Iranian Journal Fisheries Sciences 15(1) 333-346 2016

Phylogenetic relationships of the commercial marine shrimp family from Persian Gulf

Samadi S.1; Ghavam Mostafavi P.1; Rezvani Gilkolaii S.2*; Fatemi M.1; Fazli H.3

Received: July 2014 Accepted: December 2015

Abstract Phylogenetic relationships among all described (total of 5 taxa) of the shrimp genus , were examined with nucleotide sequence data from portions of mitochondrial gene and cytochrome oxidase subunit I (COI). There are twelve commercial shrimp in the Iranian coastal waters. The reconstruction of the evolution phylogeny of these species is crucial in revealing stock identity that can be used for the management of fish industries in Iran. Mitochondrial DNA sequences were used to reconstruct the phylogeny of the Penaeus species of marine shrimp. For this purpose, DNA was extracted using phenol- chloroform well as CTAB method. The evolutionary relationships among 5 species of the shrimp genus Penaeus were examined using 610 bp of mitochondrial (mt) DNA from the cytochrome oxidase subunit I gene. Finally the cladograms were compared and the resulting phylogenetic trees confirmed that the Iranian species originated from the Indo-west pacific species. The Iranian species, which were not grouped with the other Penaeid taxa, seem to always form a sister- clade to the Indo-west pacific species with strong bootstrap support of 100%. Although the Iranian species + Western Hemisphere clade is paraphyletic in our gene tree, the bootstrap support is high. However, we still lack any comprehensive and clear understanding of phylogenetic relationships in this group.

Keywords: Mitochondrial DNA, Penaeidae, Persian Gulf, Phylogeny

1-Department of Marine Biology, Science and Research Branch, Islamic Azad University, Tehran, Iran 2-Iranian Fisheries Science Research Institute, Agricultural Research, Education and Extension Organization, Tehran, Iran. 3- Caspian Sea Ecology Research Center, Iranian Fisheries Science Research Institute, Agricultural Research, Education and Extension *Corresponding author's email: [email protected]

