Molecular phylogeny of Superfamily Penaeoidea Rafinesque-Schmaltz, 1815, based on mitochondrial 16S partial sequence analysis.ABSTRACT Partial mitochondrial DNA Mitochondrial DNA (mtDNA) is the DNA located in organelles called mitochondria. Most other DNA present in eukaryotic organisms is found in the cell nucleus. Nuclear and mitochondrial DNA are thought to be of separate evolutionary origin, with the mtDNA being derived from the sequences were analyzed to reconstruct the phylogeny of Superfamily superfamily /su·per·fam·i·ly/ (soo´per-fam?i-le) 1. a taxonomic category between an order and a family. 2. Penaeoidea. In addition to 11 new 16S rRNA sequences generated for this study, 18 previously reported sequences (including 3 outgroups) were examined. The phylogenetic phy·lo·ge·net·ic adj. 1. Of or relating to phylogeny or phylogenetics. 2. Relating to or based on evolutionary development or history. relationships estimated through maximum likelihood and neighbor joining methods supported the monophyly of the Superfamily Penaeoidea. Other findings, challenge our current classification schemes of the superfamily, and are presented as hypothesis for future work: the paraphyly of Penaeidae family and its close relationship to Solenoceridae; the close association between Aristeidae, Benthesicymidae and Sicyioniidae questions their erection as separated families. KEY WORDS: molecular phylogeny Molecular phylogeny is the use of the structure of molecules to gain information on an organism's evolutionary relationships. The result of a molecular phylogenetic analysis is expressed in a so-called phylogenetic tree. Every living organism contains DNA, RNA, and proteins. , 16S, mitochondrial DNA, Dendrobranchiata, Penaeoidea, shrimp INTRODUCTION Penaeoids shrimp of the Superfamily Penaeoidea Rafinesque-Schmaltz, 1815, are a diverse and abundant group with more than 400 species currently recognized within 49 genera representing 5 families: Aristeidae, Wood-Mason 1891; Benthesicymidae, Wood-Mason 1891; Penaeidae, Rafinesque-Schmaltz 1815; Sicyoniidae, Ortmann 1898; and Solenoceridae, Wood-Mason 1891. Members of Penaeidae and Sicyoniidae are predominantly found in littoral littoral /lit·to·ral/ (lit´ah-r'l) pertaining to the shore of a large body of water. littoral pertaining to the shore. water and include most of the shrimp commercially caught around the world in tropical and subtropical sub·trop·i·cal adj. Of, relating to, or being the geographic areas adjacent to the Tropics. subtropical Adjective of the region lying between the tropics and temperate lands areas, whereas Aristeidae, Benthesicymidae, and Solenoceridae are either deep benthic ben·thos n. 1. The collection of organisms living on or in sea or lake bottoms. 2. The bottom of a sea or lake. [Greek. dwellers or members of the meso- and bathypelagic-fauna. Penaeoids shrimp show a diverse and complex morphology (i.e., the male and female genitalia genitalia /gen·i·ta·lia/ (jen?i-tal´e-ah) [L.] the reproductive organs. ambiguous genitalia ), which have been recently reviewed by Perez-Farfante and Kensley (1997). The presence of a nauplius nau·pli·us n. pl. nau·pli·i The free-swimming first stage of the larva of certain crustaceans, having an unsegmented body with three pairs of appendages and a single median eye. larval stage as well as the fossil record that placed penaeoids as the most basal group within decapods originated in the Permic-Triasic (Felgenhauer & Abele 1983) or in the Carboniferous (Schram 1977, Schram 1982, Dall et al. 1990). One hypothesis on the evolutionary relationships within Penanoidea has been advanced (Burkenroad 1983), posing an Aeger-like organism as the common ancestor of all penaeoids, from which 2 branches arose: one early diverging branch leading to peneids and sicyoniids, and a later emerging group resulting in the modern solenocerids, aristeids, and benthesicymids. In spite of their commercial, ecological, evolutionary, and taxonomical significance, no attempts have been made to elucidate the phylogeny of Superfamily Penaeoidea. A number of molecular studies have been carried out on the phylogeny and population genetics Population genetics The study of both experimental and theoretical consequences of mendelian heredity on the population level, in contradistinction to classical genetics which deals with the offspring of specified parents on the familial level. of Penaeidae (e.g., Bauer 1986, Bauer 1991, Palumbi & Benzie 1991, Machado et al. 1993, Bouchon et a1.1994, Garcia et al. 1996, Baldwin et al. 1998, Ball et al. 1998, Tassanakajon et al. 1998, Tong et al. 2000, Chu et al. 2003). Other four families have not been approached through molecular phylogenetics phy·lo·ge·net·ics n. The study of phylogeny. . This study is the first attempt to contribute a preliminary molecular phylogeny for the Superfamily Penaeoidea through analysis of partial sequences of 16S rRNA mitochondrial mitochondrial pertaining to mitochondria. mitochondrial RNAs a unique set of tRNAs, mRNAs, rRNAs, transcribed from mitochondrial DNA by a mitochondrial-specific RNA polymerase, that account for about 4% of the total cell RNA that genes. MATERIAL AND METHODS Collection of Specimens Eleven species representing the 5 families of Superfamily Penaeoidea that were included in the study: Aristeus antillensis, Milne Edwards and Bouvier Bouvier refers to several things:
