kallersjo M, Kluge AG, Bult C. 1994. Testing significance of incongruence. Cladistics 10: 315–319.
Felsenstein J. 1981. Evolutionary trees from DNA sequences: A maximum likelihood approach. J Mol Evol 58: 131–144
Fitch WM. 1997. On the problem of discovering the most parsimonious tree. The Am Nat 111: 223–257.
FRICKE R, ESCHMEYER WN, VAN DER LAAN R eds. 2019. Eschmeyer's Catalog of Fishes: Genera, Species, References. Retrieved from http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp on 14 Aug 2019.
Froese R, Pauly D. 2014. FishBase. Retrieved from www.fishbase.org on 01 Jun 2014.
Froese R, Pauly D. 2019. FishBase. Retrieved from www.fishbase.org on 14 Aug 2019.
Guindon S, Gascuel O. 2003. A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704.
Hall TA. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95–98.
HERRE A. 1953. Check list of Philippine fishes. Washington, DC: United States Government Printing Office. 977p.
Huelsenbeck JP, Ronquist FR. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.
Lee SC, Tsai MP. 1999. Molecular systematics of the thornfishes genera Terapon and Pelates (Perciformes: Teraponidae) with reference to the new genus Pseudoterapon. Zool Stud 38(3): 279–286.
Li J, Wang X, Kong X, Zhao K, He S, Mayden RL. 2008. Variation patterns of the mitochondrial 16S rRNA gene with secondary structure constraints and their application to phylogeny of cyprinine fishes (Teleostei: Cypriniformes). Mol Phylogenet Evol 47: 472–487.
MARALIT B, VENTOLERO MF, GAERLAN RS, MAMALANGKAP M, SANTOS M. 2012. Species and endemicity status of the therapontid “Pigek”, Mesopristes cancellatus (Cuvier, 1829) in the Philippines. Philipp Sci Lett 5(1): 30–39.
Minin V, Abdo Z, Joyce P, Sullivan J. 2003. Performance-based selection of likelihood models for phylogeny estimation. Syst Biol 52: 674–83.
Nelson JS. 2006. Fishes of the World, 4th ed. New Jersey: John Wiley & Sons, Inc. 601p.
Orrell TM, Carpenter KE. 2004. A phylogeny of the fish family Sparidae (porgies) inferred from mitochondrial sequence data. Mol Phylogenet Evol 32: 425–434.
Peng Z, Wang J, He S. 2006. The complete mitochondrial genome of the helmet catfish Cranoglanis bouderius (Siluriformes: Cranoglanididae) and the phylogeny of otophysan fishes. Gene 376: 290–297.
Posada D. 2009. Selections of models of DNA evolution with jModelTest. In: Methods in Molecular Biology. New York: Humana Press. p. 93–112.
Quilang JP, Basiao ZU, Pagulayan RC, Roderos RR, Barrios EB. 2007. Meristic and morphometric variation in the silver perch, Leiopotherapon plumbeus (Kner, 1864), from three lakes in the Philippines. J Appl Ichthyol 23: 561–567.
Quilang JP, Basiao ZU, Pagulayan RC, Roderos RR, Cao EP. 2008. Low isozyme variation in native and transplanted populations of the endemic Philippine silver perch, Leiopotherapon plumbeus (Kner, 1864), from three lakes in the Philippines. Philipp Agric Sci 91: 99–103.
Ronquist F, Huelsenbeck JP, van der Mark P. 2005. MrBayes 3.1 Manual. Retrieved from http://mrbayes.csit.fsu.edu/manual.php on 01 Jan 2013.
Rowland SJ. 2001. Record of the banded grunter Amniataba percoides (Teraponidae) from the Clarence River, New South Wales. Aust Zool 31(4): 603–607.
Saitou N, Nei M. 1987. The Neighbor-joining method for estimating and testing minimum evolution trees. Mol Biol Evol 4: 406–425.
Schmidt HA. 2009. Testing Tree Topologies. In: The Phylogenetic Handbook: A Practical Approach to Phylogenetic Analysis and Hypothesis Testing, 2nd ed. Cambridge, UK: Cambridge University Press. p. 381–404.
Schwarz G. 1978. Estimating the dimension of a model. Ann Stat 6: 461–464.
Shimodaira H, Hasegawa M. 1999. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16: 1114–1116.
Slechtová V, Bohlen J, Freyhof J, Ráb P. 2006. Molecular phylogeny of the Southeast Asian freshwater fish family Botiidae (Teleostei: Cobitoidea) and the origin of polyploidy in their evolution Mol Phylogenet Evol 39: 529–541.
Sloss BL, Billington N, Burr BM. 2004. A molecular phylogeny of the Percidae (Teleostei, Perciformes) based on mitochondrial DNA sequence. Mol Phylogenet Evol 32: 545–562.
Staden R, Beal KF, Boonfield JK. 2000. The Staden Package, 1998. Methods Mol Biol 132: 115–130.
Swofford DL. 2002. PAUP* 4.0b10. Sunderland, MA: Sinauer Associates.
Thacker CE. 2003. Molecular phylogeny of the gobioid fishes (Teleostei: Perciformes: Gobioidei). Mol Phylogenet Evol 26: 354–368.
Thacker CE, Hardman MA. 2005. Molecular phylogeny of basal gobioid fishes: Rhyacichthyidae, Odontobutidae, Xenisthmidae, Eleotridae (Teleostei: Perciformes: Gobioidei). Mol Phylogenet Evol 37: 858–871.
Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM. 2007. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35: w71–w74.
Vandamme AM. 2009. Basic concepts of molecular evolution. In: The Phylogenetic Handbook: A practical Approach to Phylogenetic Analysis and Hypothesis Testing, 2nd ed. Cambridge, UK: Cambridge University Press. p.1–29.
Vari RP. 1978. The terapon perches (Percoidei, Teraponidae): A cladistics analysis and taxonomic revision. Bull Am Mus Nat Hist 159(5): 175–340.
Vari RP. 1999. Terapontidae. In: FAO Species Identification Guide for Fishery Purposes. The Living Marine Resources of the Western Central Pacific Vol. 5. Rome: FAO. p. 3305–3316.
Wang HY, Lee SC. 2002. Secondary structure of mitochondrial 12S rRNA among fish and its phylogenetic applications. Mol Biol Evol 19(2): 138–148.
Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN. 2005. DNA barcoding Australia's fish species. P Roy Soc B-Biol Sci 360: 1847–1857.
Xia X, Xie Z, Salemi, M, Chen L, Wang Y. 2003. An index of substitution saturation and its application. Mol Phylogenet Evol 26: 1–7.
Xia X, Lemey P. 2009. Assessing substitution saturation with DAMBE. In: The Phylogenetic Handbook: A Practical Approach to DNA and Protein Phylogeny Testing, 2nd ed. Cambridge, UK: Cambridge University Press. p. 615–630.
Xiao H, Chen Sy, Liu ZM, Zhang RD, Li WX, Zan RG. 2005. Molecular phylogeny of Sinocyclocheilus (Cypriniformes: Cyprinidae) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 36: 67–77.
Yagishita N, Miya M, Yamanoue Y, Shirai SM, Nakayama K, Suzuki, N, Satoh, TP, Mabuchi K, Nishida M, Nakabo T. 2009. Mitogenomic evaluation of the unique facial nerve pattern as a phylogenetic marker within the perciform fishes (Teleostei: Percomorpha). Mol Phylogenet Evol 53: 258–266.