334 Samadi et al., Phylogenetic relationships of the commercial marine shrimp family…

Introduction has been reported (Chong and The Penaeid shrimp form a diverse Sasekumar, 1982). group of marine decapods with over As is known, mtDNA is a useful 400 species globally distributed and maternal marker because of its inhabiting both shallow waters and matrilineal mode of inheritance. In abyssal zones below 5000 m (Pérez , mtDNA genes such as COI are Farfante and Kensley, 1997). The particularly suitable for the Penaeid industry has grown rapidly determination of intraspecific genetic through the last 30 years and the diversity owing to a high evolutionary dominant species are Penaeus monodon rate found in this maternally transmitted (Fabricius 1798), P. vannamei (Boone genome (Avise et al., 1987). Therefore 1931), P. chinensis (Osbeck 1765) P. it has been widely used as a genetic stylirostris (Stimpson 1874), P. marker to assess the phylogeography japonicus (Bate 1888), P. merguiensis and phylogeny within numerous species (De Man 1888) and P. indicus (H. and genera (Baldwin et al., 1998; Milne Edwards 1837). O’Grady et al., 1998; Funk, 1999; Reed Shrimp of the genus Penaeus and Sperling, 1999; Masta, 2000; (Crustacea: ) are the most Walton et al., 2000). Baldwin et al. abundant group of marine groups in (1998) examined 13 different species of tropical and subtropical waters around Penaeus using 558 bp of mitochondrial the world. Due to the lack of research in DNA from COI and was able to Iran, to resolve phylogeny relationships successfully divide the genus into two within this group is the main reason to groups (Burkenroad, 1934). perform this study. It is important to Mitochondrial DNA (mtDNA) manage wild stocks differently than it sequences have proved extremely was done for P. monodon. P. useful in elucidating phylogenetic merguiensis. For example, P. indicus, relationships among many P. japonicus, and P. vannamei together groups (Cunningham et al., 1992). can be easily be matured in captivity Mitochondrial large subunit ribosomal without eyestalk ablation (Bailey-Brock RNA (16S rRNA) and cytochrome c and Moss, 1992). Unfortunately, oxidase subunit I (COI) genes have Chaitiamvong and Supongpan (1992) been particularly helpful in analyzing tolled the existence of over 50 Penaeid crustacean phylogeny at the species species in Thai waters, four of them (P. level (Chu et al., 2003). Baldwin et al. merguiensis, P. indicus, P. silasi, and P. (1998) examined the phylogenetic penicillatus) are considered relationships of 13 Penaeus s.l. species morphologically similar species. based on COI sequences. The Taxonomic difficulties about the evolutionary partitions resolved do not external morphology of P. merguiensis support the subgenus division but are concordant with biogeographic Iranian Journal of Fisheries Sciences 15(1) 2016 335 groupings within the genus. In the true relationships among all particular, their data show that Penaeus species, and we still lack any Litopenaeus and are comprehensive and clear understanding not valid phylogenetic groupings, but of phylogenetic relationships in this are paraphyletic (Baldwin et al., 1998). group. To date, 28 species are recognized in The aim of this study was the Penaeus (Dall et al., 1990). There have molecular identification of 5 been two studies so far based on 16S commercial shrimp species of the rRNA or combined 16S and COI Persian Gulf and Oman Sea, using a sequences of the superfamily DNA sequencing analysis of Penaeoidea in which 16 species cytochrome oxidase subunit I (COI). In (Vázquez-Bader et al., 2004) and 11 the present study, the mitochondrial species (Quan et al., 2004) of the cytochrome oxidase subunit I gene was Penaeidae were included. Results from chosen for analysis as it has proven the studies, however, question the useful in studying phylogenetic monophyletic status of the family relationships at the species level in Penaeidae. Voloch et al. (2005) many (Howland and Hewitt, examining the phylogenetic 1995).This study provides new COI relationships of the Penaeidae by sequences from 5 species, allowing COI analyzing 16S and COI sequences of 39 phylogenetic analysis of almost the species of the Penaeidae based on entire group. The Indian-Pacific has the existing data (Tong et al., 2000; most diverse species, with about five Maggioni et al., 2001; Lavery et al., times of that found in the Atlantic, 2004; Quan et al., 2004). Since showing the region of the origin for this Penaeus s.l. shrimp are remarkably widespread genus (Dall et al., 1990). well-known and are of great economic The second goal of this study was to importance separating them into six determine whether the Indo-West genera can produce significant impact Pacific is the origin of the genus. on both scientific and commercial Finally, the material presented here practices. provides a phylogenetic framework for In recent years there have been a management of these important natural variety of phylogenetic researches on resources. Bernatchez (1995), reported Penaeus species using genetic markers wildlife management programs that to solve questions regarding their depend on an understanding of the and evolution. Unfortunately, phylogenic relation. Marine shrimp of all previous analyses have been the superfamily Penaeoidea represent severely constrained by data limitations approximately a third of the world’s in the number of species and the commercially important shrimp species number of genetic characters. Overall and account for over 80% of the wild there is still considerable doubt about catch. In addition, members of the 336 Samadi et al., Phylogenetic relationships of the commercial marine shrimp family… genus Penaeus represent over 90% of The sampling sites and the number of the cultured species worldwide. specimens examined are listed in Table 1. Materials and methods The Chinese mud shrimp, Solenocera Collection of materials koelbeli De Man, 1911, of the family Five species of commercial shrimp Solenoceridae (Decapoda, belonging to the family Peneaidae, were , Penaeoidea), was collected by fishing trawler vessel involved in the study that was chosen as Ferdows II from northern parts of the an outgroup (Table 1). Five individuals Persian Gulf and preserved in 95% of each species were used for molecular ethanol. The sampled species are the sequence analysis and the species were following: Parapenaeopsis stylifera identified using several shrimp species (H. Milne Edwards, 1837 [in H. Milne keys (Dall et al., 1990) and they were Edwards, 1834-1840]), Metapenaeus also identified by the researcher stebbingi Nobili, 1904, M. stridulans (Mohsen Safaiee), who is an (Alcock, 1905). P. semisulcatus, P. experienced shrimp taxonomist. (Fenneropenaeus) merguiensis.