tr.v. bat·ed, bat·ing, bates 1. To lessen the force or intensity of; moderate: "To his dying day he bated his breath a little when he told the story" 1881 (collected during the oceanographic cruise BATO BATO Batman and the Outsiders (comic) BATO Balloon Assisted Take-Off , Biota de los Arrecifes de la Plataforma y Talud continental en el noroeste del Banco de Campeche, Golfo de Mexico Noun 1. Golfo de Mexico - an arm of the Atlantic to the south of the United States and to the east of Mexico Gulf of Mexico Atlantic, Atlantic Ocean - the 2nd largest ocean; separates North and South America on the west from Europe and Africa on the east ); Sicyonia burkenroadi, Cobb 1971; Sicyonia dorsalis, Kingsley 1878; Sicyonia brevirostris, Stimpson 1871; Farfantepenaeus duorarum (Burkenroad 1939); Litopenaeus setiferus (Linnaeus 1767); and Solenocera vioscai, Burkenroad 1934 were caught during the oceanographic cruise SGM-6 (Banco y Sonda de Campeche, Golfo de Mrxico), both cruises were carried on board the R/V R/V Research Vessel R/V Aerial Rendezvous R/V Record Primary/Voice Alternate Justo Sierra (Instituto de Ciencias del Mar y Limnologfa, UNAM). Gennadas sp., and Bentheogennema intermedia Intermedia - A hypertext system developed by a research group at IRIS (Brown University). (Bate 1888), were collected during the oceanographic cruise DgoMB (Deep Gulf of Mexico Noun 1. Gulf of Mexico - an arm of the Atlantic to the south of the United States and to the east of Mexico Golfo de Mexico Atlantic, Atlantic Ocean - the 2nd largest ocean; separates North and South America on the west from Europe and Africa on the east Benthos benthos: see marine biology. Study), carried on board the R/V GYRE gyre: see ocean. (Texas A & M, University), and identified by M. Wickstein. All samples consisted of a piece of pleopod (70-80 mg) preserved either in 70% ethanol or in liquid nitrogen. DNA DNA: see nucleic acid. DNA or deoxyribonucleic acid One of two types of nucleic acid (the other is RNA); a complex organic compound found in all living cells and many viruses. It is the chemical substance of genes. Isolation and Amplification DNA extractions were carried out using the Blood & Cell Culture DNA Mini Kit (Qiagen), following the instruction from the manufacturer. A 418-bp fragment of the 16 s gene was amplified through polymerase chain reaction polymerase chain reaction (pŏl`ĭmərās') (PCR), laboratory process in which a particular DNA segment from a mixture of DNA chains is rapidly replicated, producing a large, readily analyzed sample of a piece of DNA; the process is performed in a BioRad Mastercycler Gradient. The 50-[micro]1 reaction mixture contained: 0.2 mM each dNTP (Gibbco BRL BRL In currencies, this is the abbreviation for the Brazilian Real. Notes: The currency market, also known as the Foreign Exchange market, is the largest financial market in the world, with a daily average volume of over US $1 trillion. ), x1 Amplification Buffer (Invitrogen), 1 mMgS[O.sub.4] (Invitrogen), 1 [micro]M each primer (Invitrogen), 0.5 unit Platinum Pfx DNA Polymerase DNA polymerase /DNA po·lym·er·ase/ (pah-lim´er-as) any of various enzymes catalyzing the template-directed incorporation of deoxyribonucleotides into a DNA chain, particularly one using a DNA template. (Invitrogen), and 80-100 ng template DNA (undiluted or diluted 10-20 x in dd[H.sub.2]0. Two primers were developed for this study and used to amplify the homologous homologous /ho·mol·o·gous/ (ho-mol´ah-gus) 1. corresponding in structure, position, origin, etc. 2. allogeneic. ho·mol·o·gous adj. 1. 3' end of 16S mitochondrial region: Forward E 5'TAGAGAATTCGACCGTGCGAAGGTAGC-3'; Reverse X 5'TTGAGAGCTCATTCAACATCGAGGTGGC-3'. These primers contained EcoRI and XhoI sites, respectively, to facilitate ligation ligation /li·ga·tion/ (li-ga´shun) the application of a ligature. tubal ligation sterilization of the female by constricting, severing, or crushing the uterine tubes. into standard plasmids for sequencing, although, in this report all sequencing was carried out from PCR PCR polymerase chain reaction. PCR abbr. polymerase chain reaction Polymerase chain reaction (PCR) products. Cycling conditions were: 94[degrees]C/4 min initial denaturing step followed by 30 cycles of 94[degrees]C/1 min, 45 to 55[degrees]C/1 min, 72[degrees]C/1 min, and final extension step of 72[degrees]C/10 min. Doubled-stranded PCR products were purified from gel (Montage DNA Gel Extraction Kit, Millipore) or directly from the PCR reaction mixture (Microcon-PCR Filter Unit, Millipore). Purified PCR products (10 [micro]l) were sequenced in both directions using the ABI- Big Dye-Terminator Sequencing Kit (Applied Biosystem Inc.) under manufacturer-recommended reaction conditions. Sequence Analysis All nucleotide sequences were aligned using Clustal W 1.5 c (Thompson et al. 1994) and then manually adjusted. Phylogenetic analysis was initially carried out with PAU[P.sup.*] 4.10 (Swofford 2003). To determine which model of sequence evolution best fitted the data set, a nested likelihood ratio test was performed using Modeltest program version 3.0 (Posada po·sa·da n. A Christmas festival originating in Latin America that dramatizes the search of Joseph and Mary for lodging. [American Spanish, from Spanish, lodging, from posar, & Crandall 1998). After the evolution model was determined, phylogenetic relationships were inferred using maximum likelihood (Felsenstein 1981). Fifty random taxon taxon (pl. taxa), in biology, a term used to denote any group or rank in the classification of organisms, e.g., class, order, family. addition heuristic A method of problem solving using exploration and trial and error methods. Heuristic program design provides a framework for solving the problem in contrast with a fixed set of rules (algorithmic) that cannot vary. 1. searches with tree bisection-reconnection branch swapping were conducted. To support the relationships among the taxa taxa: see taxon. 100 bootstrap See boot. (operating system, compiler) bootstrap - To load and initialise the operating system on a computer. Normally abbreviated to "boot". From the curious expression "to pull oneself up by one's bootstraps", one of the legendary feats of Baron von Munchhausen. searches were performed (Felsenstein 1985). Figure was prepared in part using the programs RETREE and DRAWGRAM from PHYLIP PHYLIP Phylogeny Inference Package (genetics software) (Felsenstein 1999). Phylogenetic relationships were also estimated using neighbor-joining (NJ) analysis (Saitou & Nei 1987). NJ analysis was performed using Jukes-Cantor and pair-wise deletion options (MEGA 2.0, Kumar et al. 1993). Boot-strapping (1000 replicates) was performed to assess the confidence level at each branch. RESULTS In addition to 11 new mitochondrial 16S partial sequences generated for this study, another 15 partial sequences from 5 different Penaeoidea families, and 3 outgroup taxa were also included. Our dataset consisted of 29 sequences, 303-374 bp long. New sequences have been deposited in GenBank under accession numbers shown in Table 1. Aligned sequences were considerably AT-rich (75%). Base composition was A = 0.37, C = 0.026, G = 0.17, and T = 0.38. The average distance in all Penaeoidea species was 0.137 [+ or -] 0.12 and ranged from 0.001 between Sicyonia dorsalis and Aristaeopsis edwardsiana to 0.234 between Aristeus antillensis and Farfantepenaeus duorarum as well as A. antillensis and Litopenaeus setiferus (Table 2). The likelihood ratio test indicated that the model with best fit for the data set was the Hasegawa-Kishino-Yano model (HKY HKY Hickory, NC, USA (Airport Code) ; Hasegawa et al. 1985), with a heterogeneity rate: (+G; Yang 1994); a transition/transversion ratio of 2.1355; a gamma shape parameter of 0.44; and with invariable in·var·i·a·ble adj. Not changing or subject to change; constant. in·var  i·a·bil sites (+I) of 0.2147. Maximum likelihood