Table 1: Details of specimens and sequences used in this study.

Species N Location GenBank Accession Nos.a P. (Farfantepenaeus) aztecus 1 Gulf of Mexico, USA AF279834 P. (Farfantepenaeus) brasiliensis 1 AF0293931 P. (Farfantepenaeus) californiensis 1 NC 012738 P. (Farfantepenaeus) duorarum 1 Gulf of Mexico, USA AF279835 P. (Farfantepenaeus) notialis 1 X84350 P. (Farfantepenaeus) paulensis 1 AF0293921 P. (Farfantepenaeus) subtilis 1 AF2485594 P. (Fenneropenaeus) chinensis 1 Zhujiang estuary, China AF279836 P. (Fenneropenaeus) indicus 1 Bonaparte Gulf, W. Australia AF279837 P. (Fenneropenaeus) merguiensis 4 Moreton Bay, Australia AF279838 Persian Gulf KR261589(40), KR261590(41), KR261591(43) P. (Fenneropenaeus) penicillatus 1 Zhujiang estuary, China AF279839 P. (Fenneropenaeus) silasi 1 Singapore AF279840 P. (Litopenaeus) setiferus 1 Gulf of Mexico, USA AF279841 P. (Litopenaeus) stylirostris 1 AF2550572 S652616 Iranian Journal of Fisheries Sciences 15(1) 2016 337

Continued Table 1:

Species N Location GenBank Accession Nos.a P. (Litopenaeus) vannamei 1 Hawaii, USA AF279842 P. (Marsupenaeus) japonicus 1 Hong Kong AF279832 P. (Melicertus) canaliculatus 1 Taiwan AF279843 P. (Melicertus) kerathurus 1 Spain AF279844 P. (Melicertus) latisulcatus 1 Hong Kong AF279845 P. (Melicertus) longistylus 1 North Queensland, Australia AF279846 P. (Melicertus) marginatus 1 Taiwan AF279847 P.(Melicertus) plebejus 1 Moreton Bay, Australia AF279848 P. (Penaeus) esculentus 1 Moreton Bay, Australia AF279849 P. (Penaeus) monodon 1 Hong Kong AF279833 P. (Penaeus) semisulcatus 4 Hong Kong AF279831 Persian Gulf KR261586(30), KR261587(33), KR261588(34) P. stylifera 3 Persian Gulf KR261592(20), KR261593(22), KR261594(23) M. stebbingi Nobili 1 Persian Gulf KR261595(2) M. stridulans 3 Persian Gulf KR261583(112), KR261584(113), KR261585(114) Solenocera koelbeli Hong Kong AF105049 Sources sequences: 1Baldwin et al. (1998); 2Maggioni et al. (2001); 3Garcia-Machado et al. (1996), 4Gusm~ao et al. (2000);5 Guti_errez-Mill_an et al. (2002); 6Palumbi and Benzie (1991).

DNA extractiogarcian, PCR 1% SDS, and 1 Ag/ml proteinase K). amplification and sequencing The homogenate was incubated at 37 Muscle tissues of pleopods, antenna and °C, 1 h, and 55 °C overnight. The DNA preiopods were removed from was extracted using exoskeleton, preserved in 95º ethanol phenol/chloroform/isoamyl alcohol (Ovenden et al., 1997), and transferred (25:24:1) and recovered by ethanol to the laboratory. Three individuals of precipitation. DNA concentrations were each species were used for molecular spectrophotometrically determined analysis. Samples of muscle from (Sambrook et al., 1989). pleopods (10–15 mg) were used for Total DNA was isolated using extraction of total DNA using standard phenol-chloroform extraction proteinase-K digestion and either protocol (Hillis and Moritez, 1990). phenol/chloroform and CTAB method Segments of mitochondrial genes, 610 extraction. Total genomic DNA was bp fragment of cytochrome c oxidase individually extracted from frozen subunit I (COI) gene were amplified muscle of shrimp. from total DNA by polymerase chain The tissue was cut into small pieces reaction (PCR) (Saiki et al., 1988) with and was homogenized in an appropriate conserved primers: L-CO1490 and H- volume of the extraction solution (10 CO2198 for COI (Folmer et al., 1994). mM Tris–HCl, pH 7.5, 100 mM EDTA, 338 Samadi et al., Phylogenetic relationships of the commercial marine shrimp family…