analysis using this model yielded two trees with a -1 n likelihood of
2942.592. Differences among both trees were the position of Aristeus
antillensis, Aristaeopsis edwardsiana, and S. dorsalis. Despite the
number of polytomies in the ML tree (Fig. 1), several features can be
observed, being the monophyly of the Penaeoidea superfamily the most
conspicuous, well apart from the 3 outgroup species: Synalpheus
pectiniger, Cataleptodiusfloridanus, and Xantho poressa. Surprisingly,
the Penaeidae family appeared as a paraphyletic paraphyletic Relating to a taxonomic group that includes some but not all of the descendants of a common ancestor. In the traditional taxonomy of vertebrates, where fish are a separate class from the classes of terrestrial vertebrates, the class of fish is assemblage formed by at least 3 clades. Clade A, formed by 9 species within 6 genera (according to Perez-Farfante & Kensley 1997) including the three species of American Farfantepenaeus and the two Litopenaeus species, the Indo-West Pacific Melicertus canaliculatus and Marsupenaeus japonicus, as well as 2 separated species, Penaeus monodon and Fenneropenaeus indicus, which were not resolved in the ML tree, although clearly separated from the other genera. Clade B consisted of 2 Indo-West Pacific species Trachysalambria curvirostris and Parapenaeopsis hardwickii, and the western Atlantic Xiphopenaeus kroyeri. Clade C included Parapenaeus fissurus and Metapenaeopsis barbata from the Indo-West Pacific and Penaeopsis serrata from the western Atlantic, unexpectedly associated with the species of the Solenoceridae family: Solenocera koelbeli and S. crassicornis from the Indo-West Pacific, and S. vioscai from the Western Atlantic. The only species of the Penaeidae family that appeared isolated was Metapenaeus ensis, which showed the highest genetic distances within Penaeidae (see Table 2). Another remarkable feature from the ML tree was the grouping of species belonging to families Sicyoniidae, Benthesicymidae, and Aristeidae in Clade D. Finally, the three outgroup species appeared well separated, with the caridean Synalpheus pectinger as the sister for all Superfamily Penaeoidea. The average genetic distances within each clade was: A = 0.108 [+ or -] 0.011, B = 0.094 [+ or -] 0.012, C = 0.075 [+ or -] 0.010, and D = 0.025 [+ or -] 0.004, whereas the average between 2 clades was: A-B A-B Air-Britain (UK-based aviation historical society) A-B Research Centre Applied Biocatalysis (Graz, Austria) = 0.151 [+ or -] 0.016, A-C A-C Air Conditioning = 0.133 [+ or -] 0.014, A-D A-D Advance-Decline, or measurement of the number of issues trading above their previous closing prices less the number trading below their previous closing prices over a particular period. = 0.191 [+ or -] 0.021, B-C = 0.125 [+ or -] 0.015, B-D B-D Becton, Dickinson & Co. = 0.174 [+ or -] 0.021, and C-D = 0.159 [+ or -] 0.019. [FIGURE 1 OMITTED] The lack of resolution in some branches of the ML tree led us to carry out a NJ analysis. Like the ML, the NJ tree provided evidence supporting the monophyly of Superfamily Penaeoidea, and showed a similar arrangement of species in four clades (Fig. 2). However, in the NJ tree, clades A, C, and D formed a larger assemblage separated from clade B, which was placed as the sister group of all other members in the superfamily. Again, P. fissurus, M. barbata, and P. serrata were closely associated with the species of the Solenoceridae family. M. ensis appeared outside the major grouping of peneids, although in the NJ tree it was related to clade D, formed by the species of families Aristeidae, Benthesicymidae, and Sicyoniidae. Again, the three outgroup species appeared clearly separated from the Penaeoidea. [FIGURE 2 OMITTED] DISCUSSION Despite the limited information to solve the relationships with these partial 16 S sequences, several general considerations emerged from both analyses and might be erected as hypothesis for future work using larger sequence data: (1) The monophyly of Superfamily Penaeoidea; (2) The paraphyly of Penaeidae family and its close relationship to Solenoceridae family; and (3) Aristeidae, Benthesicymidae and Sicyioniidae form a compact group with small genetic distances and might not deserve erection as separated families. The relatively large genetic divergence observed within family Penaeidae (Clades A-C) seems to be in agreement with morphologic traits described long ago (Burkenroad 1936, Burkenroad 1983, Kubbo 1949). Members of clade A showed the greatest mean divergence (0.0108); taken as a natural group, they might be characterized morphologically by the presence of an epipod on third maxilliped max·il·li·ped n. One of the three pairs of crustacean head appendages located just posterior to the maxillae and used in feeding. [maxill(a) + -ped.] , pleurobranchiae on fifth pereiopod, ventral ventral /ven·tral/ (ven´tral) 1. pertaining to the abdomen or to any venter. 2. directed toward or situated on the belly surface; opposite of dorsal. ven·tral adj. and dorsal rostral rostral /ros·tral/ (ros´tral) 1. pertaining to or resembling a rostrum; having a rostrum or beak. 2. situated toward a rostrum or toward the beak (oral and nasal region), which may mean superior (in relationships teeth, as well as by the absence of branchiostegal, pterygostomian and parapenaeid spines, and transverse and longitudinal sutures on carapace carapace (kâr`əpās), shield, or shell covering, found over all or part of the anterior dorsal portion of an animal. In lobsters, shrimps, crayfish, and crabs, the carapace is the part of the exoskeleton that covers the head and thorax . All but the two species of Litopenaeus within clade A, show a symmetrical and semiclosed petasma without distolateral projections, uninvaginated and unpaired seminal receptacles, simple spermatophore sper·mat·o·phore n. A capsule or compact mass of spermatozoa extruded by the males of certain invertebrates and primitive vertebrates and directly transferred to the reproductive parts of the female. without accessories, and thelycum closed with two lateral plates (with the exception of Marsupenaeus, which shows a thelycum with one plate, and spermatophore with accessories). The Litopenaeus species have a semiopen petasma and thelycum without seminal receptacles, and a complex spermatophore with accessories. Our results are in agreement with a previous study based on 16S mitochondrial DNA (Maggioni et al. 2001), proposing similar differentiation between Farfantepenaeus with closed thelycum and semiclosed petasma versus Litopenaeus with open thelycum and semiopen petasma. Clade B formed by Trachysalambria, Parapenaeopsis, and Xiphopenaeus appeared divergent from the other penaeids. They are morphologically different from Clade A by the absence of pleurobranchiae on pereiopods 4 and 5, the lack of epipod on third maxilliped, presence of rostral teeth only on dorsal side, symmetrical and semiclosed petasma with hornlike or spoutlike distolateral projections, closed thelycum with one lateral plate, and the seminal receptacles paired and invaginated. Clade C differs from Clades A and B by the lack of pleurobranchia only on fifth pereiopod and the presence of pterygostomian and parapenaeid spines. However, members of clade C are morphologically similar to those in clade B in several sexual characters: symmetrical and semiclosed petasma with invaginated and paired seminal receptacles, closed thelycum with one plate and simple spermatophore without accessories (except for Metapenaeopsis which shows asymmetric petasma and uninvaginated and unpaired seminal receptacles). Association of family Solenoceridae deserves further attention because the uniqueness of their postorbital post·or·bit·al adj. Situated behind the socket of the eye. spine within Superfamily Penaeoidea. Relationships between solenocerids and penaeoids suggested in our analyses were surprising, although are not without precedent. Burkenroad (1983) proposed that some genera within Solenoceridae (e.g., Haliporus), are closer to Aristeidae (by the presence of appendix interna, the two arthrobranchiae on first maxilliped and the mesial mesial /me·si·al/ (me´ze-al) nearer the center of the dental arch. me·si·al adj. 1. Of, in, near, or toward the middle. 2. tubercle tubercle (t  `bərkyl') [Lat.,=little swelling], small, usually solid, nodule or prominence. on optic calathus cal·a·thus n. pl. cal·a·thi A vase-shaped basket represented in Greek painting and sculpture. [Latin, from Greek kalathos.] ), whereas others (e.g., Solenocera and Pleoticus) resemble Penaeidae by the presence of pterygostomian, brachiostegal and ocular spines, an orbital scale, similar branchial branchial /bran·chi·al/ (brang´ke-al) pertaining to or resembling gills of a fish or derivatives of homologous parts in higher forms. bran·chi·al adj. formula, a semiopen petasma, and an open thelycum. Our results certainly differ from previous systematic studies and might suggest that morphologic characters used to differentiate among families within Superfamily Penaeoidea, have been over-emphasized. Further molecular analyses with larger sequence data and including other genera of Solenoceridae, will be necessary to elucidate the status of this family. The apparently anomalous position of M. ensis within peneids seems to agree with some atypical morphologic characters like the petasma with distolateral projections, the lack of pleurobranchia and exopod on fifth pereiopod, the fifth male pereiopod modified and the presence of basial spine on third maxilliped and pereiopods 2-3. On this respect, previous study using allozyme markers (Tam & Chu 1993) have also revealed considerable genetic differences between Metapenaeus and other subgenera of Penaeus. The largest genetic distance (mean = 0.175), was found between the compact group (Clade D) formed by Sicyoniidae, Benthesicymidae, and Aristeidae and the other penaeoid families. Our results strongly suggest that the 3 families are closely related and separated from families Penaeidae and Solenoceridae, however, the status of each family within Clade D will require further molecular analysis. Aristeidae and Benthesicymidae share a similar branchial formula and presence of a reduced prosartema, but differ in features of the genitalia: A. antillensis and A. edwardsiana show open thelycum and petasma, whereas B. intermedia and Gennadas. sp. have closed petasma and thelycum with invaginated and paired seminal receptacles. Nevertheless, the seminal receptacles and the spermatophores in Benthesicymidae are not homologous with Penaeidae and Sicyoniidae (Burkenroad 1936, Bauer 1986, Bauer 1991). Species of Sicyonia, resemble those of Penaeidae in some genitalia characteristics, whereas with Aristeidae and Benthesicymidae share the lack of exopods in the pereopods 1-5, and absence of the ocular scale. On the other hand, sicyoniids possess morphologic characters that otherwise are unique to Penaeoidea: a single pleurobranchia on the fifth pereiopod, uniramous third to fifth pleopods, lack of exopods in all pereiopods, closed petasma with distal, sclerotized projections, without true spermatopores, and thelycum with lanceolate Lanceolate Narrow, leaf shape that is longer than it is wide, and pointed at the end. Mentioned in: Echinacea median plate. A recent molecular analysis of the phylogenetic relationships of genus Penaeus s.l. based in partial sequences of 16S and Cytochrome oxidase cytochrome oxidase n. An oxidizing enzyme containing iron and a porphyrin, found in mitochondria and important in cell respiration as an agent of electron transfer from certain cytochrome molecules to oxygen molecules. I (COI) is consistent with our results within clade A (Lavery et al. 2004). As indicated earlier, the value of this study is to direct the attention to three major questions about Superfamily Penaeoidea, and in particular, about the status and relationships among families. Additional molecular studies are needed to provide stronger evidence on the evolutionary history within the superfamily.