PCR amplifications were conducted in parsimonious tree or trees with tree a Amersham Pharmacia Biotechthermal bisection-reconnection (TBR) branch- cycler TC 341 using a 5 min pre- swapping heuristic searches in PAUP⁎ denaturation at 95 ºC followed by 30 in which, all characters were equally cycles of 1 min at 95 ºC, 1 min at 40-46 weighted and the starting trees were ºC, 90 s at 72 ºC and a final 5 min at 72 obtained by 100 random stepwise ºC, were used to amplify 2 Ml of the additions. Nodal support was estimated DNA extract (undiluted or diluted 10_ by calculation of non-parametric in ddH2O), 2.5 Ml of Mg2 free buffer bootstrap (1000 pseudo-replicate, 10

(Promega), 0.7 Ml MgCl2, 0.3 Ml of random addition) proportions each primer, 0.45 Ml of dNTPs, 0.3 Ml (Felsenstein, 1985) and decay indices of Taq polymerase (Promega), and (Bremer, 1994) using PAUP⁎ PAUP* v ddH2O. 4.0b10. The Model Test (Posada and In all PCR amplifications, negative Krandall, 1998) was used to determine controls consisting of template-free the optimal model of nucleotide reactions were used to detect substitution in the ML analysis. contamination. The size and quality of Because of the number of taxa involved PCR products were evaluated on 1.5 % and computational time requirement, agarose gels. branch support for the best fitting tree from ML analyses was assessed using Phylogenetic analysis 100 bootstrap replicates, Solenocera Alignment and Phylogenetic Analyses koelbeli was also included in all Alignments of the sequences for this analyses. gene region were analyzed in a two-step The consensus phylogenetic trees process. First they were created with generated by these three methods are Clustal W (Higgins and Sharp, 1988) shown in Fig. 1. and then adjusted by eye to make the final alignments. The 38 taxa for COI Results alignment were subjected to maximum The sequences used for phylogenetic parsimony, and maximum likelihood analyses were 610 bp COI. Including (Felsenstein 1981) as applied in version the out group species and all the new 4.0 b10 of PAUP* (Swofford, 1999). sequences from the current study have Bayesian analyses was conducted using been deposited in GenBank (see Table MrBayes v 3.0b4 (Ronquist and 1 for accession numbers). Huelsenbeck, 2003). The COI sequences of P. The construction of phylogenetic semisulcatus and P. merguiensis from hypotheses from the data set was done Lavery et al. (2004) were not very using the maximum parsimony (MP), different from the sequences of P. and maximum likelihood (ML) semisulcatus and P. merguiensis gained methods. For MP, we obtained the most in the present report. Iranian Journal of Fisheries Sciences 15(1) 2016 339

The sequence analyses were based on species, although the presence of P. 610 bp for COI. All species were chinensis in the monophyletic clade collected from Persian Gulf the species with Farfantepenaeus and Litopenaeus were identified using several shrimp subgenera weakened the support species keys. slightly (bootstrap P 54+69). We decided to use sequences of Iranian shrimp is in the monophyletic Indo-West Pacific species and Western clade to indopacific group of high hemisphere from Lavery et al. (2004) bootstrap values (bootstrap P 100) in all for the subsequent phylogenetic the analyses. analyses. Using Model test (Posada and M. stridulans and P. stylifera were Crandall, 1998), the best-fitting models most closely related with P. of substitution for the COI data was the merguiensis as the sister taxon. P. transversion model with the general semisulcatus then joined this subclade time reversible model with a proportion with M. stebbingi as the most outlying of invariable sites and with a gamma sister taxon. distribution (GTR + I +G). The two species, P. merguiensis and Fig. 1 shows the best-fitting tree P. semisulcatus, were always placed in topology based on maximum likelihood the different clade in all analyses with analysis, Bayesian and parsimony relatively strong bootstrap support (100 analysis. by parsimony analysis, 84 by maximum In all the trees data approach, there likelihood and Bayesian). was very strong support (bootstrap P M. stebbingi and other Iranian 100) for the monophyletic status of species were always placed in the species (Fig. 1). There was also strong different monopyletic groups in all support for the monophyletic status of analyses with relatively strong the indo-pacific speices and Iranian bootstrap support (100 by all analysis).