TABLE 1.
List of the Superfamily Penaeoidea species used in this study.
Zoogeographic GenBank
Distribution Accesion
Family/Species Numbers
Aristeidae
Aristaeopsis edwardsiana * (A. edw) WA, EA, IP AY601734
Aristeus antillensis * (A. ant) WA AY601738
Benthesicymidae
Bentheogennema intermedia * (B. int) WA, EA, EP, IP AY601737
Gennadas sp * (Germ) WA, EP, IP, EA AY601739
Penaeidae
Farfantepenaeus aztecus (F. azt) WA AF279811
Farfantepenaeus brasilliensis (F. bra) WA AF192053
Farfantepenaeus duorarum * (F. duo) WA AY601732
Fenneropenaeus merguiensis (F. mer) EA, IP AF279814
Litopenaeus setiferus * (L. set) WA AY601735
Litopenaeus vannamei (L. van) EP AF279818
Marsupenaeus japonicus (M. jap) IP AF279820
Melicertus canaliculatus (M. can) IP AF279825
Metapenaeopsis barbata (M. bar) IP AY264905
Metapenaeus ensis (M. ens) IP AF279810
Parapenaeopsis hardwickii (P. har) IP AY264910
Parapenaeus fissurus (P. fis) IP AY264909
Penaeopsis serrata * (P. ser) WA, EA AY601733
Penaeus monodon (P. mon) IP AF279829
Trachysalambria curvirostris (T. cur) EA, IP AY264916
Xiphopenaeus kroveri (X. kro) EP, WA AF192092
Solenoceridae
Solenocera crassicornis (S. cra) IP AY264915
Solenocera koelbeli (S. koe) IP AF105038
Solenocera vioscai * (S. vio) WA AY601736
Sicyoniidae
Sicyonia brevirostris * (S. bre) WA, EP AY601742
Sicyonia burkenroadi * (S. bur) WA AY601741
Sicyonia dorsalis * (S. bur) WA AY601740
Outgroups
Synalpheus pectiniger (S. pec) WA AF230259
Cataleptodius floridanus (C. flo) WA AJ274698
Xantho poressa (X. por) WA AJ130814
Abbreviation for the species names are shown in brackets.
* Species sequenced for this work.
WA, Western Atlantic; EA, Eastern Atlantic; EP, Eastern Pacific;
IP, Indo-West Pacific.
TABLE 2. Pairwise mitochondrial 16S sequence divergence for 26
Penaeoidea species and three outgroups. Data were calculated
using Jukes-Cantor distance parameter (MEGA2.0). Abbreviations
for species are shown in Table 1.
C. flo X. por S. pec F. bra L. van
C. flo --
X. por 0.129 --
S. pec 0.290 0.307 --
F. bra 0.287 0.314 0.290 --
L. van 0.281 0.298 0.288 0.100 --
F. azt 0.295 0.328 0.315 0.047 0.088
T. cur 0.253 0.302 0.264 0.129 0.122
P. har 0.266 0.333 0.237 0.173 0.162
P. fis 0.253 0.306 0.280 0.154 0.109
M. ens 0.283 0.305 0.286 0.120 0.159
M. can 0.268 0.304 0.336 0.127 0.126
M. jap 0.277 0.313 0.336 0.094 0.136
F. mer 0.267 0.311 0.282 0.149 0.097
X. kin 0.273 0.310 0.276 0.103 0.144
P. mon 0.280 0.309 0.272 0.067 0.119
F. duo 0.307 0.332 0.285 0.126 0.103
P. ser 0.241 0.297 0.276 0.106 0.097
L. set 0.278 0.306 0.306 0.142 0.070
M. bar 0.261 0.309 0.288 0.134 0.125
S. vio 0.273 0.302 0.309 0.147 0.133
S. koe 0.278 0.310 0.307 0.149 0.139
S. cra 0.281 0.305 0.306 0.210 0.138
A. ant 0.337 0.370 0.371 0.196 0.222
A. edw 0.325 0.357 0.368 0.184 0.212
Gen 0.307 0.335 0.340 0.184 0.198
B. int 0.306 0.326 0.339 0.183 0.198
S. dot 0.298 0.326 0.335 0.181 0.195
S. bur 0.303 0.330 0.335 0.184 0.198
S. bee 0.313 0.341 0.335 0.192 0.187
F. azt T. cur P. har P. fis M. ens
C. flo
X. por
S. pec
F. bra
L. van
F. azt --
T. cur 0.119 --
P. har 0.172 0.079 --
P. fis 0.135 0.067 0.107 --
M. ens 0.166 0.097 0.120 0.115 --
M. can 0.126 0.119 0.148 0.126 0.149
M. jap 0.133 0.119 0.155 0.123 0.152
F. mer 0.103 0.124 0.142 0.109 0.146
X. kin 0.141 0.047 0.094 0.094 0.126
P. mon 0.124 0.102 0.126 0.106 0.136
F. duo 0.055 0.118 0.175 0.128 0.166
P. ser 0.119 0.082 0.119 0.047 0.132
L. set 0.111 0.150 0.182 0.125 0.166
M. bar 0.132 0.100 0.138 0.058 0.141
S. vio 0.140 0.113 0.143 0.101 0.127
S. koe 0.152 0.122 0.148 0.082 0.138
S. cra 0.155 0.125 0.148 0.081 0.141
A. ant 0.226 0.142 0.197 0.159 0.169
A. edw 0.216 0.132 0.188 0.152 0.153
Gen 0.201 0.132 0.178 0.147 0.151
B. int 0.194 0.129 0.175 0.143 0.144
S. dot 0.198 0.129 0.175 0.143 0.144
S. bur 0.201 0.132 0.178 0.147 0.148
S. bee 0.205 0.150 0.193 0.157 0.155
M. can M. jap F. mer X. kro P. mon
C. flo
X. por
S. pec
F. bra
L. van
F. azt
T. cur
P. har
P. fis
M. ens
M. can --
M. jap 0.017 --
F. mer 0.011 0.109 --
X. kin 0.136 0.143 0.141 --
P. mon 0.118 0.112 0.078 0.134 --
F. duo 0.136 0.132 0.121 0.138 0.124
P. ser 0.116 0.126 0.100 0.100 0.112
L. set 0.157 0.164 0.105 0.164 0.127
M. bar 0.143 0.154 0.125 0.118 0.128
S. vio 0.124 0.127 0.136 0.123 0.123
S. koe 0.148 0.144 0.129 0.135 0.126
S. cra 0.151 0.147 0.128 0.134 0.125
A. ant 0.207 0.198 0.186 0.175 0.156
A. edw 0.193 0.185 0.173 0.164 0.145
Gen 0.197 0.189 0.165 0.163 0.140
B. int 0.189 0.181 0.161 0.156 0.136
S. dot 0.189 0.181 0.161 0.160 0.136
S. bur 0.193 0.185 0.165 0.163 0.140
S. bee 0.201 0.193 0.157 0.171 0.147
F. duo P. ser L. set M. bar S. vio
C. flo
X. por
S. pec
F. bra
L. van
F. azt
T. cur
P. har
P. fis
M. ens
M. can
M. jap
F. mer
X. kin
P. mon
F. duo --
P. ser 0.128 --
L. set 0.123 0.115 --
M. bar 0.154 0.061 0.141 --
S. vio 0.129 0.073 0.156 0.104 --
S. koe 0.155 0.093 0.148 0.100 0.062
S. cra 0.158 0.096 0.148 0.099 0.065
A. ant 0.234 0.163 0.234 0.176 0.176
A. edw 0.224 0.156 0.228 0.169 0.169
Gen 0.208 0.150 0.212 0.161 0.161
B. int 0.201 0.147 0.208 0.157 0.154
S. dot 0.204 0.147 0.208 0.157 0.157
S. bur 0.208 0.150 0.212 0.161 0.161
S. bee 0.208 0.154 0.216 0.162 0.154
S. koe S. cra A. ant A. edw Gen
C. flo
X. por
S. pec
F. bra
L. van
F. azt
T. cur
P. har
P. fis
M. ens
M. can
M. jap
F. mer
X. kin
P. mon
F. duo
P. ser
L. set
M. bar
S. vio
S. koe --
S. cra 0.003 --
A. ant 0.172 0.176 --
A. edw 0.165 0.168 0.007 --
Gen 0.161 0.164 0.017 0.010 --
B. int 0.157 0.157 0.010 0.003 0.011
S. dot 0.157 0.160 0.007 0.000 0.011
S. bur 0.161 0.164 0.010 0.003 0.014
S. bee 0.165 0.165 0.077 0.067 0.068
B. int S. dor S. bur S. bre
C. flo
X. por
S. pec
F. bra
L. van
F. azt
T. cur
P. har
P. fis
M. ens
M. can
M. jap
F. mer
X. kin
P. mon
F. duo
P. ser
L. set
M. bar
S. vio
S. koe
S. cra
A. ant
A. edw
Gen
B. int --
S. dot 0.006 --
S. bur 0.008 0.008 --
S. bee 0.062 0.062 0.065 --
ACKNOWLEDGMENTS The authors thank P. de la Torre, A. Gomez, and C. Padilla for the technical support and field work. Special gratitude is extended to D. Pinero for kindly introducing me to Molecular Biology molecular biology, scientific study of the molecular basis of life processes, including cellular respiration, excretion, and reproduction. The term molecular biology was coined in 1938 by Warren Weaver, then director of the natural sciences program at the Rockefeller Research (A. R. V. B). This work was partially supported by research grants from CONACYT CONACYT Consejo Nacional de Ciencia y Tecnología (National Board of Science and Technology; Mexico, Bolivia, Paraguay) (41693-M: J. P. L. and J. C. C.), DGAPA UNAM (IN206102-3: J.P.L. and J. C. C.) and Fundaci6n Miguel Aleman, A.C. (J. P. L.). LITERATURE CITED Baldwin, J. D., A. L. Bass, B. W. Bowen & W. H. Clark, Jr. 1998. Molecular Phylogeny and biogeography Biogeography A synthetic discipline that describes the distributions of living and fossil species of plants and animals across the Earth's surface as consequences of ecological and evolutionary processes. of the marine shrimp Penaeus. Mol. Phylogenet. Evol. 10:399-407. Ball, A. O., S. Leonard & R. W. Chapman. 