340 Samadi et al., Phylogenetic relationships of the commercial marine shrimp family…

AF105049.1 Solenocera koelbeli 100 40 Fenneropenaeus merguiensis 100 100 9341 Fennero penaeus merguiensis

65

Fenneropenaeus merguiensis 43 100 96 112 M etapenaeopsis stridulans

91 113 M etapenaeopsis stridulans 100 114 Metapenaeopsis stridulans 57

84 64 84 20 Parapen eopsis stylifera 100 100 100 23 Parapeneopsis stylifera 100

22 Parapeneopsis stylifera

100 100 34 Penaeus semisulcatus 100 99 100 100

78 30 Penaeus semisulcatus

61 Penaeus semisulcatus 33 100 100 100 100 100 100 2Metapenaeus stebbingi Nobili

AF279849 Penaeus esculentus 100 Penaeus PACIFIC INDO 100 AF279833 Penaeus monodon

AF279831 Penaeus semisulcatus

- WEST PACIFIC AF2798471 Melicertus marginatus Meliceratus

84 59 AF279 843 Melicertus canaliculatu 98 AF279832 Marsupenaeus japonicus 56 70 AF279848 Melicertus plebejus 54 83 Meliceratus 54 AF279845 Melicertus latisulcatus 70 AF279846 Melicertus longistylus

AF279836 Fenneropenaeus chinensi 99 78 AF279834 Farfantepenaeus aztecus hemisphere hemisphere Western 70 Farfantepenaeus AF029392 Penaeus paulensis 53

AF248559 Penaeus subtilis 99 54 100 AF279835 Farfantepenaeus duoraru 69 100 X84350 Penaeus notialis 96 52 91 AF279842 Litopenaeus vannamei 52 Lit op 52 99 AF279841 Litopenaeus setiferus enae

us 100 S65261 Litopenaeus stylirostris 98 92 AF029393 Penaeus brasiliensis

NC 012738 Farfantepenaeus califo

AF279838 Fenneropenaeus merguien

90 AF279837 Fenneropenaeus indicus 98 Feneropenaeus 65 100 AF279839 Fenneropenaeus penicill 99 AF279840 Fenneropenaeus silasi

10 Figure 1: Numbers above branches indicate bootstrap values from Bayesian analysis (in italics), Parsimony analysis (normal text), and Maximum Likelihood analysis (in bold). Branches without bootstrap numbers indicate that the bootstrap values are not existent in the trees.

Bootstrap support of the Western latisulcatus of within Melicertus hemisphere group was lower than that longistylus, but parsimony, Maximum of the Indo-west Pacific. Among the likelihood and MrBayes failed to Indo-Pacific species there is robust resolve relationships among the support were the relationships between remaining Indo-Pacific species, P. Marsupenaeus japonicas and monodon and P. semisulcatus. Melicertus plebejus, and Melicertus Iranian Journal of Fisheries Sciences 15(1) 2016 341