1998. Characterization of [(GT).sub.n] microsatellites from native white shrimp (Penaeus setiferus). Mol. Ecol. 7:1251-1253. Bate, C. S. 1888. Report on the scientific results of the voyage of Challenger during the years 1873-76. H. M. Stationery, Edinburgh. 24:1-942. Bauer, R. T. 1986. Phylogenetic trends in sperm transfer and storage complexity in decapod decapod (dĕk`əpŏd') (Gr.,=10 feet), name for invertebrate animals of the crustacean order Decapoda (phylum Arthropoda) including the crabs, the lobsters and crayfish, and the true shrimps, all having five pairs of legs. crustaceans. J. Crust. Biol. 6:313-325. Bauer, R. T. 1991. Sperm transfer and storage structures in penaeoid shrimps: functional and phylogenetic perspective. In: R.T. Bauer, J. W. Martin, editors. Crustacean crustacean (krŭstā`shən), primarily aquatic arthropod of the subphylum Crustacea. Most of the 44,000 crustacean species are marine, but there are many freshwater forms. sexual biology. New York New York, state, United States New York, Middle Atlantic state of the United States. It is bordered by Vermont, Massachusetts, Connecticut, and the Atlantic Ocean (E), New Jersey and Pennsylvania (S), Lakes Erie and Ontario and the Canadian province of : Columbia University Press Columbia University Press is an academic press based in New York City and affiliated with Columbia University. It is currently directed by James D. Jordan (2004-present) and publishes titles in the humanities and sciences, including the fields of literary and cultural studies, . pp. 183-207. Bouchon, D., C. Souty-Grosset & R. Raimond. 1994. Mitochondrial DNA variation and markers of species identity in two penaeid shrimp species: Penaeus monodon Fabricius and P. japonicus Bate. Aquaculture aquaculture, the raising and harvesting of fresh- and saltwater plants and animals. The most economically important form of aquaculture is fish farming, an industry that accounts for an ever increasing share of world fisheries production. 127:131-144. Burkenroad, M. D. 1936. The Aristeinae, Solenocerinae and pelagic pelagic living in the middle or near the surface of large bodies of water such as lakes or oceans. Penaeinae of the Bingham oceanographic collection. Bull. Bingham Oceanogr. Coll. 5:1-151. Burkenroad, M. D. 1939. Further observations on Penaeidae on the northern Gulf of Mexico. Bull. Bingham Oceanogr. Coll. 6:1-162. Burkenroad, M. D. 1983. Natural classification of Dendrobranchiata, with a key to recent genera. Crustacean Issues 3:279-290. Chu, K. H., C. P. Li, Y. K. Tam & S. Lavery. 2003. Application of mitochondrial control region in population genetic studies of the shrimp Penaeus. Mol. Ecol. Notes 3:120-122. Cobb, S. P. 1971. A new species of Sicyonia (Decapoda, Penaeidae) from the western Atlantic with notes on S. stimpsoni Bouvier. Crustaceana 20:104-112. Dall, W., B. J. Hill, P. C. Rothlisberg & D. J. Staples. 1990. The Biology of Penaeidae. Adv. Mar. Biol. 27:1-484. Felgenhauer, B. E. & L. G. Abele. 1983. Phylogenetic relationships among shrimp-like decapods. In: F. R. Schram, editor. Crustacean phylogeny. Crustacean Issues 1. London: Academic Press. pp. 291-311. Felsenstein, J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17:368-376. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using bootstrap. Evolution 39:783-791. Felsenstein, J. 1999. PHYLIP (phylogeny inference package), version 3.572c. Seattle: University of Washington. Garcia, D. K., A. K. Dhar & A. Alcivar-Warren. 1996. Molecular analysis of a RAPD RAPD Randomly Amplified Polymorphic DNA RAPD relative afferent pupillary defect (ophthalmology; aka Marcus-Gunn Pupil) marker (B20) reveals two microsatellites and differential mRNA expression in Penaeus vannamei. Mol. Mar. Biol. Biotech. 5:71-83. Hasegawa, M. K., K. Kishino & T. Yano. 1985. Dating the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22:160-174. Johnson, J. Y. 1867. Descriptions of a new genus and new species of macrurous Ma`cru´rous a. 1. (Zool.) Of or pertaining to the Macrura; having a long tail. decapod Crustaceans belonging to the Penaeidae, discovered at Madeira. Proc. Biol. Zool. Soc. Lon. 1867:895-901. Kingsley, J. S. 1878. Notes on the North American North American named after North America. North American blastomycosis see North American blastomycosis. North American cattle tick see boophilusannulatus. Caridea in the museum of the Peabody Academy of Science at Salem. Mass. Proc. Acad. Nat. Sci. Philadelphia 30:89-98. Kubbo, I. 1949. Studies on Penaeids of Japanese and its Adjacent Waters. J. Tokyo Coll. Fish. 36:1-467. Kumar, S., K. Tamura & M. Nei. 1993. Molecular evolutionary genetics analysis (MEGA), version 1.01. University Park: Pennsylvania State University Pennsylvania State University, main campus at University Park, State College; land-grant and state supported; coeducational; chartered 1855, opened 1859 as Farmers' High School. . Lavery, S., T. Y. Chan, Y. K. Tam & K. H. Chu. 2004. Phylogenetic relationships and evolutionary history of the shrimp genus Penaeus s.l derived from mitochondrial DNA. Mol. Phylogenet. Evol. 31:39-49. Linnaeus, C. 1767. Systema naturae per regna tria naturae, secuudum classes, ordines or·di·nes n. A plural of ordo. , genera, species, cum characteribus, differeniis, synonymis, locis. L. Salvii, Holmiae. 