In all three methods of analysis P. relationships of these studies brief these kerathurus, the sole eastern Atlantic relationships. species which was grouped strongly The present study compares the (indicated by high bootstrap support) phylogenetic hypotheses of the with P. japonicus and P. Penaeidae derived from new molecular canaliculatusto formed a distinct clade. data from Iran on Penaeidae, to the The eastern Pacific species P. vannamei previous schemes, and analyzing 610 and P. stylirostris show close bp of aligned mitochondrial COI gene relationships. sequences using, maximum parsimony, Among the Iranian species the maximum likelihood and Bayesian monophyly of the clade including F. inference methods yields similar merguiensis and M. stridulans, P. topologies (Fig. 1) with two major stylifera is strongly supported by clades. parsimony bootstrap (100). Lavery et al. (2004) used 26 16S partial sequences to study the Discussion phylogenetic relationships of the family Our study reveals the utility of COI Penaeidea. We tried to re-analyze the genes in the reconstruction of Penaeus sequences of the Penaeidae (with phylogeny. The combinations of almost outgroup taxa) utilized by them and all species from the whole genus has found that the Penaeid taxa formed two allowed the present study to show a major clades, which are consistent with relatively clear and well-supported our own results. The Iranian species, pattern of phylogenetic relationships which were not grouped with the other among the major groups of Penaeus Penaeid taxa, seem to always form a species in Iran. The Penaeidae sister-clade to Indo-west pacific species evolutionary history is elongated (Dall with strong bootstrap support of 100%. et al., 1990). The family has highest We found out that the origin of Iranian diversity in the Indo-West Pacific species is the Indo-west pacific species. region. About 200 species are known The molecular data support an Indo- and these have generally been grouped West Pacific origin of the genus with a into 17 genera (Dall et al., 1990) single relatively recent colonisation of although, the recent studies of the the Western Hemisphere, and the Penaeus genera, established 26 genera subsequent subdivision into two clades in the family Penaeidae. Pérez Farfante prior to the emergence of the and Kensley (1997). While the Panamanian isthmus (Lavery et al., taxonomy of Penaeids has been 2004). generally studied, research on the The results of Lavery et al. (2004) complete phylogenetic relationships that the subgenera Farfantepenaeus and between the genera and species is Litopenaeus are not paraphyletic are in limited. In Iran the lack of phylogenetic accordance with those in our study, 342 Samadi et al., Phylogenetic relationships of the commercial marine shrimp family… however, they differ from those given sequence is found in GenBank for P. by Baldwin et al. (1998) and Gusmao et stylifera and no sequence of M. al. (2000). The key conclusion from a stridulans and M. stebbingi is found. previous molecular study indicating that The current results on these three the subgenera Farfantepenaeus and mitogenomes can be used to obtain Litopenaeus are paraphyletic was more important information in later rejected. Litopenaeus species express a studies. clade, with close relationship to The phylogenetic relationships of the Farfantepenaeus, both of which clade decapods are as contentious as ever. to the sister clade of Fenneropenaeus. Despite the limited number of taxa Similar results for the phylogenetic tested in this study, studies with more relationships among the Penaeid shrimp taxa involving the complete were obtained in previous studies. It is mitochondrial genomes of this family based on protein-coding genes (Shen et are desirable to understand the al., 2007). Parsimony bootstrap and ML phylogeny of the Penaeidae. In strong statistical bootstrap support the summary, our molecular phylogeny has monophyly of all Penaeids that was clarified the relationships within the observed across the analysis (Shen et genus Peneaidae family in Iranian al., 2007). coastal waters. Our phylogenetic results Although the Iranian species + represent the first step toward Western Hemisphere clade is understanding the pattern of speciation paraphyletic in our gene tree, the in Penaeidae in Iran, the basis of bootstrap support is very high. molecular characters. Maximum parsimony tree, Maximum Likelihood tree and Bayesian tree show Acknowledgements a similar topology for the Penaeid Sincere thanks are extended to the shrimp (Fig. 1). Parsimony bootstrap Iranian Fisheries Research Behnam and ML strong statistical bootstrap Daghooghi and Mohammad Momeni support for the monophyly of all Iranian for kindly providing us with samples. Penaeid were observed across the We express our gratitude to Dr. A. analysis. P. stylifera define a clade, Nouri and Dr. Alireza Bamdad in with close relationship to M. stridulans, helping with data analysis using PAUP and both clade to the sister group of and invaluable comments. Penaeus, F. merguiensis, and P. We thank Dr. M. Safaie for all the semisulcatus. P. stylifera and F. help in the laboratory. This study was merguiensis, as were defined, are supported by Islamic Azad University apparently monophyletic. Science and Research Tehran Branch Information about M. stridulans and and Iranian Fisheries Research M. stebbingi and P. stylifera genes is Organization of Iran. Their help is very limited, currently only one greatly appreciated. Iranian Journal of Fisheries Sciences 15(1) 2016 343

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