12th ed. 1056 pp. Machado, E. G., N. Dennebuoy, M. O. Suarez, J. C. Mounolou & M. Monnerot. 1993. Mitochondrial 16S-rRNA gene for two species of shrimps: sequence variability and secondary structure. Crustaceana 65:279-286. Maggioni, R., A. D. Rogers, N. MacLean & F. D'Incao. 2001. Molecular phylogeny of western Farfantenaeus and Litopenaeus shrimp based on mitochondrial 16S Partial Sequences. Mol. Phylogenet. Evol. 18:66-73. Milne Edwards, A. & E. L. Bouvier. 1909. Reports on the results of dredging, under the supervision of Alexander Agassiz, in the Gulf of Mexico (1878-79), and along the Atlantic coast of the United States (1880), by the US Coast Survey Steamer Blake, Lieut.-Com. Sigsbee, C.D., U.S.N., and Commander Bartlett, J.R., U.S.N., commanding. 44. Les Peneides et Stenopides. Mem. Mus. Comp. Zool. Harvard College 27:177-274. Ortmann, A. 1898. Gliederfussler: Arthropoda. Bronns Klassen und Ordnungen des Tierreichs 5:1057-1168. Palumbi, S. R. & J. Benzie. 1991. Large mitochondrial differences between morphologically similar Penaeid shrimp. Mol. Mar. Biol. Biotech. 1: 27-34. Perez-Farfante, I. & B. F. Kensley. 1997. Penaeoid and Sergestoid shrimps and prawns of the world: keys and diagnoses for the families and genera. Bulletin du Museum national d'Histotoire naturelle. Paris 175: 1-233. Posada, D. & K. A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818. Rafinesque-Schmaltz, C. S. 1815. Analyse de la nature ou tableau de Iunivers et des corps organises. Palermo. 224 pp. Saitou, N. & M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425. Schram, F. R. 1977. Paleozoogeography of late paleozoic and triasic malacostraca. Paleontology paleontology (pā'lēəntŏl`əjē) [Gr.,= study of early beings], science of the life of past geologic periods based on fossil remains. 55:126-137. Schram, F. R. 1982. The fossil record and evolution of Crustacea. In: L. G. Abele & D. E. Bliss, editors. "The biology of crustacea (1). Systematics systematics: see classification. , the fossil record and biogeography". London: Academic Press. pp. 93-147. Stimpson, W. 1871. Notes on North American crustacea, in the Museum of the Smithsonian Institution. No. III. Ann. Lyc. Nat. Hist. N.Y. 10:92-136. Swofford, D. L. 2003. Phylogenetic analysis using parsimony par·si·mo·ny n. 1. Unusual or excessive frugality; extreme economy or stinginess. 2. Adoption of the simplest assumption in the formulation of a theory or in the interpretation of data, especially in accordance with the rule of (PAUP PAUP Phylogenetic Analysis Using Parsimony ). Version 4.0. Sunderland, MA: Sinauer Associates. Tam, K. Y. & K. H. Chu. 1993. Electrophoretic Study on the Phylogenetic Relationships of some species of Penaeus and Metapenaeus (Decapoda: Penaeidae), from the South China Sea. J. Crust. Biol. 13:697-705. Tassanakajon, A., A. Tiptazwonnukul, P. Supungul, V. Rimphanitchayakit, D. Cook, P. Jarayabhand, S. Klinbunga & V. Boonsaeng. 1998. Isolation and characterization of microsatellites markers in the black tiger prawn prawn: see shrimp. Penaeus monodon. Mol. Mar. Biol. Biotech. 7:55-61. Thompson, J. D., D. G. Higgins & T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment A multiple sequence alignment (MSA) is a sequence alignment of three or more biological sequences, generally protein, DNA, or RNA. In general, the input set of query sequences are assumed to have an evolutionary relationship by which they share a lineage and are descended from a through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Nucleic acids The cellular molecules DNA and RNA that act as coded instructions for the production of proteins and are copied for transmission of inherited traits. Res. 22:4673-4680. Tong, J. G., T. Y. Chan& K. H. Chu. 2000. A preliminary phylogenetic analysis of Metapenaeopsis (Decapoda: Penaeidae) based on mitochondrial DNA sequences of selected species from the Indo-West Pacific. J. Crust. Biol. 20:541-549. Yang, Z. 1994. Estimating the pattern of nucleotide substitution. J. Mol. Evol. 39:105-111. Wood-Mason, J. 1891. Phylum phylum, in taxonomy: see classification. Appendiculata. Branch Arthropoda. Class Crustacea. In: Wood-Masson, J., Alcock, A. Natural History notes from H.M. Indian survey steamer Investigator, Commander R.F. Hoskyn, R.N., commanding Series II, No. 1. On the results of deep-sea dredging during the season 1890-1891. Ann. Mag. Nat. Hist. 6:269-286. ANA R. VAZQUEZ-BADER, (1) JULIO C. CARRERO, (2) MARTIN GARCIA-VARELA, (2) ADOLFO GRACIA (1) * AND JUAN P. LACLETTE (2) * Corresponding author. E-mail: gracia@mar.icmyl.unam.mx (1) Dept. of Marine Ecology, Instituto de Ciencias del Mar y Limnologia UNAM, A. P. 70305, 04510 Mexico, D.F. Mexico; (2) Dept. of Immunology, Instituto de Investigaciones Biomedicas, UNAM, 04510 Mexico D.F., Mexico. |
|
||||||||||||||||
Printer friendly
Cite/link
Email
Feedback
Reader Opinion